DIETARY INTAKE AND FOOD CRAVING
DURING NORMAL MENSTRUAL CYCLING
A thesis submitted to the Kent State University
College of Education, Health, and Human Services
in partial fulfillment of the requirements
for the degree of Masters of Science
By
Amal Albeshri
December 2015
©Copyright, 2015 by Amal Al-Beshri
All Rights Reserved
ii
Thesis written by
Amal Al-Beshri
B.S., King Saud University, 2006
M.S., Kent State University, 2015
Approved by
______________________________, Director, Master's Thesis Committee
Natalie Caine-Bish
______________________________, Member, Master's Thesis Committee
Karen Gordon
______________________________, Member Master's Thesis Committee
Tanya Flacone
Accepted by
______________________________, Director, School of Health Science
Lynne Rowan
______________________________, Dean, College and Graduate School of
Mark Kretovics
Education, Health and Human Sciences
iii
ALBESHRI, AMAL K., M.S., December 2015
Nutrition and Dietetics
DIETARY INTAKE AND FOOD CRAVING DURING NORMAL MENSTRUAL
CYCLING (165 pp.)
Director of Thesis: Natalie Caine-Bish, Ph.D., R.D., L.D.
The purpose of this study was to measure dietary changes and food craving
between different phases of the menstrual cycle in normal menstruating women attending
Kent State University in Kent Ohio. It was hypothesized that there is a change in dietary
intake during the menstrual cycle, and women experience food cravings during the
menstrual cycle. Data collection was divided into two main stages. First, the pre
assessment stage where data from (N=60) women were collected using online survey that
contains four sections: Health History Questionnaire, Eating Attitude Test-26 (EAT-26),
The Mental and Physical Symptom Daily Rating Scale, and Food craving questionnaire.
Based on the result of the first stage, eligible participants were allowed to continue to the
second stage, the assessment phase (n=18), where the cycle was divided into three mail
phases (menstrual, follicular, ad luteal) and six measurement methods were used: The
menstrual cycle tracking record, the ovulation test to measure Luteinizing hormone (LH)
surge, Food Record, Craving Screening, Food Craving Record, Mental and Physical
Symptom Daily Rating Scale. The data was entered by the Kent State University
Research Bureau using the social science (SPSS, version21) and significant level of
(p≤0.05). Statistical methods included descriptive statistics, Simple Analysis of Variance
(ANOVA), and Repeated Measures Analysis of Variance (RM ANOVA). Result: there
were no significant differences in dietary intake, energy and macronutrients
(carbohydrate, protein, and fat), during the three phases of the normal menstrual cycle.
On the other hand, food cravings results indicated that food craving exists during
menstrual cycle in normal menstruating women, during the three phases, and was not
significantly related to specific phase. Further studies are needed to examine the dietary
behaviors of women during different phases of the cycle. The type of the craved foods
needs to be analyzed and measured in correlation with the severity of food restriction.
ACKNOWLEDGMENTS
I would like to express my gratitude to my committee chair, Dr. Natalie CaineBish, and to my committee members Dr. Karen Gordon and Tanya Falcone.
Dr. Natalie Caine-Bish, thank you for your support throughout my graduate study
and for your motivation and guidance in every step of this thesis. Dr. Karen Gordon,
thank you for providing valuable suggestions and comments to improve the content of
this thesis. Tanya Falcone, thank you for providing feedback for my thesis. Also, thank
you for assisting me in recruiting participants, and in analyzing the food records.
My deepest gratitude to all my family and friends who helped me throughout my
graduate school journey. My parents Fayza and Khudher, my sister Emtinan, and my
husband Abdulazim, thank you for your endless support and encouragement. My
daughters Ward and Noor, thank you for bringing the light and joy into my life.
Lastly, I would like to thank Mr. Edward Bolden from the Kent State Research
and Evaluation Bureau for his assistance in analyzing the data and interpreting the results.
Also, my biggest thanks go to all the participants for taking from their valuable time to
participate in this study and for their commitment to complete all required measurements.
iv
TABLE OF CONTENTS
ACKNOWLEDGMENTS ................................................................................................. iv
LIST OF FIGURES ......................................................................................................... viii
LIST OF TABLES ............................................................................................................. ix
CHAPTER
Page
I.
INTRODUCTION ......................................................................................................1
Problem Statement ......................................................................................................3
Purpose Statement ......................................................................................................5
Hypothesis...................................................................................................................5
Operational Definitions ...............................................................................................5
II.
REVIEW OF LITERATURE .....................................................................................6
Menstrual Cycle ..........................................................................................................6
Menarche.....................................................................................................................7
Menstrual Cycle Phases ..............................................................................................9
Follicular Phase .....................................................................................................9
Luteal Phase ........................................................................................................12
Menstrual Phase ..................................................................................................15
Hormonal Changes during Menstrual Cycle.............................................................18
Estrogen ..............................................................................................................20
Progesterone ........................................................................................................21
Follicle Stimulating Hormone (FSH)..................................................................23
Luteinizing Hormone (LH) .................................................................................25
Polycystic Ovarian Syndrome.............................................................................27
Endometriosis .....................................................................................................28
Factors Affecting Menstrual Cycle ...........................................................................30
Physiological Factors ..........................................................................................30
Environmental Factors ........................................................................................31
Alcohol ..........................................................................................................31
Caffeine .........................................................................................................32
Smoking ........................................................................................................32
Physical activity ............................................................................................33
Oral contraceptives .......................................................................................34
Psychological Factors .........................................................................................35
Stress .............................................................................................................35
Depression.....................................................................................................36
Eating disorders ............................................................................................36
v
TABLE OF CONTENTS (Continued)
CHAPTER
Page
Dietary Changes during Menstrual Cycle .................................................................38
Metabolism .........................................................................................................38
Dietary Intake......................................................................................................39
Appetite and Menstrual Cycle ............................................................................41
Food Craving ......................................................................................................42
Types of cravings ..........................................................................................43
Causes of food craving..................................................................................44
Food craving during menstrual cycle ............................................................45
Premenstrual Syndrome (PMS) ................................................................................47
III.
METHODOLOGY ...................................................................................................49
Purpose......................................................................................................................49
Design .......................................................................................................................49
Subjects .....................................................................................................................49
Instruments of Measure.............................................................................................50
Pre Assessment Phase .........................................................................................50
Assessment Phase ...............................................................................................52
Procedure ..................................................................................................................54
Data Analysis ............................................................................................................56
Pre Assessment Phase ........................................................................................56
Assessment Phase ..............................................................................................57
IV. JOURNAL ARTICLE ..............................................................................................59
Introduction ...............................................................................................................59
Methodology .............................................................................................................61
Design .................................................................................................................61
Participants ..........................................................................................................61
Measures .............................................................................................................62
Pre assessment phase ....................................................................................62
Assessment phase..........................................................................................63
Procedure ............................................................................................................66
Pre assessment phase ...................................................................................66
Assessment phase .........................................................................................66
Data Analysis ............................................................................................................68
Pre Assessment Phase .........................................................................................68
Assessment Phase ...............................................................................................69
vi
TABLE OF CONTENTS (Continued)
CHAPTER
Page
Results .......................................................................................................................71
Pre Assessement Phase ......................................................................................71
Assessment Phase ...............................................................................................76
Eligible participants' characteristics ..............................................................76
Food record ..................................................................................................77
Food craving record ......................................................................................80
Discussion .................................................................................................................83
Dietary Intake During the Menstrual Cycle ........................................................83
Food Craving During the Menstrual Cycle ........................................................84
Dietary Restriction During the Menstrual Cycle ................................................85
Application................................................................................................................88
Limitations ................................................................................................................92
Strengths ...................................................................................................................93
Conclusion ................................................................................................................93
APPENDICES ...................................................................................................................95
APPENDIX A. CONSENT FORM ..........................................................................96
APPENDIX B. HEALTH HISTORY QUESTIONNAIRE ....................................100
APPENDIX C. EATING ATTITUDE TEST-26 (EAT-26) ...................................103
APPENDIX D. THE MENTAL AND PHYSICAL SYMPTOM
DAILY RATING SCALE ................................................................................106
APPENDIX E. FOOD CRAVING HISTORY QUESTIONNAIRE......................109
APPENDIX F. THE MENSTRUAL CYCLE TRACKING RECORD .................113
APPENDIX G. FOOD RECORD ...........................................................................116
APPENDIX H. PART A. FOOD CRAVING RECORD .......................................118
APPENDIX I. THE FLOW OF THE 3 PHASES OF THE CYCLE
(OVERVIEW OF THE ASSESSMENT PHASE PROCESS) .........................123
APPENDIX J. KSU IRB PERMISSION ................................................................125
REFERENCES ................................................................................................................128
vii
LIST OF FIGURES
Figure
Page
1.
Menstrual cycle phases .............................................................................................17
2.
The reproductive axis in menstrual cycle .................................................................19
viii
LIST OF TABLES
Table
Page
1
Female Participant Delographics Characteristics (Age, Weight Status,
Menstrual Cycle Status) During the Pre Assessment Phase of the Study
(N=60) .......................................................................................................................71
2
Factors Measured during the Pre Assessment Phase that may Interfere with
Normal Menstrual Cycling, and were used to Exclude Women Not Eligible to
Participate in the Study (N=60) ................................................................................72
3
Preassessment Screening for Eating Disorders and Premenstrual Syndrome
Scores that Determines Participants Eligibility to Continue the Study (N=60)........74
4
Craving History Questionnaire during the Pre-Assessment Phase (N=52) ..............75
5
Eligible Participant Characteristics (Health History Questionnaire, and
PMS Scale) (N=18) ...................................................................................................77
6
Food Record Data are Summarized as Mean (M) and Standard Deviation
(LSD) of the Percent of Recommended Intake of Energy and Macronutrients
during the Three Phases of Menstrual Cycle (N=14) ...............................................78
7
Food Record Data Summarized as Mean (M) and Standard Deviation (SD)
of Energy (Kcal) and mean Grams of Carbohydrates, Mean Grams of Protein,
and Mean Grams of Fat during the Three Phases of Menstrual Cycle (N=84) ........79
8
The Mean Difference of Food Craving Characteristics Pre and Post the
Craving Episode across the Three Phases M (Menstrual), F (Follicular),
L (Luteal) at Significance Level of P=0.05 ..............................................................81
9
The Mean Difference of Food Craving Criteria on a Scale of 100 during the
Three Phases of the Menstrual Cycle........................................................................82
ix
CHAPTER I
INTRODUCTION
Each month, women during the reproductive age will have a menstrual cycle
(Goodman, 2003; Levy & Lightman, 1997) that lasts 28 days on average (Carr &
Blackwell, 1993; Barbieri, Jaffe & Yen, 1999; Silberstein & Merriam, 2000). During the
menstrual cycle, women’s body will experience physiological and psychological
fluctuations due to hormonal changes in the body (Rapkin, 2003) this might have a great
impact on the quality and quantity of the food consumed, therefore, the regular diet will
be imbalanced. Approximately 74 percent of women experience food cravings during the
menstrual cycle (Dye, Warner & Bancroft, 1995).
Menstruation is known as the process of losing blood from the uterus each month
during reproductive age (Goodman, 2003; Levy & Lightman, 1997). Each menstrual
cycle consists of three main phases: follicular, luteal, and menstrual phase (Jones, 1991;
Henriet, Gaide Chevronnay & Findlay, 1999). The follicular phase occurs in the first half
of the cycle (Barbieri, Jaffe & Yen, 1999) and varies in length between 10 to 16 days
(Levy & Lightman, 1997). The Luteal phase begins with ovulation and ends on the first
day of the menstrual phase (Owen, 1975; Croxatto, 2008). Lastly, the menstrual phase
starts with the end of the luteal phase and lasts for 4 ±2 days (Levy & Lightman, 1997).
Normal reproductive function and menstrual cycle require organized work between
hypothalamus which produces gonadotropin -releasing hormones (GnRH), pituitary
gland which produces leutinizing hormone (LH) and follicular stimulating hormone
1
2
(FSH), and the ovaries which produce steroids, estrogen and progesterone (Silberstein &
Merriam, 2000).
Balanced and healthy diet is essential to maintain healthy body weight. However,
many researchers found that appetite and dietary intake are affected during different
phases of the menstrual cycle (Dye & Blundell, 1997). Essentially, the proposed cause of
changing dietary intake was hormonal fluctuations, primarily estrogen and progesterone
(Howe, Rumpler & Seale, 1993). The elevation in progesterone level during the luteal
phase was found to be associated with an increase in food intake, while elevation
estrogen level during the follicular phase was found to be associated with decrease food
intake (Dalvit-McPhillips, 1983; Johnson, Corrigan, Lemmon, Bergeron & Crusco, 1994;
Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988).
The dietary intake was studied by many researchers and measured by analyzing
the macronutrients intake (carbohydrate, fat, and protein) and the total energy intake
throughout various phases of the menstrual cycle (Tarasuk & Beaton, 1991; Lyons,
Truswell, Mira, Vizzard & Abraham, 1989; Lissner, Stevens, Levitsky, Rasmussen &
Strupp, 1988; Gong, Garrel & Calloway, 1989). The common findings among these
studies were an increase in dietary consumption during the luteal phase when compared
to the menstrual and the follicular phase.
In addition to measuring the amount and types of different macronutrients during
menstrual cycle phases, the cravings of food were investigated by measuring the intensity
rate and type of food items that is craved. Many opinions have been proposed about the
food craving phenomenon, some researchers considered the process of food craving to be
3
a response from the women’s body to the increase level of energy expenditure or to
dietary deficiency (Yen et al., 2010), while others associated it to hormonal and
psychological changes during menstrual cycle (Cohen, Sherwin, Fleming, 1987), though,
Rabinovitz ( 2005) suggested that craving for particular food is mainly results from
psychological purpose to relief intense desire for that food in addition to stress or
tension.Moreover, several studies have linked the episodes of food craving during the
menstrual cycle with psychological conditions such as depression, premenstrual
syndrome (PMS), and premenstrual dysphoric disorder (PMDD) (Dye, Warner &
Bancroft, 1995; Yen, Chang, Ko, Yen, Chen, Yeh & Chen, 2010; Smith & Sauder, 1969).
Comparing to the menstrual and follicular phase, the luteal phase tend to have the highest
craving episodes, and chocolate was found to be among the most craved food items (Hill
& Heaton-Brown, 1994; Hormes & Timko, 2011). During the menstrual cycle, women
who have high craving episodes found to have low control of body weight and feeling of
guilt associated with the craving process (Hormes & Timko, 2011).
Problem Statement
Women during reproductive age will experience monthly menstrual cycles
(Goodman, 2003; Levy & Lightman, 1997). During each menstrual cycle, psychological,
Physiological, and hormonal changes will happen (Rapkin, 2003).As a result, the dietary
pattern of women may be affected. Many studies have measured the dietary intake of
women during menstrual cycle and found significant increase during the luteal phase of
the cycle, and this change was proposed to be a result of hormonal changes (DalvitMcPhillips, 1983; Johnson, Corrigan, Lemmon, Bergeron & Crusco, 1994; Lissner,
4
Stevens, Levitsky, Rasmussen & Strupp, 1988), or it was connected it to depression and
PMS (Wurtman, Brzezinski, Wurtman & Laferrere, 1989).
In addition to dietary intake, food craving during the menstrual cycle was
investigated by several researchers. In general, women tend to experience food cravings
more than men throughout their life due to various physiological and psychological
conditions (Hill & Heaton-Brown, 1994). Many literatures associate the food craving
phenomenon during the menstrual cycle with several factors such as depression, PMS
(Dye, Warner & Bancroft, 1995; Yen, Chang, Ko, Yen, Chen, Yeh & Chen, 2010; Smith
& Sauder, 1969), anxiety and negative mood (Hill, Weaver & Blundell, 1991), dietary
restrictions, and eating disorders (Gendall, Sullivan, Joyce & Bulik, 1997). Many
undesirable consequences of food cravings have been reported such as feelings of guilt,
weight fluctuation (Hormes & Timko, 2011), it might initiate binge eating and
consequently lead to Bulimia (Waters, Hill & Waller, 2001), or it might lead to addiction
of the craved food item (West, 1987).
There are several studies linked the fluctuation in dietary intake with hormonal
changes, and other studies linked the food carving episodes with the psychological
changes during the menstrual cycle. Consequently, the quantity and quality of diet are
affected, and difficulties in maintaining normal body weight might happen, which lead to
monthly imbalance of women’s dietary habits. Therefore, it is essential to consider and
investigate the variation in dietary changes and food cravings during the menstrual cycle.
5
Purpose Statement
The purpose of this study is to determine if dietary changes and food cravings occur
during the menstrual cycle.
Hypothesis
H1: There is a change in dietary intake during the menstrual cycle
H2: Women experience food cravings during the menstrual cycle.
Operational Definitions
•
Women: healthy women during reproductive age, 18 to 40 years old, who have
regular menstrual cycles and do not complain of any illness and do not use oral
contraceptives or medications.
•
Regular menstrual cycle: occurs every month (25 to 35 days) and consists of 3
phases: menstrual, follicular, and luteal. The menstrual phase lasts for 4 ±2 days,
the follicular phase lasts for 10 to 16 days, and the luteal phase which lasts for 14
days (Levy & Lightman, 1997).
•
Dietary intake: the daily consumption of food and drinks, (Carbohydrates “g”, fat
“g”, protein “g”, and total energy “Kcal”).
•
Food craving: Craving is “increase desire to a particular substance” (Weingarten
& Elston, 1990).
CHAPTER II
REVIEW OF LITERATURE
Menstrual Cycle
Losing blood from the uterus at monthly interval is known as “Menstruation”
(Goodman, 2003; Levy & Lightman, 1997). The menstrual discharge composed of blood
and fluids secreted from the vagina and other fluid secreted in the last stage of
menstruation when the endometrial lining shed from the uterus (Jakubowsk,
Maciejewska, Bielawski & Pawłowski, 2014). Once the bleeding occurred, it is clinically
considered as the first day of the menstrual cycle (Barbieri, Jaffe & Yen, 1999; Jones,
1991). The word “Menstrual” is derived from “Menses” which is a Latin word that means
“month”, because each cycle takes about 29.5 days to be completed (Jones, 1991).
However, this duration of the menstrual cycle applied for only 10 to 15 percent of women
(Jones, 1991), and most cycle’s length has ranged from 25 to 30 days with an average of
28 days (Carr & Blackwell, 1993; Barbieri, Jaffe & Yen, 1999; Silberstein & Merriam,
2000). The length of the menstrual cycle is measured from the beginning of bleeding
until the first day of bleeding of the next proceeding cycle (Carr & Blackwell, 1993;
Barbieri, Jaffe & Yen, 1999). The menstrual cycle will proceed every month at the
reproductive age, except during periods of pregnancies and lactations (Goodman, 2003;
Levy & Lightman, 1997), and when the menopause phase begins around the age of 51,
which will be the end of the menstrual cycle (Goodman, 2003; Levy & Lightman, 1997).
Although the median period between each cycle is about 28 days (Carr & Blackwell,
6
7
1993; Barbieri, Jaffe & Yen, 1999; Levy & Lightman, 1997), there is a variation at the
beginning and the end of the reproductive age of the women, during periods of
adolescence and menopause transition which will result in increasing the frequencies
anovulatory cycles (Barbieri, Jaffe & Yen, 1999; Jones, 1991). The rise in estradiol and
gonadotropin secretion lead to luteal phase defect or anovulatory cycles, and this will
increase the length of the interval between the cycles (Barbieri, Jaffe & Yen, 1999).
When the hypothalamic, pituitary, and ovarian system interact with the target
tissues in the female’s genital tract - uterus, oviduct, endometrium, and vagina- this
interaction will result in menstruation (Barbieri, Jaffe & Yen, 1999; Carr & Blackwell,
1993). Each menstrual cycle consists of three main phases (Jones, 1991; Henriet, Gaide
Chevronnay & Findlay, 1999), as shown on figure 1 (Farage, Osborn & MacLean2008):
The menstrual phase, which lasts for 4 ±2 days, the follicle (proliferative/ estrogenic)
phase which has a varying length between 10 to 16 days, and the luteal ( secretory/
progestational) phase which lasts for a constant 14 days (Levy & Lightman, 1997)
Menarche
Menarche is defined as the first menstrual period (Levy & Lightman, 1997;
Goodman, 2003). It is a sign of pubertal maturation and development in female (Barbieri,
Jaffe & Yen, 1999). The first year of menarche is characterized by irregular cycle length
because of the unsynchronized hypothalamic-pituitary-ovarian axis that causes
anovulatroy cycles (Barbieri, Jaffe & Yen, 1999). The age of the menarche onset is
between nine and 16 years (Barbieri, Jaffe & Yen, 1999), with an average age of 13 years
(Levy & Lightman, 1997; Goodman, 2003). The mean age of menarche when measured
8
for 371 females in a longitudinal study was 12.75 years (Towne, Czerwinski, Demerath,
Blangero, Roche & Siervogel, 2005).
There are many factors that influence the process of menarche development of the
female, such as genetic and environmental factors (Karapanou & Papadimitriou, 2010;
Freedman, Khan, Serdula, Dietz, Srinivasan & Berenson, 2002). Mother and daughter
age at menarche are usually measured to determine the influence of genetics on
menarcheal age, however, it was also suggested that because of shared environmental
factors between the mother and daughter, this causes a strong association and similarities
at menarcheal age (Freedman, Khan, Serdula, Dietz, Srinivasan & Berenson, 2002).
Ethnic and racial variations are also important factors in determining the onset of
menarche Karapanou & Papadimitriou, 2010). Freedman et al., 2002 found differences
between black and white girls in their pubertal maturation and menarcheal age. In a
sample of 2058 girls, the mean age of menarche in black girls was 12.3 years, while 12.6
years in white girls (Freedman, Khan, Serdula, Dietz, Srinivasan & Berenson, 2002).
Other factors that affect the pubertal maturation and the onset of menarche are physical
activity, body weight, and nutritional status (Karapanou & Papadimitriou, 2010;
Freedman, Khan, Serdula, Dietz, Srinivasan & Berenson, 2002). It was Found that fat
distribution is related to differences in menarche development, with positive correlation
between high fat content in hips and buttock and early menarche development in subjects
between the age of 10 and 14 years, while high fat content in triceps skinfold was
correlated negatively (Lassek & Gaulin, 2007). When the relation between body weight
and menarche was measured by (Matkovic et al., 1997), they found that serum leptin
9
was correlated with increase percent of body fat and body mass index. They also found
that there was a correlation between high levels of leptin and early onset of menarche, as
for each 1ng/ml increment in serum leptin level was associated with one month earlier of
menarcheal age (Matkovic et al., 1997). Leptin is known to stimulate the reproduction in
females and helps in pubertal maturation (Chehab, Mounzih, Lu & Lim, 1997). Therefore
it associates with earlier menarche (Chehab, Mounzih, Lu & Lim, 1997). Another study
that measured the weight factor and menarche was conducted by (Stark, Peckham &
Moynihan, 1989). In this study they measured the weight and the menarcheal age of 4427
girls, and found an association between overweight and early menarche age, as 18
percent of the girls who developed their menarche before the age of 11 were overweight,
while only three percent who developed their menarche after the age of 14 were
overweight. In addition to body weight, nutritional status plays an important role in the
menarche onset (Karapanou & Papadimitriou, 2010). Berkey et al., 2000 found that
earlier menarche was associated with higher consumption of animal protein and high
consumption of fat at an early age (Berkey, Gardner, Frazier & Colditz, 2000).
Menstrual Cycle Phases
The follicular phase occurs in the first half of the menstrual cycle (Barbieri, Jaffe
& Yen, 1999). This phase is characterized by thickening of the endometrium that
increases tenfold than the regular size (Jones, 1991; Levy & Lightman, 1997), and
elongation of the uterine glands (Owen, 1975). Also in this phase, some follicles will
grow and increase in size while other follicles will not survive (Levy & Lightman, 1997).
Ovarian follicle is the functional unit of the ovary; it is composed of oocyte and somatic
10
cells (granulosa and theca cells) (McGee et al., 1997; Palermo, 2007). Palermo (2007)
classified ovarian follicle to primordial follicle that belongs to the resting pool of
follicles, and primary follicle which belongs to the growing pool of follicles. As ooccyte
grows and granulose cell layers increases, parental follicle will develop, followed by
antral follicle, and finally griffin follicle in the last stage with a size ranged from 15 to 25
mm in diameter (Palermo, 2007).
Follicular Phase
During follicular phase, the follicle undergoes a series of steps (Zeleznik, 2004).
Follicular growth starts with a pool of primordial follicles “quiescent” (Findlay, 1994).
The primordial follicle will be converted to a parental follicle as a result of granulose
cells multiplication (Zeleznik, 2004). When parental follicle increases in size, antral
cavity will be formed due to theca internea layer development, and this makes the early
antral stage of follicular development (Zeleznik, 2004).
Carr & Blackwell (1993) have described the three major stages of the follicular
phase that allows the dominant single follicle to be chosen and developed during this
phase. First is the recruitment stage, which occurs in the early follicular phase, day one to
four of the cycle. As a result of the increased level of follicular stimulating hormone
(FSH) that stimulates follicle recruitment (Zeleznik, 2004), a cohort of follicles are
recruited in order to be ovulated or degenerated (Carr & Blackwell, 1993).Next is the
selection, the second stage that is characterized by choosing follicle to ovulate from the
recruited follicles, which takes place on the day five to seven of the cycle (Carr &
Blackwell, 1993; Zeleznik, 2004). Rise of FSH concentration above the FSH threshold
11
will stimulate the recruited follicles (Messinis, Messini & Dafopoulos, 2010; Palermo,
2007), and causes an increase in growth rate by (1.62 ±0. 05mm/day) (Baerwald, Walker
& Pierson, 2009). This leads to opening the “FSH window” which allows the selected
antral follicle to enter, because the dominant follicle is the most sensitive to the FSH
(Palermo, 2007). After the dominant follicle has been selected, fulliculogenesis occurs at
the end of the follicular phase, day eight to 12 of the cycle, which is characterized by
growing of the dominant follicle and degenerating the other less mature follicles (Carr &
Blackwell, 1993). This stage ends with ovulation (Carr & Blackwell, 1993). The
diameter of antral follicle starts with three to five mm and decreases at the end of this
phase (Gougeon & Lefèvre, 1983). This diameter decreases by (4.20±0.50 mm) in the
mid follicular phase, and by (1.90 ± 0.45mm) by late follicular phase (Carr & Blackwell,
1993). In contrast, the dominant follicle continues to grow and reaches 13mm by the mid
follicular phase (Carr & Blackwell, 1993), and will continue to grow until it reaches the
pre ovulatory status at the end part of this phase (Baerwald, Adams & Pierson, 2012).
When granulosa cells increased in the dominant follicle, this means having high
estrogenic capacity (Baird, 1983). Increasing oestradiol secretion causes FSH to decline
below FSH threshold, this will lead to close the “FSH window” and will affect the less
mature follicles that depend on FSH for their growth causing them to undergo atrasia
(Palermo, 2007; Zeleznik, 2004), while the dominant follicle will proceed to the pre
ovulatory stage (Baird, 1983). After decreasing FSH level, granulosa cells in the
dominant follicle will develop leuteinizing hormone (LH) receptors in replacement to the
FSH receptors, which will help the follicle to be less dependent on the FSH (Zeleznik,
12
2004). Committed follicle can become ovulatory follicle when the granulosa cells
develop LH receptors, after nine to 12 days, and under the process of LH surge ovulation
(Jones, 1991; Findlay, 1994). During this phase, there is variation in the action of
gonadotropin levels, FSH will rise in the early follicular phase and later will decline,
while the LH level will start at a low level and later increases in response to the rise in
estrogen level (Carr & Blackwell, 1993). The process of folleculogenesis, or follicular
growth, is initiated at the end of the luteal phase of the previous cycle, and ends with the
beginning of ovulation (Carr & Blackwell, 1993; Barbieri, Jaffe & Yen, 1999).
Luteal Phase
Luteal phase begins with ovulation or follicular collapse, and ends on the first day
of next menstrual phase (Owen, 1975; Croxatto, 2008). The main feature of this phase is
the rapid growth and development of corpus luteum and increasing level of the
progesterone that helps in maintaining the process of pregnancy (Niswender, Juengel,
Silva, Rollyson & McIntosh, 2000). Luteal phase lasts about 14 days, with a range of 13
to 15 days, of 70 percent menstrual cycles (Owen, 1975; Carr & Blackwell, 1993; Jones,
1991). Luteal phase is considered to be more constant and straightforward when
compared to the follicular phase (Owen, 1975; Carr & Blackwell, 1993; Croxatto, 2008)
as most variations that occur during the menstrual cycle is related to variability in
follicular phase length (Croxatto, 2008).
The process of ovulation begins with the rapture that occur in the follicular wall,
which leads to release the ovum and therefore it will attach to the Fallopian tube (Owen,
1975). Later, the ovum will go to the uterus where it will be degenerated or fertilized
13
(Owen, 1975). Lutenization will occur for the contracting empty follicle. The rapid
growth of the dominant follicle before ovulation stimulates the production of lutenizing
hormone which will continue to increase at the time of ovulation and causes “LH surge”
that will initiate lutenization (Owen, 1975). The LH surge is initiated when estrogen
concentration rise, stimulating the process of granulosa cell lutenization and corpus
luteum development (Devoto et al., 2009). This surge lasts for about 48 hours (Barbieri,
Jaffe & Yen, 1999), where the ovulation occurs after 34 to 36 hours of the beginning of
the surge (Carr & Blackwell, 1993). The follicle starts to have its own vascular supply
when the antrum developed, but before that; the primordial and antral follicles depend on
the surrounding vessels for blood supply (Hazzard & Stouffer, 2000). However, the
granulosa layer doesn’t become vascular until ovulation occurs, and this because the
vascular supply before ovulation is located in the basement membrane of the follicle
(Hazzard & Stouffer, 2000).
Lutenization of granulose and theca cells happens when there is a rise in the levels
of progesterone and 17-α-hydroxyprogesterone in plasma, and this occurred following
LH surge (Devoto, Kohen, Muñoz & Strauss, 2009). Therefore, the corpus luteum (CL)
can be formed (Stocco, Telleria & Gibori, 2007). Lutenization enhances progesterone
synthesis and the large production of progesterone causes the angiogenic activity of
granulosa cells to increase in order to form blood capillary vessels (Croxatto, 2008). It is
mainly the LH level, which controls the angiogenesis in ovaries (Hazzard & Stouffer,
2000). When CL developed, vascular supply around the follicle increases forming a large
network of capillaries (Hazzard & Stouffer, 2000). CL is known to have a high
14
angeiogenic capacity (Reynolds, Grazul-Bilska & Redmer, 2000). CL is developed after
two to three days of ovulation, and its angeinesis activity will reach the highest level
(Acosta & Miyamoto, 2004), stimulating the blood flow and CL growth size (Baird,
1992). CL is consists of two types of cells that are important in the synthesis of luteal
steroids, those cells are non-steroidegenic cells ( immune and fibroblasts), and
steroidegenic cells (theca and granulosa cells) (Devoto, Kohen, Muñoz & Strauss, 2009).
CL is also considered to be a non-permanent endocrine gland that is made from the
ovulated follicle and produces androgens, oestradiol, as well as progesterone (Devoto,
Kohen, Muñoz & Strauss, 2009). Before ovulation, rise in FSH and LH occur as a result
of increase in progesterone and estrogen level, however, in the mid-luteal phase a high
concentration of progesterone and estradiol will cause negative feedback lead to reduce
FSH and LH (Jones, 1991).
In the non-fertile cycle (absence of conception), lutiolysis will occur (Carr &
Blackwell, 1993; Devoto, Kohen, Muñoz & Strauss, 2009; Stocco, Telleria & Gibori,
2007), as a result of changing in LH pulse that causes inhibition in progesterone (Devoto,
Kohen, Muñoz & Strauss III, 2009). CL will undergo regression and cell death (Stocco,
Telleria & Gibori, 2007). On the other hand, the fertile cycle is characterized by rapid CL
growth due to HCG production (Devoto, Kohen, Muñoz & Strauss, 2009).
At the late stage of this phase, reduction of progesterone, oestradiol, and inhibinA will occur in addition to CL regression (Devoto, Kohen, Muñoz & Straus, 2009).
Consequently this will cause secretion of pulsatile gonadotropin- releasing hormone
15
(GnRH) to increase, which will stimulate FSH and lead to recruiting a new early antral
follicle, and a new cycle can be initiated (Stocco, Telleria & Gibori, 2007).
Menstrual Phase
The menstrual phase is initiated at the end of the luteal phase when the levels of
progesterone and estrogen decline (Owen, 1975) accompanied with CL degeneration
(Goodman, 2003). At the same time when there is a decline in estrogen and progesterone
due to regression of the CL, ischemic necrosis occurs in endometrial arteries following
prostaglandin secretion, therefore bleeding occurs and menstruation begins (Levy &
Lightman, 1997). Failure of implantation leads to drop in steroids,therefore shedding of
the endometrium, and the first day of bleeding is the sign of the beginning of menstrual
phase (Strassmann, 1996). Endometrium regression, due to low supply of estrogen and
progesterone, causes compression of the spiral arteriols, this leads to vasoconstriction and
low oxygen supply for the vessels (Flowers & Wilborn, 1978). Costricting in blood
vessels that supply the functionalis layer of endometrium causes degeneration of this part
of uterus and result in bleeding (Jones, 1991). Although there is a reduction in the
vascular properties and the height of endometrium, the framework of endometrium
doesn’t change because it needs to be stimulated by FSH and estrogen in order to start a
new reproductive cycle after menstruation finished (Flowers & Wilborn, 1978).
The process of endometrium homeostasis is important in regulating menstrual
bleeding, and it is controlled by many factors: procoagulants, anticoagulants,
antifibrinolytics, and fibrinolytics (Davies & Kadir, 2012). This process undergoes two
main steps, first is the accumulation of platelets at the injured place on endothelial wall
16
and forming a platelet plug. The second step is forming a clot on the platelet plug, which
is done by the fibrin (Davies & Kadir, 2012). At the same time when hormones declined
to initiate the menstrual phase, many factors such as macrophages, prostaglandin,
cytokines, lysosomes, apoptosis, and matrix metaloproteineasis, needed to be activated
so that the vascular breakdown is stimulated (Hickey & Fraser, 2000). The major role of
these factors is to produce certain enzymes or molecules that causes tissue destruction
and therefore bleeding (Hickey & Fraser, 2000).
Endometrial arteriols are important in providing oxygen and nourishment to the
endometrium (Strassmann, 1996; Rogers, 1996). In case implantation occurred, the
endometrial arteriols will help with blood supplying and nourishing the placenta.
However, if implantation failed, the endometrium will diminish and bleeding will occur
(Strassmann, 1996). With each menstrual cycle, functional layer of the endometrium
undergoes structural changes, while the basal layer remains the same and doesn’t undergo
degeneration (Rogers, 1996). The transient functionalis is located in the superficial layer
of endometrium (Strassmann, 1996). The constriction that occurs for the spiral arterioles
usually followed by vasodilation and relaxation of these arteries that result in bleeding
(Rogers, 1996). After the third day of menstruation, the endometrium will start to
develop with the help of rise in estrogen level (Levy & Lightman, 1997). Increase
estrogen level causes the epithelial cells of the endometrium to elongate and increase in
size, thus it helps in thickening the endometrium (Goodman, 2003). However,
progesterone level will remain low until post ovulation (Levy & Lightman, 1997).
17
From menarche to menopause, the estimated numbers of periods that women
experience is about 400 cycles. The expected blood loss per cycle is between 33 to 83 ml
(Jones, 1991). Blood loss above 80 ml is considered abnormal and called (HMB) heavy
menstrual bleeding (Davies & Kadir, 2012). There are many factors that affect the
amount of blood lost each month, such as the number and length of endometrial vessels,
endometrial thickness, and the uterus size (Strassmann, 1996). The menstrual blood is
characterized by low coaguability that helps to avoid uterine cavity obstruction
(Strassmann, 1996). Five days are considered as a mean duration of menstruation phase,
while more than seven days is considered abnormal (Davies & Kadir, 2012).
Figure1. Menstrual cycle phases.
Figure 1. Menstrual cycle phases
18
Hormonal Changes during Menstrual Cycle
Normal reproductive function and menstrual cycle require organized work
between hypothalamus, pituitary gland, and the ovaries (Silberstein & Merriam, 2000), as
shown on figure 2 (Popat, Prodanov, Calis & Nelson, 2008). The gonadotropin releasing
hormones (GnRH) are produced by the hypothalamus under the influence of many
neurotransmitters such as serotonin and norepinephrine (Silberstein & Merriam, 2000).
Consequently, the gonadotrophs in the anterior lobe of the pituitary gland will be
stimulated to release two glycoprotiens that are related to menstrual cycle: leutinizing
hormone (LH) and follicular stimulating hormone (FSH) (Levy & Lightman, 1997).
Those hormones are secreted in paulstile mode and are controlled by the central nervous
system (Goodman, 2003). This process helps the ovary to produce steroids, estrogen and
progesterone, which play an essential role in the menstrual cycle (Silberstein & Merriam,
2000).
The concentration of steroids (progesterone and 17 β- estradiol) is responsible to
regulate gonadotropins production from the pituitary, and therefore, regulate the
menstrual cycle (Baird & Van Look, 1980). Each stage of the menstrual cycle is
characterized by different rate of steroid production, for example, progesterone level is
(1mg) during early stage of the follicular phase, (4mg) before the ovulation, and increase
to reach (25mg) in the middle of luteal phase. On the other hand, Estrogen reaches high
levels in the pre-ovulation (350 µg), decrease to (250 µg) in mid-luteal phase, and the
lowest rate is during follicular phase (36 µg) (Barbieri, Jaffe & Yen, 199). Some of the
conditions, such as PCOS, that causes disturbance in HPO axis regulation, lead to
19
abnormality in uterine bleeding and causes menorrhagia (Livingstone & Fraser, 2002).
Menorrhagia is defined as heavy blood loss from the uterus that exceeds 80 ml (Van
Eijekeren, Christiaens, Sixma & Haspels, 1989). Another abnormality that is related to
HPO disturbance is Amenorrhea. One of the groups that are exposed to amenorrhea are
the anorexic females, and it is a result of very low level of FSH and LH that occurs
because of GnRH inhibition (Barbieri, Jaffe & Yen, 1999).
Oral contraceptives contain estrogen, progestin, or both. The main action of the
oral contraceptive is to decrease the production of FSH and LH and this leads to inhibit
the process of ovulation. The combined oral contraceptive was linked to decrease glucose
tolerance, magnesium, zinc, serum folate, B vitamins, albumin, and serum calcium (Carr
& Blackwell, 1993).
Figure 2. The reproductive axis in menstrual cycle.
20
Estrogen
Estrogen is a hormone that plays essential role in the female’s sexual
development, breast duct development, endometrium proliferation, prevention of mineral
loss in female’s bones and also prevention of atheroschelerosis (Levy & Lightman,
1997). During the menstrual cycle, estrogen plays important role in the preovulatory
phase (Ingamells, Campbell, Anthony & Thomas, 1996). In blood, estrogen is circulated
binding with sex hormone globin (Goodman, 2003). The synthesis of Estrogen depends
on LH and FSH concentration, and the level of progesterone (Goodman, 2003). A
balance between estrogen and progesterone level is essential for a normal menstrual cycle
(Goodman, 2003). Estrogen helps in preparing the target tissue to react with the
progesterone, and It helps in the formation of progesterone receptors therefore
stimulating the tissue in response to progesterone (Goodman, 2003). When progesterone
level increases in the second part of the follicular phase, a negative effect will occur that
leads to inhibit estrogen (Silberstein & Merriam, 2000).
In the follicular phase, as the follicles grow, estrogen level will increase with
increasing granulosa cell multiplication, which causes decreased FSH level in mid cycle,
therefore the progesterone level will rise with the LH surge (Carr & Blackwell, 1993). In
the process of preovulatory follicle development, stimulation of the P450 aromatase
enzyme will occur. Granulosa cells, a major ovarian steroidogenic cells, is the place
where estrogen will be synthesized under the influence of P450 aromatase (Hillier &
Tetsuka, 1997). This enzyme controls the process of androgen formation in thecal cells,
androgen is needed to form estrogen (Hillier & Tetsuka, 1997). Another important
21
enzyme is 13β-HSD which is needed to catalyze the process of converting estradiol to a
less active compound that is called estrone, and vice versa. This process is important in
maintaining estrogen balance and modulate estrogen levels in different tissues such as
ovaries, placenta, and breast (Zhu & Conney, 1998). In the uterus, the activity of
13β-HSD enzyme is at the highest level during the luteal phase of the cycle that occur as
a result of increase in progesterone production (Zhu & Conney, 1998). Metabolic
degeneration of estrogen occurs in the liver, while the excretion is done by the kidneys
(Goodman, 2003). In order for the estrogen to be excreted, it is converted to
metabolically inactive compound (Zhu & Conney, 1998) by the hydroxylation and
conjugation with sulfate and gluconoride, and then excreted by kidneys (Goodman,
2003).
Progesterone
Progesterone plays a major role during the preovulatory stage of the menstrual
cycle (Ingamells, Campbell, Anthony & Thomas, 1996). The main site for its production
during menstrual cycle is the corpus luteum in ovaries (Gellersen, Fernandes & Brosens,
2009). Progesterone secreted by CL helps the endometrium to accept the fertilized ovum
in order to promote pregnancy (Levy & Lightman, 1997). However, it can also be
produced by other sites such as placenta and the adrenal gland (Gellersen, Fernandes &
Brosens, 2009). The major function of progesterone is to maintain a normal pregnancy
(Young & Lessey, 2010), thus a very low level of progesterone is known to be associated
with several problems in the reproductive tract such as pregnancy loss, endometriosis,
and abnormal bleeding (Gellersen, Fernandes & Brosens, 2009).
22
The formation of progesterone from cholesterol is considered the initial step in
steroidogenesis, and this process is controlled by the rate limiting cytochrome (P450 scc)
which depends on cAMP for its expression (Oonk, Krasnow, Beattie & Richards, 1989;
Simpson & Waterman, 1988). cAMP helps to increase the level of cholesterol synthesis
and facilitate its movement to inner mitochondrial membrane, where there it can be
expressed to the cholesterol side chain cleavage cytochrome (Simpson & Waterman,
1988). P450-scc is a side-chain cleavage enzyme that is forming pregnolone,
progesterone precursor, by cleaving the cholesterol side chains (Tsutsui, 2008). The next
step is converting progesterone to a compound called 17α-hydroxy prognelone, catalyzed
by (P450 17α) enzyme (Simpson & Waterman, 1988). In a later step, 3β-HSD enzyme
will convert it to progesterone (Oonk, Krasnow, Beattie & Richards, 1989).
Thecal cells, major ovarian steroidogenic cells, is a site for progesterone and
androgen production in the ovaries, where it produces progesterone under the influence
of LH (Hillier & Tetsuka, 1997). Although granulosa cells are the place for estrogen
production, when it becomes lutenized this will lead to progesterone synthesis in the
corpus luteum (Hillier & Tetsuka, 1997). The synthesis of progesterone in thecal cells is
regulated by LH, while in granulosa cells by FSH (Oonk, Krasnow, Beattie & Richards,
1989).
During the follicular phase, estrogen helps to stimulate the development of
progesterone receptors in endometrium, which will help to increase progesterone level,
and consequently, estrogen will decrease (Young & Lessey, 2010). Progesteron reduces
the level of estrogen by stimulating the enzyme 17β hydroxyl steroid dehydrogenase
23
(17β-HSD) which catalyzes the formation of inactive estrones from the estradiols, this
will decrease estrogen concentration (Bulun et al., 2002). In addition, progesterone can
decrease the regulation of estrogen receptors in endometrium, which will reduce the
response to estrogen by endometrium (Young & Lessey, 2010). A balance between both
hormones is required for normal menstrual cycles and normal reproduction (Young &
Lessey, 2010).
Follicle Stimulating Hormone (FSH)
The follicle stimulating hormone is a glycoprotein synthesized by the pituitary
gland and stimulated by gonadotropin releasing hormone (GnRH) which is responsible
for controlling FSH production (Palermo, 2007). FSH has mean half-life of 149 minutes,
and it can be cleared from the blood by the liver (Palermo, 2007). The major function of
FSH is to initiate the process of follicular recruitment and development during the
follicular phase of the menstrual cycle (Levy & Lightman, 1997). In addition, it helps in
synthesizing oestradiols (Levy & Lightman, 1997). FSH is composed of α-subunit and
β-subunit (Palermo, 2007). All glycorprotiens - FSH, LH, gonadotropins, and thyroid
stimulating hormone- have similar α-chain but they differ in their β-chain which specifies
the function of each hormone (Fan & Hendrickson, 2005). Besides GnRH, FH is also
controlled by inhibin and activin (Gregory & Kaiser, 2004), both with follastin are able to
regulate the production and secretion of FSH and also LH from the gonadotropin cells
that are located in the anterior pituitary gland (Gregory & Kaiser, 2004). Inhibin is
produced from the ovary and its main function is to inhibit FSH production (Gregory &
Kaiser, 2004), which occur before the process of follicular selection (Baerwald, Adams &
24
Pierson, 2012). Activin is produced from many tissues in the body such as granulosa cells
and anterior pituitary gland, it helps in granulose cells development in follicles and
stimulates FSH production (Baerwald, Adams & Pierson, 2012).
Gonadal hormones can have different mechanisms in FSH regulation, they can
work on the gonadotrope cells, or gonadotropin releasing hormone receptors in order to
stimulate the hormone. Gonadal hormones can also affect the hypothalamus neuron that
controls the secretion of gonadotropin hormones (Gregory & Kaiser, 2004).
Gonadotropin hormones can function through receptors called G-protein coupled
receptors (GPCRs) ( Fan & Hendrickson, 2005). LH acts through LH receptors (LHR)
that are stimulated under the FSH action, in order to help the developing follicles to react
with the LH in a later stage of the follicular phase (Sullivan, Stewart-Akers, Krasnow,
Berga & Zeleznik, 1999). FSH acts through FSH receptors (FSHR) that are located in the
granulose cells, and it was found that the different FSHR genotypes between women
result in variation in FSH secretion levels in normal menstrual cycle (Mayorga, Gromoll,
Behre, Gassner, Nieschlag & Simoni, 2000).
FSH has an essential role in stimulating the enzyme aromatase (Mayorga,
Gromoll, Behre, Gassner, Nieschlag & Simoni, 2000). In the final stage of the follicular
growth, (P450 aroma) is stimulated, which leads to estrogen synthesis in granulosa cells
from the androgen that is located in theca cells (Tetsuka & Hillier, 1997). Estrogen will
stimulate the follicular sensitivity to FSH as it is required for the growth and development
of the follicles (Owen, 1975).
25
The “FSH window” concept is defined as the time when FSH concentration
increases, and maintains this concentration at a level above the FSH threshold, which is
required to determine the process of dominant follicle selection (Baerwald, Adams &
Pierson, 2012). The FSH threshold mechanism is controlling the concentration of FSH in
the blood, as when FSH reaches high concentration, then several reactions will occur in
order to decrease the level below threshold (Sullivan, Stewart-Akers, Krasnow, Berga &
Zeleznik, 1999). Decline FSH helps the dominant follicle to grow alone, while the less
mature follicles will not be able to survive under the low FSH concentration and they will
undergo atresia (Sullivan, Stewart-Akers, Krasnow, Berga & Zeleznik, 1999).
Luteinizing Hormone (LH)
The Lutenizing hormone, or lutropin, is a glycoprotein that is synthesized by the
pituitary gland under the control of by gonadotropin releasing hormone (GnRH)
(Palermo, 2007). LH contains two subunits α-subunit and β-subunit (Palermo, 2007;
Shoham, 2002). Each subunit contains different number of amino acids and different
molecular weight (Shoham, 2002). Beta subunit is what differentiates the LH from the
other glycoproteins and gives it its unique function (Shoham, 2002).
The process of LH production is affected by negative and positive feedback
mechanisms (Shoham, 2002). The production is stimulated under the rise of estrogen
level, while inhibiting under the rise of progesterone that causes negative feedback
(Shoham, 2002). When LH is synthesized, it is not easy to measure it in the plasma until
the LH surge occurs (Owen, 1975). The main reason for the LH surge occurrence is to
stimulate the process of ovulation (Levy & Lightman, 1997). LH has a shorter half-life
26
when compared to FSH (Shoham, 2002). with a mean half-life of 30 minutes (Palermo,
2007). In addition, the process of LH excretion through the liver and kidney is faster than
FSH, because it contains lower amounts of sialic acid residues (Shoham, 2002). The
highest level that LH can reach is 10 to 16 hours before ovulation (Silberstein &
Merriam, 2000).
The major function of LH is helping the follicular development and
steroidogenesis by stimulating cAMP synthesis (Shoham, 2002). At the beginning of the
follicular phase, LH receptors are located on the thecal cells of the follicle (Goodman,
2003; Caglar, Asimakopoulos, Nikolettos, Diedrich & Al-Hasani, 2005). The main role
of LH at this stage is to stimulate androgen production, which will convert later to
estrogen under the influence of FSH (Caglar, Asimakopoulos, Nikolettos, Diedrich &
Al-Hasani, 2005). During the late stage of follicular phase, LHR will also be located on
granulosa cells, helping the selected follicle to grow and survive under a low
concentration of FSH (Caglar, Asimakopoulos, Nikolettos, Diedrich & Al-Hasani, 2005).
The mature follicle becomes less dependent on FSH and more rely on LH as they have
the LHR, however, only one percent of these receptors are needed for the follicle growth
(Palermo, 2007).
During the luteal phase, the main function of LH is to stimulate progesterone
production (Levi-Setti, Cavagna, Baggiani, Zannoni, Colombo & Liprandi, 2004). Luteal
phase is initiated when LH concentration goes beyond the “LH ceiling” which ends the
granulosa cells multiplication (Palermo, 2007). High LH concentration will stimulate the
ovulation of mature follicles, helps in the formation of the corpus luteum, and stimulates
27
the production of steroids by CL (Goodman, 2003). LH is critical for CL formation, but
with a minimal amount (Owen, 1975). Although LH is important in follicular
development, high level can cause post-mature occyte that undergoes ovulation, and it
also contributes to miscarriage (Levi-Setti, Cavagna, Baggiani, Zannoni, Colombo &
Liprandi, 2004) and related to polycystic ovarian syndrome (Shoham, 2002).
The secretion of FSH and LH during the menstrual cycle is interval related
(Caglar, Asimakopoulos, Nikolettos, Diedrich & Al-Hasani, 2005). In the beginning of
the follicular phase, FSH level is high which causes a decline in LH, this helps in
follicular growth. In mid follicular phase, FSH will stimulate estrogen production, which
then will lead to inhibit FSH and causes LH surge to occur (Caglar, Asimakopoulos,
Nikolettos, Diedrich & Al-Hasani, 2005).
Polycystic Ovarian Syndrome
Polycystic ovarian syndrome is an endocrine disorder that is characterized by
anovulation and hyperandrogenism which are not related to pituitary or adrenal gland
disorders (Franks, 1995). Elevated level of androgen, acne, alopecia, and hirsutism are
signs that are related to hyperandrognism (Franks, 1995). Women with PCOS have high
number of large follicles in their ovaries – more than 12- and each one is range from two
to nine mm in diameter (Hart, Hickey & Franks, 2004). Many signs and symptoms are
related to PCOS and in different degrees such as oligomenorrhea, amenorrhea, obesity,
hirsutism, acne, and infertility (Hart, Hickey & Franks, 2004). Ultrasonographic method
is mainly used in PCOS diagnosis, in addition, clinical and biochemical assessments
should be taken into account (Franks, 1995). When pelvic ultrasound was taken to 173
28
women who were complaining of either amenorrhea (n=73), oligomenorrhea (n=75), or
idiopathic hisutism(n=25), it was found that 92 percent of women with hirsutism, 87
percent of women with oligomenorrhea, and 26 percent of women with amenorrhea were
diagnosed with PCOS (Adams, Polson & Franks, 1986).
Endocrine disturbance that occurs in PCOS is characterized by elevated level of
LH, high concentration of androgens (testosterone and androsterone), disturbance in
estrogen production, high prolactin level, and low growth hormone production (Franks,
1995). One of the major risk factors that is associated with PCOS is insulin resistance.
Insulin has the ability to decrease the secretion of sex hormone binding globin and insulin
like growth factor binding protein. This result in rise in testosterone and androgen
production (Norman, Hickey, Moran, Boyle, Wang & Davies, 2004). Obesity has been
found to be associated with PCOS especially because it relates to many risk factors such
as high level of insulin resistance (Norman, Hickey, Moran, Boyle, Wang & Davies,
2004). Many treatment methods are suggested such as weight loss to treat obesity, oral
antihyperglycemic medication to sensitize insulin (Wei & Pritts, 2003). Some therapies to
stimulate ovulation are used such as clomiphine citrate or gonadotropins injection.
Surgical procedures can be used in order to reduce thecal layer of the follicle, thus help in
decreasing androgen production. In addition, oral contraceptives are used to reduce LH
and androgen levels (Wei & Pritts, 2003).
Endometreosis
Endometriosis is characterized by the endometrium-like glandular tissue and
storma are located outside the uterus (Vinatier, Orazi, Cosson & Dufour, 2001). The
29
prevalence of endometriosis is about five to 15 percent in women, and it affects 60 to 80
percent of infertile women or who complain of pelvic pain (Vinatier, Orazi, Cosson &
Dufour, 2001). Endometriosis is related to early manarcheal age and heavy menstrual
bleeding (Viganò, Parazzini, Somigliana & Vercellini, 2004). Endometreosis is known to
be a risk factor for infertility and dysmenorrheal (Darrow, Vena, Batt, Zielezny, Michalek
& Selman, 1993). It was found that irregular menstrual cycle in women less than 30 years
old was associated with increase the risk of developing endometriosis by 50 percent. The
signs of irregular cycle were more than six days menstruation, with heavy bleeding and
severe cramps (Darrow, Vena, Batt, Zielezny, Michalek & Selman, 1993).
Apoptosis is an importanl physiological process that helps to maintain cellular
homeostasis by programmed cell death. This process is essential during the menstrual
cycle in order to maintain homeostasis in healthy women, however, in endometriosis
patient the apoptosis of endometrial cells is affected and reduced (Viganò, Parazzini,
Somigliana & Vercellini, 2004). The main tools that are used to diagnose endometriosis
are laposcopy, magnetic resonance imaging (MRI), in addition to physical and clinical
assessment such as history of pelvic pain and dysmenorrhea (Teirney & Prentice, 2002).
A major goal of endometriosis treatment is to reduce the ovarian steroid hormone
secretion, therefore inhibit endometrium growth. Some treatment methods are using oral
contraceptive pills, progesterone, danazol, or gonadotropn releasing hormone analogues
(Teirney & Prentice, 2002).
30
Factors Affecting Menstrual Cycle
Normal body weight is essential to maintain normal reproduction, as very low or
very high body weight is associated with menstrual disturbance and failure to maintain
reproductive function (Pasquali, Patton & Gambineri, 2007). In addition, obesity is
known to be associated with high leptin level, high insulin, and changing in reproductive
hormone profile. One of the tissues that aromatase activity takes place on is the adipose
tissue, and mainly this enzyme will be affected by central obesity that causes androgen
accumulation (Pasquali, Patton & Gambineri, 2007).
Physiological Factors
Obese infertile women are having significantly higher level of androgen and
testosterone (Bates & Whitworth, 1982). Central obesity is also related rise the insulin
levels that affects androgen production from the ovaries, and raise the level of insulin like
growth factor (IGF-1) that increases the androgens. In addition, they tend to have an
irregularity in gonadotropin secretion presented by low level of LH (Pasquali, 2006). Sex
hormone-binding globin (SHBG) is an important carrier for androgens and estrogens
(Pasquali, Pelusi, Genghini, Cacciari & Gambineri, 2003). In obese women, especially
central obesity- a high level of insulin causes suppressed SHBG production from the
liver, this causes the testosterone to accumulate as it requires the SHBG for its clearance.
In addition, estrogen level increases with declining SHBG, however, estrogen level tend
to be higher in peripheral obesity than in central obesity (Pasquali, Pelusi, Genghini,
Cacciari & Gambineri, 2003). The data of a case control study showed a relationship
between obesity and menstrual cycle disturbance (Castillo-Martínez, López-Alvarenga,
31
Villa & González-Barranco, 2003). In 120 women who were obese, 18.3 percent of them
had oligimenorrhea, 11.4 percent had amenorrhea, and 30 percent complained of irregular
menstruation. 45 percent of the dysmenorrhic women were in grade four or five of
obesity. In this study, it was found that as obesity grade increased, consequently the risk
of oligomenorrhea and amenorrhea increased (Castillo-Martínez, López-Alvarenga, Villa
& González-Barranco,2003). In a study where the menstrual cycle of 3941 women was
measured, it was found that there was a correlation between body mass index (BMI) and
menstrual cycle regularity and length. As BMI increases, the menstrual cycle irregularity
and length increases (Rowland, Baird, Long, Wegienka, Harlow, Alavanja, Sandler,
2002). Increased body fat is related to many reproductive problems such as irregular
menstruation, miscarriage, and anovulation (Pasquali, Pelusi, Genghini, Cacciari &
Gambineri, 2003).
Environmental Factors
There are many internal and external factors that affect the Hypothalamicpituitary-ovarian axis, therefore causing changes in steroid hormones and these changes
affect the length of menstrual cycle, duration of bleeding, and variation in menstrual
pattern (Cooper, Sandler, Whelan & Smith, 1996).
Alcohol. Alcohol drinking is known to cause changes in the menstrual cycle
(Liu, Gold, Lasley & Johnson, 2004). Drinking more than one alcoholic drink per week
was associated to decrease the duration of the follicular phase, thus decreasing the
menstrual length (Liu, Gold, Lasley & Johnson, 2004). In a study where 80 women were
measured to determine the effect of alcohol on menstrual cycle, it was found that
32
drinking was related to menstrual cycle and reproductive hormone disturbance among 60
percent of heavy drinkers ( more than 5 drinks /day), and 50 percent of social drinkers
(2.5 to 5 drinks/day). In addition, high prolactin level was seen in three on the heavy
drinkers and one social drinker, and anovulatory cycles were found in three social
drinkers (Mendelson & Mello, 1988). Shorter menstrual cycle was found in women with
alcohol abuse (Barron, Flick, Cook, Homan & Campbell, 2008).
Caffeine. It was hypothesized that caffeine can cause changes in hormone profile
in women therefore change menstrual cycle pattern (Fenster et al., 1999). The caffeine
intake from coffee, tea and soda was measured in 403 women, and they were divided into
four groups according to the amount of caffeine consumed: none, low intake (1 to 150
mg/d), moderate (151 to 300 mg/d), and high (˃300mg/d). The results showed that heavy
caffeine intake was associated decrease menstrual cycle length compared with the other
groups especially the low intake. The proposed mechanism was the vasoconstriction
ability of caffeine that reduces blood flow in the uterus and also the ability for caffeine to
alter sex hormones (Fenster et al., 1999).
Smoking. Cigarette smoking is associated with irregular and short menstrual
cycles (Rowland, Baird, Long, Wegienka, Harlow, Alavanja, Sandler, 2002). Windham et
al., 1999) measured the steroid hormones for 408 women to determine the pattern of
seven menstrual cycles, also the smoking level was measured by dividing the subjects
into three groups: nonsmokers, low smokers (<20 cigarettes /day) and heavy smokers
(˃20 cigarettes /day). The result showed that the menstrual cycles of heavy smokers were
irregular and shorter (less than 25 days for one cycle). 20.5 percent of the women who
33
were experiencing short cycles were heavy smokers, 14.5 percent were low smokers,
while only 8.7 percent were nonsmokers (Windham, Elkin, Swan, Waller & Fenster,
1999).
Physical activity. Different types of sports have an effect of female’s
reproductive function and menstrual cycle pattern, whether these sports are weight
bearing activities such as ballet, or non-weight bearing such as swimming. Delayed
menarcheal age, amenorrhea, and irregular menstruation are some of the complications
that are caused by hormonal disturbance as a result of intense exercise pattern (Warren,
Perlroth, 2001).
Participating in sports that require a low body weight such as ballet, causes
disturbance in hormonal profile. Very low body weight affects the hypothalamicpituitary-ovarian axis, therefore the production of GnRH, LH, and FSH will be
suppressed, causing delay in menarche (Warren & Perlroth, 2001). Studies who examined
the effect of physical activity on female growth found that females who participate in
strenuous sports such as gymnastics tend to have lower body fat content, height and
weight, comparing with those who are engaged in less strenuous activities (Rogol, Clark
& Roemmich, 2000). Brooks-Gunn et al., 1987 measured the menstrual pattern in 55
ballet dancers. They found that 56 percent of the dancers had significantly delayed
menarche (M= 14.29 years, P <0.0). Menstrual irregularity such as oligomenorrhea was
present of 40 percent of the dancers, and amenorrhea was present in 19 percent of the
dancers and was significantly related to very low body weight (Brooks-Gunn, Warren &
Hamilton, 1987).
34
Strenuous exercise is associated with menstrual cycle disturbance, as it causes
suppression in hypothalamic function which leads to decrease LH, FSH, and estradiol
production (Mitan, 2004). Many factors determine the severity of reproductive
dysfunction and menstrual disturnbance such type of exercise, percent of body fat, body
weight,dietary restriction, and the presence of eating disorder such as anorexia nervosa
(Warren, Perlroth, 2001). Theintz et al., 1993 assessed the effect of physical activity on
pubertal development of 22 highly trained female gymnasts and 21 moderately trained
swimmers, at the age of 12. By following the groups, it was found that the subjects in the
swimming group developed their menarche earlier (12.9 ±0.9 years) than the gymnasts
group (14.5 ±1.2 years). Similar to this result (Georgopoulos et al., 1999) found a delay
in menarche age in 32 percent of 22 female gymnasts ( 14.3 ±1.46) when that result
compared to the menarch age of their mothers and sisters, in addition, a positive
correlation was found between training intensity and delayed menarche age (P < 0.001)
(Theintz, Howald, Weiss & Sizonenko, 1993).
Oral Contraceptives. Oral contraceptives (OC) are prevalent among women for
birth control (Spitzer, Lewis Heinemann & Thorogood, 1996). Some studies, they found
using low doses of OC helpful in maintaining one mass and preventing osteoporosis
(Kuohung, Borgatta & Stubblefield, 2000). Another finding that the body composition
and BMI for the OC users did not differ from the non-OC users (Lloyd, Lin, Matthews,
Bentley & Legro, 2002). When food craving and negative mood examined between OC
users and non-OC users, both groups were similar in their cravaing, however, the OC
group experienced low levels of negative mood (Bancroft & Rennie, 1993). Some women
35
may experience headache, change in weight and nausea when using OC, and it was found
to be associated with an increase in cholesterol level (Lloyd, Lin, Matthews, Bentley &
Legro, 2002).
Psychological Factors
During the menstrual cycle, many psychological changes can occur and causes
fluctuations in different phases of the cycle (Herrera, Gómez-Amor, Martínez-Selva &
Ato, 1990).
Stress. Severe stress is known to be associated with amenorrhea and irregular
menstruation (Young, Midgley, Carlson & Brown, 2000) the main proposed mechanism
is that stress stimulates the hypothalamus-pituitary-adrenal axis (HPA) activity in this
causes inhibition in the activity of hypothalamic-pituitary-ovarian axis (HPO). In
addition, it causes disturbance in the reproductive hormones especially lowering the LH
production (Young, Midgley, Carlson & Brown, 2000). Collins, Eneroth & Landgren,
1985 stress was related to FSH and estradiol fluctuation throughout the menstrual cycle.
Barsom, Mansfield, Koch, Gierach & West, 2004 found no association between stress
level and menstrual cycle ( length or bleeding ), however, decreasing the stress was
related to increase menstrual phase length. Work stress was measured by (Fenster,
Waller, Chen, Hubbard, Windham, Elkin & Swan, 1999) and found its relation to
decrease menstrual cycle length (≤ 24 days) especially reducing the duration of the
follicular phase in women aged from 18 to 39 years.
36
Depression. On the other and, depression was associated with long and irregular
menstrual cycles (Rowland, Baird, Long, Wegienka, Harlow, Alavanja, Sandler, 2002).
Angst, Sellaro, Stolar, Merikangas & Endicott, 2001 measured several psychologic
symptoms and its relation to the timing of menstruation. They found association between
the occurance of depressed mood and the irregularity of menstrual phase when compared
with other symptoms such as anxiety, tension, and nervousness. It was also found that the
prevalence of these symptoms was the highest during premenstrual phase (Angst, Sellaro,
Stolar, Merikangas & Endicott, 2001). Chau, Chang & Chang, 1998 measured different
scales of anxiety, craving water retention, and depretion in relation to premenstrual
tension. It was found that the anxiety scale (tension, mood swing, irritability) had the
highest effect on premenstrual tension. One of the psychiatric disorders that was studied
in relation to the menstrual cycle is bipolar disorder (BPD) (Rasgon et al.,2005).
Irregular menstrual cycle was found in 65 percent of 80 women complaining of
BPD, also change in cycle frequency and blood flow was observed (Rasgon et al.,2005).
In addition, many psychiatric medications such as psychotropic medication causes
irregular menstruation due to their effect in changing reproductive hormone level
(Rasgon et al.,2005).
Eating disorders. Eating disorders such as anorexia nervosa (AN) and bulimia
nervosa (BN) are related to menstrual cycle irregularity (Casanueva, Borras, Burguera,
Muruais, Fernandez & Devesa, 1987; Devlin, 1989).
Anorexia nervosa (AN) is a health condition where the patient fails to maintain
normal body weight, with a decrease of more than 25 percent of regular weight that is
37
caused by psychological problems mainly the concern of being obese (Casanueva,
Borras, Burguera, Muruais, Fernandez & Devesa, 1987). AN is one of the main risk
factors of amenorrhea (absence of menses) (Mitan, 2004). It is characterized by
disturbance in reproductive hormones. Estrogen, LH and FSH are low which causes
absence or irregular menstruation depending on the severity and the amount of weight
loss (Mitan, 2004; Casanueva, Borras, Burguera, Muruais, Fernandez & Devesa, 1987).
In addition, low levels of leptin and insulin like growth factor are seen in anorexic female
who developed amenorrhea (Mitan, 2004). Surbey, 1987 believed that amenorrhea is a
normal response by the body for the stress and starvation. Amenorrhea in considered to
be main diagnostic criteria for anorexic patient (Devlin, 1989). It was suggested that
diminish GnRH is an important cause for menstrual cycle cessation in anorexic women
(Devlin, 1989).
Another eating disorder is bulimia which is characterized by frequent episodes of
binging followed by purging or a very low diet intake. Bulimia patients usually have
regular weight, in addition to some of AN characteristics such as amenorrhea or
oligomenorrhea. HPA axis dysfunction was seen in AN and BN subjects. Fichter, Pirke,
Pöllinger, Wolfram, G., & Brunner, 1990 found that a high number of fasting days and
increase in dietary restriction are related to reduction in FSH and LH (Devlin, 1989).
38
Dietary Changes during Menstrual Cycle
There are many factors that affect energy expenditure, and one of these factors is
menstrual cycle (Howe, Rumpler & Seale, 1993). Hormonal changes during different
phase causes change in metabolism, with high level of progesterone during luteal phase
linked to increase metabolic energy expenditure (Howe, Rumpler & Seale, 1993).
Metabolism
The luteal phase is characterized by having high resting metabolic rate (RMR) by
18.4 percent higher than the follicular phase. In this study, high RMR was not related to
significant increase in energy and macronutrient intake during the luteal phase (Piers,
Diggavi, Rijskamp, Van Raaij, Shetty & Hautvast, 1995). Bisdee, James & Shaw, 1989
found an increase in energy expenditure during the luteal phase especially in the last
stage of this phase. In addition, (Tai, Castillo & Pi-Sunyer, 1997) found that the last stage
of luteal phase was characterized by high thermic effect of food (TEF), however, TEF
was low at an early stage of this phase. Webb, 1986 found that in the 14th day of the
menstrual cycle –during luteal phase- energy expenditure increases by 8 to 16 percent
after the process of ovulation. Webb, 1986 suggests that 9 percent of this increase in EE
was due to increase progesterone level as it is responsible to stimulate the metabolic rate.
Solomon, Kurzer & Calloway, 1982 measured basal metabolic rate (BMR) throughout
the menstrual cycle, found that the menstrual phase had a low level of BMR while the
lowest level was before one week of ovulation.
39
Dietary Intake
Fluctuation in both hormones, estrogen and progesterone, was linked to changes
in food intake in different phases of the menstrual cycle. Increase in food intake during
luteal phase is related to elevated progesterone levels, while low appetite and decreased
food intake during the follicular phase was linked to high estrogen levels
(Dalvit-McPhillips, 1983; Johnson, Corrigan, Lemmon, Bergeron & Crusco, 1994;
Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988). Many studies have measured the
changes in macronutrient intake ( carbohydrate, fat, and protein) and total energy intake
during throughout the menstrual cycle (Tarasuk & Beaton, 1991; Lyons, Truswell, Mira,
Vizzard & Abraham, 1989; Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988;
Gong, Garrel & Calloway, 1989).
(Lissner et al., 1988) found that the mean energy intake during luteal phase – 10
days before menstruation- ( 2335 kcal ) was significantly higher (p<0.006) by 87 kcal
when compared to post menstrual phase. High progesterone level was linked to increase
the appetite in this study (Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988).
Another study found a high caloric intake during the luteal phase (M=214 kcal)higher
than follicular phase. However, this study found no significant difference between luteal
and menstrual phase in total energy consumption (Gong, Garrel & Calloway, 1989). Hill
& Heaton-Brown, 1994 have found a 500 kcal difference between premenstrual and post
menstrual phases, with higher calories during the premenstrual phase. Dalvit-McPhillips,
1983 measurd the intake of carbohydrate, protein and fat in the period before and after
ovulation. The results showed a stable intake of both protein and fat throughout the cycle,
40
while carbohydrate was fluctuated. Carbohydrate intake was higher by about 54 percent
before menstrual cycle (Dalvit-McPhillips, 1983). In addition, (Johnson et al., 1994)
found a significant difference in fat intake between follicular and luteal phase, with
higher amounts (9.2 g) of fat during the luteal phase, while protein intake was stable in
both phases (Johnson, Corrigan, Lemmon, Bergeron & Crusco, 1994). Similar to this
finding, (Tarasuk & Beaton, 1991) resulted in a significant increase of fat consumption
during the luteal phase, but there wasn’t differences in protein and carbohydrates. By
measuring the macro and micronutrients intake, (Martini, Lampe, Slavin & Kurzer, 1994)
have found significant increases in all micronutrients and energy intake during the luteal
phase. Although there was a higher intake of vitamin D, phosphorus, and magnesium
during the luteal phase, but it wasn’t significant (Martini, Lampe, Slavin & Kurzer,
1994).
One of the disorders that affects food intake during the menstrual cycle is
premenstrual syndrome (PMS) (Wurtman, Brzezinski, Wurtman & Laferrere, 1989).
PMS women had significantly higher rates of depression, carbohydrate intake, and
appetite during the last stage of luteal phase (p < 0.0001). During this stage, caloric
consumption increased by 274 kcal, and carbohydrate intake was higher by 24 percent,
while protein intake did not change. Carving for carbohydrates in PMS subjects was
linked to decrease depression and negative emotions (Wurtman, Brzezinski, Wurtman &
Laferrere, 1989). Each phase of the menstrual cycle is characterized by different energy
and macronutrient intake. Luteal phase is considered to have higher intake when
compared with the rest of the menstrual cycle (Barr, Janelle & Prior, 1995).
41
Appetite and Menstrual Cycle
Appetite has objective and subjective characteristics that control the amount and
type of food consumed (Dye & Blundell, 1997). Some of the objective characteristics are
sensory reactions such as taste and smell, combined with amount of food. While the
subjective characteristics such as feelings of hunger and fullness that initiate the
beginning and ending of the eating process (Dye & Blundell, 1997). There are many
factors that contribute to increase and decrease the appetite in females (Hill & HeatonBrown, 1994). One of the main factors is hormonal fluctuation during different phases of
the menstrual cycle. Hormone fluctuation affects food intake therefore eating pattern
(amount, type, timing) of food consumed (Dye & Blundell,1997). The two main
hormones that have an effect on regulating appetite, whether this effect was direct or
indirect, are estrogen and progesterone (Buffenstein, Poppitt, McDevitt & Prentice,
1995). Many mechanisms that occur in the body parallel to ovarian hormone vary during
the menstrual cycle such as gluconeogenesis and lipid metabolism, these mechanisms
have an effect on signaling the appetite and affecting food intake. Estrogen has its effect
in the process of lipolysis which results in increase free fatty acids and decrease the
appetite (Buffenstein, Poppitt, McDevitt & Prentice, 1995).
In addition, estrogen has an effect in regulating many neurotransmitters such as
serotonin, dopamine, and noradrenalin (Buffenstein, Poppitt, McDevitt & Prentice,
1995). Brain serotonin (5-HT) concentration is known to be related to food intake and
appetite regulation. It was found that high concentration of serotonin was linked to
suppression the preference to carbohydrate- rich food m while slightly enhance the
42
preference of fat and proteins (Leibowitz, Weiss, Walsh & Viswanath, 1989). The effect
of serotonin on macronutrient intake was higher in carbohydrate comparing with the
other macronutrients (Leibowitz, Weiss & Suh, 1990). It was found that decreasing
carbohydrate was associated with high level of serotonin, while the protein and fat
consumption wasn’t affected (Leibowitz, Weiss & Suh, 1990). Carbohydrate was related
to stimulate serotonin precursor (tryptophan). Carving the CHO might be a reaction to the
low level of serotonin (Buffenstein, Poppitt, McDevitt & Prentice, 1995). In addition, the
conversion of domapmin to noradrenalin is catalyzed by (dopamine beta-hydroxylase).
Estrogen is able to inhibit this enzyme, leading to decrease appetite as a result of low
level of noradrenalin (Buffenstein, Poppitt, McDevitt & Prentice, 1995).
Food Craving
Craving is generally defined as “an increase desire to a particular substance”
(Weingarten & Elston, 1990). In many situations “craving” was linked to “addiction”
(West, 1987). Although craving was always defined as a strong desire or urge, this may
result later to cause addiction, in order to fulfill this particular need for the craved
substance. However, (West, 1987) argued that in order to give the word craving this
definition is not clear or precise, because the level of “feeling a strong desire” might
differ in strength and intensity from one person to another. When compared to addiction,
(Kozlowski & Wilkinson, 1987) considered craving to be more subjective. Kozlowski &
Wilkinson, 1987 argued that the researchers who were the term “craving” in explaining a
desire for substance like alcohol, this term is nor specific and he suggested that this term
should explain an action that is characterized by sudden, not expected, and strong
43
reaction, and this action could be socially unacceptable. There are many proposed ways
to measure cravings, such as self-report of craving episode on a scale from one to ten.
Another way is to measure the amount of the craved substance, whether it was specific
nutrient, alcohol, or drug. Also, measuring the speed of consumption of the substance. In
addition, psychological indicators such as measuring heart rate can be used (Weingarten
& Elston, 1990).
Types of cravings. One of the types of craving is food craving. Food craving
was studied in many research and was linked to many conditions such as menstrual cycle,
PMS, bulimia nervosa, and compulsive eating disorder.Some of the most craved food is
chocolates and carbohydrate rich food (Kozlowski & Wilkinson, 1987). Another type is
pica. Craving for non-food or non-nutritious items is the definition of pica that is seen
mainly in pregnant women or in individuals who are complaining of nutritional
deficiencies such as iron deficiency anemia (Rose, Porcerelli & Neale, 2000). Many
substances are consumed by pica patients such as ice, ashes, clay, and chalks (Rose,
Porcerelli & Neale, 2000).
Another type of craving is alcohol. High level of alcohol craving was associated
with high level of obsession among alcoholic subjects (Modell, Glaser, Cyr & Mountz,
1992). Craving for cigarette smoking is another type of craving. There are many variables
that are used to determine craving for cigarettes such as: having a desire or urge to
smoke, wanting cigarettes immediately when thinking of it, also measuring whether it is
associated with a decrease in negative emotions (Kozlowski, Pillitteri, Sweeney,
Whitfield & Graham, 1996). Another type is drug craving. Measuring the episodes and
44
the level of drug craving was used to determine the process of drug withdrawal and
relapse (Kozlowski & Wilkinson, 1987).
Causes of food craving. The phenomenon of food craving was linked to many
physiological and psychological conditions, such as pregnancy, depression, and eating
disorders (Weingarten & Elston, 1990). It is also linked to the hormonal and
psychological changes during menstrual cycle (Cohen, Sherwin, Fleming, 1987). Pelchat
suggested that the process of food craving is not a result of increase appetite or hunger
and the episodes of food craving are not usually occur on a daily basis by consuming
regular food (Pelchat, 2002). When the feeling of hunger is results from psychological
demand for food due to low calorie intake, craving for certain food is mainly results from
psychological purpose to relief intense desire for that food in addition to stress or tension
(Rabinovitz, 2005).
Eating disorders are characterized by many factors that predispose to food craving
such as mood change, anxiety dietary restriction, and a low serotonin level (Gendall,
Sullivan, Joyce & Bulik, 1997). In some bulimic subjects, food craving is considered as a
beginning of binge episode. It was found that food craving when accompanied with
binging leads to increase negative emotions and feeling the tension, while food craving
alone was associated with decrease the negative emotions (Waters, Hill & Waller, 2001).
The process of “emotional eating” was linked to psychological factors. A high level of
anxiety and negative mood were linked to increased food craving, however, in this study
they found no significant relation between dieting and food craving (Hill, Weaver &
Blundell, 1991).
45
The types of food are an important component of the carving experience, as
carbohydrate rich food considered more craved than savory food (Tiggemann & Kemps,
2005). Serotonin level was linked to food craving especially carbohydrates (Pelchat,
2002). Carbohydrate is known to stimulate the process of serotonin synthesis from
tryptophan. A low serotonin level causes increases the appetite to carbohydrate
containing food (Pelchat, 2002). When correlation between sensory modalities and
imagining the craved food was measured, it was found that the visual effects of food had
the highest score in stimulating the craving process compared to gesture, olfactory,
tactile, and auditory factors (Tiggemann & Kemps, 2005).
Other factors related to food craving are age and gender (Pelchat, 1997). women
tend to crave more chocolate than men . When 128 subjects were measured, there was 42
percent of women craved chocolate compared with only 11 percent of men (Tiggemann
& Kemps, 2005). found that young adults significantly had a higher craving level than
older adults . In addition, female were more than males in their craving episodes
especially for chocolates (Pelchat, 1997) Another cause for food craving is dietary
restriction, people who follow a restricted diet tend to have more craving episodes
(Pelchat, 1997). Alcohol relapse, tobacco cessation,and drug withdrawal are among the
factors that are related to craving (Kozlowski & Wilkinson, 1987).
Food craving during menstrual cycle. Many studies have linked the episodes of
food craving during the menstrual cycle with psychological conditions such as
depression, PMS, and PMDD (Dye, Warner & Bancroft, 1995; Yen, Chang, Ko, Yen,
Chen, Yeh & Chen, 2010; Smith & Sauder, 1969). ( Dye, Warner & Bancroft, 1995)
46
found a relationship between food craving and menstrual cycle, where 74.3 percent of the
tested subjects (n=5549) reported that they experienced food craving. In addition, high
level of food craving was associated with a high degree of depression in all phases of the
cycle. By measuring 284 nurses, (Smith & Sauder, 1969) found that 66 percent of theses
nurses were experiencing signs of depression before menstrual phase. Also they found a
significant relationship between sweets craving, PMS, and depression (p< 0.001). PMS
was lower in 30 percent of the subjects who craved spicy food .
When the premenstrual –luteal phase was compared to the menstrual and
follicular phases, It was found that it had the highest percentage of occurrence of food
craving episodes (66 percent). Among all the food studied, chocolate was significantly
the most craved food by women (79 percent) when compared to other food items (Hill &
Heaton-Brown, 1994). When chocolate craving was measured in 97 women, (Hormes &
Timko, 2011) found that in 28.9 percent of the subject’s chocolate craving was related to
menstrual cycle, and 67.9 percent of menstrual cycle craving was during the luteal phase.
On the other hand, when the levels of depression and anxiety of the menstrual and nonmenstrual carvers were compared, it was found that there was no significant difference
between both groups (p˃ 0.05). Menstrual cravers were characterized by having more
weight fluctuation, more guilt associated with their craving, and more dietary restriction
(Hormes & Timko, 2011). The link between chocolate craving and menstrual cycle was
also examined by (Hormes & Timko, 2011). By measuring 97 women, 29 percent of
them have reported menstrual linked chocolate craving, and most of the cravings were
47
seen during premenstrual phase . In this study, food craving was associated with less
weight satisfaction and low dietary control.
Ye et al., 2010 measured the food cravig during menstrual cycle in women
complaining of premenstrual dysphoric disorder (PMDD). Food craving in PMDD
women was significantly higher than the control group. The craving was higher in the
high sweet-fat food category, specifically during the luteal phase. Positive emotions were
linked to consumption of the craved food in PMDD subjects (Yen, Chang, Ko, Yen,
Chen, Yeh & Chen, 2010). Another study asked 37 women to taste different food items
and to rate them into three categories (sweet, salty, bland). The consumption of the sweet
category that contained (chocolate, coffee, gum, and cake) was significantly higher than
salty and bland categories. There was significantly higher consumption of sweets during
the luteal phase (p <0.01) when compared with the follicular phase. It was found also that
high levels of estrogen and progesterone were associated to increase consumption of
sweet foods (Bowen & Grunberg, 1990).
Yen et al., 2010 Considered that the process of food craving to be a response from
the women’s body to the increase level of energy expenditure or to dietary deficiency.
Also, it is considered to be a result of hormonal fluctuation during menstrual cycle, or a
response to negative emotions and stress (Yen et al., 2010).
Premenstrual Syndrome (PMS)
PMS occurs before menstruation, mainly during the luteal phase and ends with
the first day of the menstrual phase (Usman, Indusekhar & O'Brien, 2008). In order for
the woman to be diagnosed with premenstrual syndrome (PMS), she should experience
48
more than one sign of the ACOG (American college of obstetrics and gynecologists)
PMS diagnostic criteria list (Rapkin, 2003). These criteria are divided into two
categories. First, affective which includes depression, angry mood, irritability, confusion,
and social problems. Second somatic which includes headache, extremities swelling,
bloating in the abdominal area and tenderness in the breast (Rapkin, 2003). When the
physical, psychological, and behavioral symptoms of the PMS became severe, this is
known as premenstrual dysphoric disorder (PMDD) (Usman, Indusekhar & O'Brien,
2008). To be diagnosed with PMDD, women should experience five or more of the PMS
symptoms (Milewicz & Jedrzejuk, 2006). There is no specific cause of the PMS
(Milewicz & Jedrzejuk, 2006). However, some of the proposed causes are low
concentration of progesterone during the luteal phase, dysfunction in the
hypothalamus-pituitary-adrenal axis which affects neurotransmitter production, low
calcium and magnesium intake, high body weight, and some psychological factors such
as stress (Milewicz & Jedrzejuk, 2006). Many pharmachologic methods have been
suggested to treat and prevent the PMS such as dietary modification, exercise, stress
management, and cognitive behavior therapy (Rapkin, 2003). Serotonin reuptake
inhibitor (SSRI) such as fluxetine and sertaline were suggested by the ACOG for treating
PMS (Rapkin, 2003).
CHAPTER III
METHODOLOGY
Purpose
The purpose of this study was to measure dietary changes and food craving
between different phases of the menstrual cycle in normal menstruating women attending
Kent State University in Kent Ohio. The research was approved by Kent State University
institutional Review Board (IRB). The followings are the research hypothesis: I. There is
changes in dietary intake during the menstrual cycle. II. Women experience food cravings
during menstrual cycle.
Design
The research design was a descriptive, quantitative comparative analysis of the
participant’s dietary intakes and food cravings through the three different menstrual cycle
phases. The independent variables were the menstrual cycle phases (menstrual phase,
follicular phase, and luteal phase). Dependent variables were dietary intake, including
Calories and macronutrients (carbohydrates, proteins, and fat), amount of macronutrients
(grams), and total energy intake (Kcal).
Subjects
Participants were recruited using a convenience sample of women affiliated in
Kent State University, in Kent Ohio. The inclusion criteria were women attending Kent
State University, between the ages of 18 to 40 years, and having normal menstrual cycles
(menstrual cycle that occurs every 25 to 35 days). Exclusion criteria were using
exogenous hormones (oral contraceptives, injections, implant), used oral contraceptives
49
50
for the past six months or planning to use it for the next two months, planning to get
pregnant in the next two months, having irregular menstrual cycles (less than 25 days or
more than 35 days), using medications that affect their appetite, reporting psychological,
medical condition that interfere with normal menstruation, having high rate of eating
disorder (score of more than 20 in the EAT-26), complaining of PMDD, intensive
exercise (more than seven hours per week), having high or low body weight ( BMI less
than 18, or more than 25).
Instruments of Measure
An online survey was used to determine the eligible subjects to participate in the
study.
Pre Assessment Phase
The Pre Assessment Phase consists of four sections:
1) Health History Questionnaire (Appendix B). This was used to measure age, weight,
height, BMI (kg/m2), exercise intensity (hours/week), menstrual cycle pattern (length
of the cycle), usage of oral contraceptives (yes, no), the presence of any medical
condition that interfere with the menstrual cycle. The questionnaire can be found in
appendix B.
2) Eating Attitude Test-26 (EAT-26) was used to detect the signs of eating disorders
(Garner et al., 1982). The EAT-26 consists of 26 questions that are answered based
on a six-point Likert-Scale (Always =3 points, usually = 2 points, often =1 point,
sometimes, rarely and never = 0). This test covers four areas: dieting behaviors,
bulimia, preoccupation with food and oral control. A score of 20 or higher on this test
51
indicates concern about eating habits. This can be found in appendix C part A. The
second part of the EAT-26 consists of 5 questions that measure the eating behavior
using a Likert scale (Never, once a month or less, two to three times a month, once a
week, two to six times a week, once a day or more). The scoring and interpretation
for the EAT-26 can be found in appendix C part B. The permission for using this test
can be found in Appendix C part C.
3) The Mental and Physical Symptom Daily Rating Scale (appendix D part A) was used
to measure the severity of PMS and PMDD symptoms. This scale consists of 28
questions that focus on 3 categories: questions 1 to 12 focuses on the mental
symptoms, questions 13 to 21 focus on the physical symptoms, questions from 22 to
28 are miscellaneous information. The scoring that describes the severity of the
symptoms is rated with four levels (3 = severe, 2 =moderate, 1 =slight, and 0 =not at
all) (Dhar & Pearson Murphy, 1990). Scoring one or more of the severe symptoms
for two menstrual cycles is an initial diagnosis of PMS, while scoring 5 or more of
the severe symptoms will be considered as having PMDD (Freeman, 2003).
Participants who fall in the PMDD category were excluded from the study. The
permission for using this survey can be found in appendix D part B.
4) Food craving questionnaire (Appendix E part A). This survey was used to measure
the past food craving experience, type and frequency of the craving and whether it is
linked to the emotional status and to the menstrual cycle (Weingarten & Elston,
1991). The permission for using this survey can be found in Appendix E part B.
52
Assessment Phase
After completing the pre-assessment phase, eligible participants proceeded to the
assessment phase where six measurement methods were used:
1) The menstrual cycle tracking record: was used to record the beginning and ending
date of each phase of the cycle. The menstrual phase begins with the first day of
bleeding and ends by the end of bleeding. Second is the follicular phase, which begins
with the end of menstrual phase and ends with ovulation. Third is the luteal phase,
which begins with ovulation and ends with the first day of the next menses. This
process was repeated twice as each subject completed two cycles. This record helps to
measure the length of each phase and cycle and make sure that each cycle was within
the normal range (25-35 days). The menstrual cycle tracking record can be found in
appendix F.
2) Ovulation test: the process of ovulation was detected using a urinary test to measure
Luteinizing hormone (LH) surge. The LH surge detection kit (Easy @Home
ovulation test) with the instructions was provided to each participant. It was
suggested that the ovulation is expected to occur from day eight to 18 from beginning
of menstruation (McVay, Copeland, Newman & Geiselman, 2012). Each participant
was given 10 ovulation strips per cycle. A positive test indicates the end of the
follicular phase and the beginning of the luteal phase. Detecting ovulation by
measuring urinary LH surge is considered to be a valid and reliable method (Rudy,
Ellen & Patricia, 1992).
53
3) Food Record: this was used to measure the food intake of each subject (Appendix G).
An instruction sheet that includes guideline of how to record the daily food intake
was provided to the participants. The food record is derived from (Ha, & Caine-Bish,
2009). Each subject completed three days food required for each phase for two
months (three during the menstrual phase, three during the follicular phase, and three
during the luteal phase). At the end, each subject has a total of 18 food records. The
recorded dietary intake was analyzed using Food Processor SQL (Version10.8, year
2011; ESHA Research, Salem, OR).
4) Craving Screening: with each food record, participants completed a food craving
survey that included the following: a) 100mm Visual Analog Scale (VAS) to measure
the appetite, hunger, and mood status. This was derived from (McVay, Copeland,
Newman & Geiselman, 2012). The Visual analog scale is considered a valid method
in measuring appetite (Stubbs, Hughes, Johnstone, Rowley, Reid, Elia, & Blundell,
2000) and mood (Monk, 1989). b) An initial food craving questionnaire that was
derived from (Cohen, Sherwin & Fleming, 1987). This was used to measure the
craving type and intensity. Each participant completed nine craving screening survey
per cycle.
5) Food Craving Record: The food cravings during menstrual cycle will be measured
using a Craving Record by (Massey & Hill, 2012) (Appendix H part A). Participants
completed this form every time they have a craving episode whether they consume
the craved item or not. The Craving Record consists of questions about the location,
triggers and time of the caving experience. Visual analogue scale (100 mm) was used
54
in order to measure the hunger level and the intensity of the craving episode (strength,
difficulty resisting, target food restriction, and speed of disappearance). Measuring
the mood before and after craving was by using the UWIST Mood Adjective
Checklist (Matthews, Jones, & Chamberlain, 1990), where three categories for mood
status were used and each one contains 4 adjectives (Hedonic tone: happy, sad,
dissatisfied, contented), (Tense arousal: nervous, calm, tense, relaxed), (Energetic
arousal: sluggish, tired, energetic, alert). Participants were required to choose one of
four responses (extremely “3”, moderately “2”, slightly “1”, and not at all “0”). The
permission for using this survey can be found in appendix H part B.
6) The Mental and Physical Symptom Daily Rating Scale: similar to the one used in the
preassessment phase. The aim was to measure the severity of PMS and PMDD
symptoms during the luteal phase. Each participant was given this scale attached to
the three day food record in the luteal phase.
Procedure
A web based survey was administered during the spring 2014 semester at Kent
State University. Email included the purpose of the study, inclusion and exclusion
criteria, the consent form (appendix A)and the preassessment survey was sent to the list
serve in the college of education, health and human services graduate program, college of
nursing, college of public health, and Kent State Women Center. In addition, flyers were
posted in many on campus buildings .The flyers contain information about the purpose of
the study, inclusion and exclusion criteria, and contact information of the research
investigator. The consent form and the survey were created using Qualtrics Syrvey
55
Software. Participants were asked to disclose their name and contact information (email
or phone) in order to contact them if they pass the preassessment phase. Eligible
participants were contacted through email that contains detail explanation for the
assessment phase of the study.
The assessment phase was divided into three parts (menstrual phase follicular
phase, and Luteal phase (Appendix I). Each phase has color coded folder that contains the
required document to be completed. The investigator conducted three meetings per cycle
with each participant to give instructions for the current phase and to take the completed
document for the previous phase. The same process was repeated in the second cycle.
The Menstrual Phase was the starting point for each participant. A red folder was
given to each subject that contains 1) Daily menstrual cycle track record, where
participants record the dates beginning with the first day of menses until it ends. 2) The
Food record, for three consecutive days: 2nd, 3rd, 4th day. 3) A craving screening survey,
completed in the same days of the food record. 4) The Craving Record, which was
completed when having the craving episode. This phase ends on the last day of menses.
Then, participants meet the investigator to take the next phase folder and to submit the
red folder.
The Follicular Phase, which follow the menstrual phase, a green folder was given
to each subject that contains: 1) Daily menstrual cycle track record, where participants
record the dates beginning with the first day of the follicular phase until it ends 2) The
Food record, for three consecutive days: 10th,11th, and ovulation day. 3) A craving
screening survey, completed in the same days of the food record. 4) The Craving Record,
56
which was completed when having the craving episode. 5) LH urine test, to detect
ovulation. Ovulation is the indicator for ending the follicular phase and beginning the
luteal phase. When the participant gets a positive ovulation test, she records it on the
daily menstrual cycle tracking record, contacts the investigator, and exchange folders.
The Luteal Phase, which follow the menstrual phase, a blue folder was given to
each subject that contains 1) Daily menstrual cycle track record, where participants
record the dates beginning with the first day of the luteal phase until it ends 2) The Food
record, for three consecutive days: (22th, 23th, and 24th day). 3) A craving screening
survey, completed in the same days of the food record. 4) The Craving Record, which
was completed when having the craving episode. 5) PMS scale was used to measure the
severity of PMS and PMDD. When this phase ends, by the beginning with the next
menstrual phase, this was the ending of a complete cycle. Subject submit this folder and
start a new cycle, menstrual, follicular and finally luteal phase.
Data Analysis
The data was entered by the Kent State University Research Beauru using the
social science (SPSS, version21) and significant level of (p≤0.05)
Pre Assessment Phase
Health History Questionnaire (age, BMI, menstrual cycle length and frequency,
hormonal use, medical status, exercise pattern) was summarized as a descriptive
statistics.
EAT-26 was scored as follows, questions 1 to 25 (Always=3, usually =2, often=1,
sometimes, rarely, and never =0), question 26 (Always, usually, often=1, sometimes=1,
57
rarely=2, and never =3). A score of 20 or above indicates a high level of concern
regarding eating habits and behavior (Garner et al., 1982). Detailed description for the
EAT-26 and the behavioral test can be found in appendix C part B. Data was summarized
as a descriptive statistic (frequency and percent concern of ED and No concern for ED)
and (frequency and percent behavioral problem and no behavioral problem)
The Mental and Physical Symptom Daily Rating Scale consist of 28 questions
where (severe=3, moderate=2, slight=1, and not at all=0). Scoring one or more of the
severe symptoms for two menstrual cycles is an initial diagnosis of PMS, while scoring
five or more of the severe symptoms will be considered as having PMDD (Freeman,
2003). Data was summarized as descriptive statistics (frequency and percent of PMS and
PMDD).
The craving history data (food craving experience, relation to other food, relation
to emotion and menstrual cycle) were summarized as descriptive statistics (frequency and
percent).
Assessment Phase
Food Records were analyzed using the Food Processor Software. Food items were
converted into total calories and grams of macronutrients (carbohydrate, protein, and fat).
The percentage of daily intake was calculated by dividing the actual intake by the
recommended intake and multiplying the result by 100. The recommended energy intake
was calculated using the DRI (Dietary Reference Intake) formula Adapted from (Otten, et
al., 2006).
58
EER (Estimated Energy requirement) = 354 - (6.91 x age [years]) + Physical Activity x
[(9.36 x weight [kg]) + (726 x height [ml])
The recommended macronutrients intake was calculated by the food processor
according to the recommended daily intake (RDI) for carbohydrate, protein and fat,
adapted from (Dietary Reference Intakes for Macronutrients, 2002).
The BMI (Body Mass Index) was calculated by dividing the weight (kg) by height (m²)
Data from the food records were analyzed using Rpeated Measure Analysis of
Variance (RM ANOVA) to compare the percentage of calories, fat, carbohydrates and
protein in subjects’ diets between the 3 phases of the cycle (menstrual, follicular, and
luteal).
Data from the Craving Screening test was analyzed using 3 (phases M,F,L) by 2
(craving vs non craving) ANOVA to see whether a difference exists between the cravers
and non-cravers in (hunger, satiety, stress, relaxation, anxiety, rate of craving, consuming
the food, breaking regular diet, and eating as usual) and also between the 3 phases.
Data from the Craving Records were analyzed using Repeated Measures Analysis
of Variance (RM ANOVA) to compare (the hedonic tone, tense arousal, energetic arousal
hunger level, strength and pleasantness of craving, resisting the craving) between pre and
post craving and across the three phases . Al so simple analysis of variance was used to
compare between the three phases in the strength of craving and restricting the craved
food.
CHAPTER IV
JOURNAL ARTICLE
Introduction
Each month, women during the reproductive age will have a menstrual
cycle(Goodman, 2003; Levy & Lightman, 1997) that lasts 28 days on average (Carr &
Blackwell, 1993; Barbieri, Jaffe & Yen, 1999; Silberstein & Merriam, 2000). During the
menstrual cycle, women’s body will experience physiological and psychological
fluctuations (Rapkin, 2003) this might have a great impact on the quality and quantity of
the food consumed, therefore, cause an imbalance in diet pattern. Approximately 74
percent of women experience food cravings during the menstrual cycle (Dye, Warner &
Bancroft, 1995).
Balanced and healthy diet is essential to maintain healthy body weight, however,
many researchers found that appetite and dietary intake are affected during different
phases of the menstrual cycle (Dye & Blundell, 1997). Essentially, the proposed cause of
changing dietary intake was hormonal fluctuations, primarily estrogen and progesterone
(Howe, Rumpler & Seale, 1993). The elevation in progesterone level during the luteal
phase was found to be associated with an increase in food intake, while elevation
estrogen level during the follicular phase was found to be associated with decrease food
intake (Dalvit-McPhillips, 1983; Johnson, Corrigan, Lemmon, Bergeron & Crusco, 1994;
Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988).
The dietary intake was studied and measured by analyzing the macronutrients
intake (carbohydrate, fat, and protein) and the total energy intake throughout various
59
phases of the menstrual cycle (Tarasuk & Beaton, 1991; Lyons, Truswell, Mira, Vizzard
& Abraham, 1989; Lissner, Stevens, Levitsky, Rasmussen & Strupp, 1988; Gong, Garrel
& Calloway, 1989). The common findings between these studies were an increase in
dietary consumption during the luteal phase when compared to the menstrual and the
follicular phase.
The cravings of food were investigated by measuring the intensity rate and type of
food items that is craved. Many opinions have been proposed about the food craving
phenomenon, some researchers considered the process of food craving to be a response
from the women’s body to the increase level of energy expenditure or to dietary
deficiency (Yen et al., 2010), while others associated it to hormonal and psychological
changes during menstrual cycle (Cohen, Sherwin, Fleming, 1987), though, Rabinovitz
(2005) suggested that craving for particular food is mainly results from psychological
purpose to relief intense desire for that food in addition to stress or tension .Moreover,
several studies have linked the episodes of food craving during the menstrual cycle with
psychological conditions such as depression, PMS, and PMDD (Dye, Warner &
Bancroft, 1995; Yen, Chang, Ko, Yen, Chen, Yeh & Chen, 2010; Smith & Sauder, 1969).
Comparing to the menstrual and follicular phase, the luteal phase tend to have the highest
craving episodes, and chocolate was found to be among the most craved food items (Hill
& Heaton-Brown, 1994; Hormes & Timko, 2011). During the menstrual cycle, women
who have high craving episodes found to have low control of body weight and feeling of
guilt associated with the craving process (Hormes & Timko, 2011).
60
61
The aim of this study was to determine if dietary changes and food cravings occur
during the menstrual cycle.The hypotheses were 1) There is a change in dietary intake
during the menstrual cycle, and 2)Women experience food cravings during menstrual
cycle.
Methodology
The research design was a descriptive, quantitative comparative analysis of the
participant’s dietary intakes and food cravings through the three different menstrual cycle
phases.
Design
The independent variables were the menstrual cycle phases (menstrual phase,
follicular phase, and luteal phase). The dependent variables were dietary intake, energy
consumption (Kcal) and macronutrients (carbohydrates, proteins, and fat).
Participants
Participants were recruited using a convenience sample of women (students,
faculty, and staff) attending Kent State University, in Kent Ohio. The inclusion criteria
were women between the age of 18 to 40 years, and having normal menstrual cycles (25
to 35 day cycle). Exclusion criteria were using or used exogenous hormones in the past 6
months (oral contraceptives, injections, implant), or planning to use it for the next 2
months, planning to get pregnant in the next two months, irregular menstrual cycles (<25,
˃35 days), using medications that affect appetite, reporting psychological or medical
condition that interfere with normal menstruation, having high rate of eating disorder
62
(score of ˃20 in the EAT-26), complaining of PMDD, intensive exercise (more than 7
hours per week), having high or low body weight (BMI <18, or ˃25).
Measures
An online survey was used as an initial screening test to determine the eligible
subjects to participate in the study.
Pre assessment phase. The pre assessment phase consists of four sections:
1) Health History Questionnaire was used to measure age, weight, height, BMI (kg/m2),
exercise intensity (hours/week), menstrual cycle pattern (length and frequency of the
cycle), usage of oral contraceptives, and the presence of any medical condition that
interfere with the menstrual cycle.
2) Eating Attitude Test-26 (EAT-26) was used to detect the signs of eating disorders
(Garner et al., 1982). The EAT-26 consists of 26 questions that are answered based
on a six-point Likert-Scale (Always =3 points, usually = 2 points, often =1 point,
sometimes, rarely and never = 0). This test covers four areas: dieting behaviors,
bulimia, preoccupation with food and oral control. A score of 20 or higher on this test
indicates concern about eating habits. The second part of the EAT-26 consists of five
questions that measures the eating behavior using a Likert scale (Never, once a month
or less, two to three times a month, once a week, two to six times a week, once a day
or more).
3) The Mental and Physical Symptom Daily Rating Scale was used to measure the
severity of PMS and PMDD symptoms (Dhar & Pearson Murphy, 1990). This scale
consists of 28 questions that focus on three categories: questions 1 to 12 focus on the
63
mental symptoms, questions 13 to 21 focus on the physical symptoms, questions from
22 to 28 are miscellaneous information. The symptoms were rated based on five
points Likert-Scale (severe, moderate, slight, and not at all). Scoring one or more of
the severe symptoms for two menstrual cycles is an initial diagnosis of PMS, while
scoring five or more of the severe symptoms will be considered as having PMDD
(Freeman, 2003). Participants who fall in the PMDD category were excluded from the
study.
4) A food craving questionnaire used to measure the past food craving experience, type
and frequency of the craving and whether it is linked to the emotional status and to
the menstrual cycle (Weingarten & Elston,1991).
Assessment phase. This is the second part of the study where eligible
participants started recoding their food diary and cravings, and also tracking their
menstrual cycle every day for two consecutive months. During this stage, six
measurement methods were used:
1) The Menstrual Cycle Tracking Record was used to record the beginning and ending
date of each phase of the cycle. The menstrual phase begins with the first day of
bleeding and ends by the end of bleeding. The follicular phase begins with the end of
menstrual phase and ends with ovulation. The luteal phase begins with ovulation and
ends with the first day of the next menses. This process was repeated twice as each
subject completed two cycles. This record helps to measure the length of each phase
and cycle and make sure that each cycle was within the normal range (25-35 days).
64
2) LH test is a urine test that measures Luteinizing hormone (LH) surge and this was
used to detect the process of ovulation. The LH surge detection kit (Easy @Home
ovulation test) with the instructions were provided to each participant .It was
suggested that the ovulation is expected to occur from day 8 to 18 from beginning of
menstruation (McVay, Copeland, Newman & Geiselman, 2012). Each participant was
given 10 ovulation strips per cycle. A Positive test indicates the end of the follicular
phase and the beginning of the luteal phase. Detecting ovulation by measuring urinary
LH surge is considered to be a valid and reliable method (Rudy, Ellen & Patricia,
1992).
3) The Food Record derived from (Ha, & Caine-Bish, 2009), was used to measure the
food intake of each subject.Each subject completed 3 days food record per phase for
two months (three during the menstrual phase, three during the follicular phase, and
three during the luteal phase). At the end, each subject submitted a total of 18 food
records. The recorded dietary intake was analyzed using Food Processor SQL
(Version10.8, year 2011; ESHA Research, Salem, OR).
4) The Craving Screening, with each food record, participants completed a food craving
survey that included the following: 100mmVisual Analog Scale (VAS) that measured
appetite, hunger, and mood status, this was derived from (McVay, Copeland,
Newman & Geiselman, 2012).The Visual analog scale is considered a valid method
in measuring appetite (Stubbs, Hughes, Johnstone, Rowley, Reid, Elia, ... & Blundell,
2000) and mood (Monk, 1989).in addition to the VAS, an initial food craving
65
questionnaire was used to measure the craving type and intensity (Cohen, Sherwin &
Fleming, 1987). Each participant completed 9 craving screening surveys per cycle.
5) The Food Craving Record was used to detect craving episodes (Massey & Hill,
2012). Subjects completed this form every time they had a craving episode whether
they consume the craved item or not. This Record consists of questions about the
location, triggers and time of the caving experience. Visual analogue scale (100 mm)
was used in order to measure the hunger level and the intensity of the craving episode
(strength, difficulty resisting, target food restriction, and speed of disappearance).
Measuring the mood before and after craving was by using the UWIST Mood
Adjective Checklist (Matthews, Jones, & Chamberlain, 1990), where three categories
for mood status were used and each one contains 4 adjectives (Hedonic tone: happy,
sad, dissatisfied, contented), (Tense arousal: nervous, calm, tense, relaxed),
(Energetic arousal: sluggish, tired, energetic, alert). Participants were required to
choose one of four responses (extremely “3”, moderately “2”, slightly “1”, and not at
all “0”).
6) Mental and Physical Symptom Daily Rating Scale is the same PMS/PMDD scale that
was used during the pre-assessment phase. The aim was to measure the severity of
PMS and PMDD symptoms during the luteal phase. Each participant was given this
scale attached to the 3 day food record in the luteal phase.
66
Procedure
During the spring 2014 semester at Kent State University, emails were sent to the
listserve in many colleges and also to the women's center. In addition, flyers were posted
in many on campus buildings.
Pre assessment phase. Both emails and flyers contain the purpose of the study,
inclusion and exclusion criteria, and contact information of the research investigator to
contact if interested to participate in the study. The email already attached with links of
the consent form and the preassessment survey that were created using Qualtrics Survey
Software. Participants were asked to disclose their name and contact information (email
or phone) in order to contact them if they pass the preassessment phase. Eligible
participants were contacted through email that contains a detailed explanation for the
assessment phase of the study.
After completing the Preassessment online survey, data were analyzed and each
participant who met all the following criteria was contacted by email to further describe
the second part of the study, the general criteria were: women age between18 to 40 years,
normal menstrual cycles not using exogenous hormones, not using medications or
complaining of medical problem that interfere with normal cycle and appetite, normal
BMI, normal EAT-26 and PMS scores and not participating in sport that require intense
exercise. Eligible participants must satisfy all the previous criteria. Participants who
failed to meet these criteria were excluded from proceeding to the next phase.
Assessment phase. Eligible participants received email that they passed the first
stage of the study, the email contains detailed explanations about the second stage and
67
also a list of dates to schedule appointments with the investigator for further explanation
and to take the documents required to complete in the first phase of the cycle.
The assessment phase was divided into three parts (menstrual phase, follicular phase, and
luteal phase) Each phase has color coded folder that contains the required document to
complete. The investigator conducted three meetings per cycle with each participant to
give them instructions about current phase and to take the completed document for the
previous phase, each meeting lasts about 10-20 minutes. The same process was repeated
in the second cycle.
1) The Menstrual Phase was the starting point for each participant. A red folder was
given to each subject that contains 1) Daily menstrual cycle track record, where
participants record the dates starting with the first day of menses until it ends. 2) The
Food record, for three consecutive days: 2nd, 3rd,4th day of the cycle. 3) A craving
screening survey, completed in the same days of the food record. 4) The Craving Record,
which was completed when having the craving episode. This phase ends on the last day
of menses. Then, participants meet the investigator to submit current phase folder and to
take the next one.
2) The Follicular Phase follows the menstrual phase, a green folder was given to
each subject that contains: 1) Daily menstrual cycle track record, where participants
record the dates beginning with the first day of the follicular phase until it ends 2) The
Food record, for three consecutive days: 10th,11th, and ovulation day. 3) A craving
screening survey, completed in the same days of the food record. 4) The Craving Record,
which was completed when having the craving episode. 5) LH urine test, to detect
68
ovulation. Ovulation was used as an indicator for ending the follicular phase and
beginning the luteal phase. When the participant gets a positive ovulation test, she
records it on the daily menstrual cycle tracking record, contacts the investigator, and
exchange folders.
3) The Luteal Phase follows the follicular phase, a blue folder was given to each
subject that contains 1) Daily menstrual cycle track record, where participants record the
dates beginning with the first day of the luteal phase until it ends 2) The Food record, for
three consecutive days: 22th, 23th, and 24th day of the cycle. 3) A craving screening
survey, completed in the same days of the food record. 4) The Craving Record, which
was completed when having the craving episode. 5) PMS scale was used to measure the
severity of PMS and PMDD.This phase ends, by the beginning with the next menstrual
phase, which mean completing full cycle. Participants submit this folder and start a new
cycle, menstrual, follicular and finally luteal phase.
Data Analysis
The data were entered by Kent State University Research Bureau using the social
science (SPSS, version 21) and significant level of (p ≤ 0.05).
Pre Assessment Phase
Data from the following measurement methods were analyzed using descriptive
statistics:
1) Health History Questionnaire (age, BMI, menstrual cycle length and frequency,
hormonal use, medical status, exercise pattern). The BMI (Body Mass Index) was
calculated by dividing the weight (kg) by height (m²)
69
2) EAT-26 was scored as follows, questions 1-25 (Always=3, usually =2, often=1,
sometimes, rarely, and never =0), question 26 (Always, usually, often=1,
sometimes=1, rarely=2, and never =3). A score of 20 or above indicates a high level
of concern regarding eating habits and behavior (Garner et al., 1982). Data was
summarized as (frequency and percent concern of ED and No concern for ED) and
(frequency and percent behavioral problem and no behavioral problem).
3) The Mental and Physical Symptom Daily Rating Scale consist of 28 questions where
participants rated each symptom as (severe, moderate, slight, or not at all). Scoring
one or more of the severe symptoms for two menstrual cycles is an initial diagnosis of
PMS, while scoring five or more of the severe symptoms will be considered as having
PMDD (Freeman, 2003). Data was summarized as (frequency and percent of PMS
and PMDD).
4) The craving history data (food craving experience, relation to other food, relation to
emotion and menstrual cycle) were summarized as (frequency and percent).
Assessment Phase
Data from the following measurement methods were analyzed using Repeated
Measures Analysis of Variance (RM ANOVA):
1) The food records, to compare the percentage (%) of calories, fat, carbohydrates and
protein across the three phases of the cycle (menstrual, follicular, and luteal) Food
Records were analyzed using the Food Processor Software, Food Processor SQL
(Version10.8, year 2011; ESHA Research, Salem, OR).
70
Food items were converted into total calories and grams of macronutrients
(carbohydrate, protein, and fat). The percentage of daily intake was calculated by
dividing the actual intake by the recommended intake and multiplying the result by 100.
This was used to measure how many percent of energy and macronutrients each
participant was consuming of their recommended intake. The Food Processor Software
determined the energy requirement for each participant based on the DRI (Dietary
Reference Intake) formula Adapted from: (Otten, et al.,2006). EER (Estimated Energy
requirement) = 354 - (6.91 x age [years]) + Physical Activity x [(9.36 x weight [kg]) +
(726 x height [ml])
The recommended macronutrients intake was calculated by the food processor
according to the recommended daily intake (RDI) for carbohydrate, protein and fat,
adapted from (Dietary Reference Intakes for Macronutrients, 2002).
2) The Craving Records, to compare (hedonic tone, tense arousal, energetic arousal
hunger level, strength and pleasantness of craving, resisting the craving) between pre
and post craving and across the 3 phases.
Data from the following measurement methods were analyzed using Simple
Analysis of Variance (ANOVA):
3) The Craving Records, to measure the strength of craving, restricting the craved food,
difficulty to resist the craving, pleasantness of craved food, and the quick of
disappearance of craving. All these criteria were measured across the three phases of
the cycle.
71
Results
A convenience sample of sixty KSU women (N=60) participated in the initial part
of the study.
Pre Assessment Phase
Table 1 shows the participants’ demographics. The majority of women age was
Table 1
Female Participant Delographics Characteristics (Age, Weight Status, Menstrual
Cycle Status)During the Pre Assessment Phase of the Study (N=60)
Characteristics
n
%
Age group(years)
18-20
21-30
31-40
˃40
11
40
8
1
18.0
65.6
13.1
1.6
BMI a (kg/m²)
≤18. 4 (underweight)
18.5-24.9 (normal)
25-29.9 (over weight)
≥30 (obese)
2
45
6
7
3.3
75.0
10.0
11.7
Normal menstrual cycle
Yes
No
52
8
85.2
13.1
Days between two cycles
20-24
25-29
30-35
36-40
Varies
6
32
18
1
3
9.8
52.5
29.5
1.6
4.9
Note. a BMI: (Body Mass Index) classification was adapted from the World Health
Organization http://apps.who.int/bmi/index.jsp?introPage=intro_3.html
Preassessment phase: is the initial stage of the study where the participants tested to
see if they were eligible to be included in the second stage of the study which is the
assessment phase.
72
between 21 to 30 years (n=40, 65.6%), had normal body weight (n=45, 75.0%) and
reported normal menstrual cycle (n=52, 85.2%) with 25 to 29 day period between cycles
(n=32, 52.5%). Table 2 shows the factors that suggested to interfere with normal
menstrual cycle. Most women participate in regular exercise (n=43, 70.5%), and they do
not follow a strict exercise regimen, with an average 175.70 minutes of sport training per
week (SD=115.58), while only (n=4, 6.6%) of women participate in sports that require
Table 2
Factors Measured during the Pre Assessment Phase that may Interfere with Normal
Menstrual Cycling, and were used to Exclude Women Not Eligible to Participate in the
Study (N=60)
Factors
n
%
Exercise
Yes
No
43
16
70.5
26.2
Sport Training
Yes
No
4
56
6.6
91.8
Hormonal contraceptive
Yes
No
6
54
9.8
88.5
Plan for pregnancy
Yes
No
5
55
8.2
90.2
Medication affects appetite
Yes
No
2
58
3.3
95.1
Medication affects cycle
Yes
No
1
59
1.6
96.7
Disorder affects appetite
No
60
98.4
Disorder affects cycle
No
60
98.4
73
strict training. The majority of them did not report having any medical or psychological
condition or using medications that affect appetite or interfere with regular menstrual
cycle. In addition, most of them did not use hormonal contraceptive or plan for pregnancy
in the next 2 months. Table 3 shows the eating disorder and premenstrual syndrome
scores. EAT-26 test shows that most women didn’t have a high score that indicates
concern for eating disorder (n=52, 85.2%) and only (n=7, 11.5%) had a score of (≥20)
that raise the concern for eating disorder. For the eating behavior section (n=44, 72.1%)
were normal and (n=15, 24.6%) showed a score level of behavior problem that indicate
subjects to be referred to trained mental health professional for consultation. The third
part was the premenstrual syndrome test that shows the majority of participants reported
at least one sever symptoms during the 10 days prior the menstrual phase (n=54, 88.5%),
where (n=7, 11.5%) reported more than five sever symptoms, therefore, fall in the PMDD
category.
A total of 52 participants completed the craving history survey, which was the last
section of the initial screening. Table 4 shows that the majority of participants has
experienced food craving (n=46, 75.5%). The majority responded that there is no food,
other than the craved food, would satisfy the craving (n=37, 72.5%), and most
participants responded that 50 percent of the time they will follow their craving and eat
the craved food. When they were asked about their feeling when they eat the craved food,
the majority (n=25, 41%) responded they feel satisfied. When they were asked if they feel
that the craving is related to their menstruation 36 percent (n=18) responded it is
74
sometimes related, and 20 (n=10)percent responded that it is always related to the
menstrual cycle.
Table 3
Preassessment Screening for Eating Disorders and Premenstrual Syndrome Scores that
Determines Participants Eligibility to Continue the Study (N=60)
Test
Criteria
n
%
EAT-26 b
No concern for ED
Concern for ED
52
7
85.2
11.5
EAT-26 Behavior c
No behavioral problems
Behavioral problems
44
15
72.1
25.4
Premenstrual syndrome d
PMS
PMDD
54
7
88.5
11.5
EAT-26 scoring: is when the sum of the scores is 20 or more, this indicates a high level
of concern about dieting, body weight, or problematic eating behavior. Adapted from
(Garner et al.,1982)
EAT-26 Behavior questions: choosing one or more of the checked boxes this indicates
that participant should seek an evaluation from a trained mental health professional.
ED: Eating disorder.
PMS (Premenstrual syndrome) and PMDD (Premenstrual dysphoric disorder) scale was
adapted from: (Dhar & Pearson Murphy, 1990)
Scoring one or more of the severe symptoms indicates PMS, while scoring more than five
sever symptoms indicates PMDD.
75
Table 4
Craving History Questionnaire during the Pre-Assessment Phase (N=52)
n
%
Experienced food craving
Yes
No
46
6
75.4
9.8
Other food would satisfy
craving
Yes
14
23.0
No
37
72.5
How often do you eat the
craved food
25
3
4.9
35
50
60
70
75
80
90
100
1
15
4
1
4
7
6
5
1.6
24.6
6.6
1.6
6.6
11.5
9.8
8.2
Feeling when ate craved food
Dissatisfied
Somewhat dissatisfied
Neutral
Somewhat satisfied
Satisfied
Very satisfied
1
1
5
5
25
14
1.6
1.6
8.2
8.2
41.0
23.0
Craving related to the
menstrual cycle
Never
1
2.0
Rarely
Sometimes
Often
Usually
Always
3
18
8
9
10
6.0
36.0
16.0
18.0
20.0
76
Assessment Phase
Of the 60 women who completed the initial survey, only 18 were eligible to
proceed and start the assessment phase. Reasons for exclusion were (age ˃40 or <18,
abnormal BMI ≤18. 4 or ≥25, abnormal menstrual cycle <25or ˃35 days, follow a strict
exercise pattern, use hormonal contraceptives, plan to get pregnant, complain of any
medical or psychological condition or using medications that affect appetite or menstrual
cycle, score ≥20 in the EAT-26 or check any of the categories in the eating behavior test
that require health consultation, and fall into the PMDD category. In addition, some
participants who were eligible to participate decided not proceed to the assessment phase.
Eligible participants’ characteristics. Table 5 summarizes the characteristics of
participants who satisfied the criteria to participate in the second part of the study. The
majority of the women’s age group was between 21 to 30 year (n=12, 66.6%). All
participants had normal BMI and normal menstrual cycle, does not use hormonal
contraceptives, medication or had medical illness that affects appetite or menstrual cycle,
and had normal EAT-26 score. None of them fell into the PMDD category, while only
(n=7, 38.8%) fell into the PMS category. Most of the participants were engaging in
regular exercise (n=15, 83.3%) and none of them were participating in a sport that
required intense training.
77
Table 5
Eligible Participant Characteristics (Health History Questionnaire, and PMS Scale)
(N=18)
Characteristics
n
%
Age group (years)
18-20
21-30
31-40
4
12
2
22.2
66.6
11.1
BMI (kg/m²)
18.5-24.9 (normal)
18
100
Days between two cycles
25-29
30-35
13
5
72.2
27.7
Exercise
Yes
No
15
3
83.3
16.6
Premenstrual syndrome
PMS
PMDD
7
0
38.8
00.0
Food record. Table 6 shows the average percentage of energy and
macronutrients (carbohydrates, protein, and fat) across the three phases of the cycle. No
significant differences were found between the three phases (P ˃0.05). Table 7 shows the
mean intake of kilocalories, grams of macronutrients across that three phases.
78
Table 6
Food Record Data are Summarized as Mean (M) and Standard Deviation (SD) of
the Percent of Recommended Intake of Energy and Macronutrients during the Three
Phases of Menstrual Cycle (N=14)
Nutrient
Phase
M
SD
P
Energy (%) a
Menstrual
Follicular
Luteal
69.58
62.58
63.01
21.05
14.36
14.68
0.34
Carbohydrate (%)b
Menstrual
Follicular
Luteal
64.80
63.08
61.71
21.22
15.60
18.98
0.833
Protein (%)c
Menstrual
Follicular
Luteal
132.48
132.16
123.35
30.29
47.89
41.48
0.57
Fat (%)d
Menstrual
Follicular
Luteal
77.50
67.44
70.28
21.25
21.66
17.75
0.39
Note. Percent of recommended intake was calculated by dividing the actual intake by the
recommended daily intake multiplied by 100.
79
Table 7
Food Record Data Summarized as Mean (M) and Standard Deviation (SD) of Energy
(kcal) and Mean Grams of Carbohydrates, Mean Grams of Protein, and Mean Grams of
Fat during the Three Phases of Menstrual Cycle (N=84 )
Nutrient
Phase
N
M
SD
Energy (kcal)
Menstrual
Follicular
Luteal
Total
28
30
25
83
1717.01
1490.55
1497.27
1569.00
460.80
402.31
347.61
416.93
Carbohydrate (g)
Menstrual
Follicular
Luteal
Total
28
30
26
84
220.77
202.91
200.63
208.16
65.67
49.51
59.34
58.32
Protein (g)
Menstrual
Follicular
Luteal
28
30
26
70.97
63.16
59.17
22.48
23.81
19.44
Total
84
64.53
22.36
Menstrual
Follicular
Luteal
28
30
26
63.24
52.15
50.32
20.65
20.83
16.57
Total
84
64.53
22.36
Fat (g)
80
Food craving record. Table 8 shows the results of the food craving records.
These records were completed by participants when they experience a craving episode
throughout the cycle, whether they ate the craved item or not. The data show that there
were more craving records submitted during the menstrual phase. Mood State before and
after craving and across the phases was measured as hedonic tone, tense arousal and
energetic arousal. There was no significant difference in hedonic tone and energetic
arousal, however, tense arousal pre and post craving was highly significant F (1, 52)
=7.99, P=0.007. The 100mm VAS shows a significant difference in hunger level between
pre-craving and post craving with a decrease in hunger level after craving F (1,56)=
36.03, P ≤ 0.001. However, no significant difference was found between the phases.
Strength of craving pre-craving (M=71.53, SD=15.69) and pleasantness of craved
food item post-craving (M=79.00, SD=15.64) were significantly higher during the
follicular phase compared to the other two phases F (2, 40) =4. 24, P=0. 02.
Table 9 shows that restricting the craved food was higher during the luteal phase
(M= 59.00, SD= 28.96), however, there was no significant difference with the other
phases. The strength of craving was slightly high in all phases, with no significant
difference during the cycle. Pleasantness of craved food was found to be significantly
different between the follicular and luteal phase with high pleasantness during the
follicular phase and lowest during the luteal phase, F(2)=4.64, P=0.15.
81
Table 8.
The Mean Difference of Food Craving Characteristics Pre and Post the Craving Episode
across the Three Phases M (Menstrual), F (Follicular), L (Luteal) at Significance Level
of P=0.05
Criteria
n
Phase
M (SD)
pre-craving
M (SD)
post-craving
P
Hedonic tone a
21
18
18
M
F
L
4.85(2.41)
4.44(2.09)
4.85(2.41)
5.33(1.87)
5.00(2.08)
4.05(1.58)
0.41
Tense arousal b
21
17
17
M
F
L
3.33(1.52)
3.17(1.70)
3.82(1.87)
2.76(1.44)
2.70(1.44)
3.05(1.56)
0.007 *
Energetic arousal c
21
17
17
M
F
L
5.04(2.10)
4.58(2.18)
5.29(2.08)
5.19(2.22)
5.64(1.80)
5.70(2.86)
0.08
Hunger level d
22
17
20
M
F
L
51.18(32.10)
49.94(25.03)
52.90(25.84)
32.27(29.27)
20.23(16.33)
29.10(23.93)
≤ 0.001*
Note. Food Craving Record adapted from Dieting and food craving. A
descriptive, quasi-prospective study by (Massey & Hill, 2012).
a
Hedonic tone (happy, sad, dissatisfied, contented), b Tense arousal (nervous, calm, tense,
relaxed), c Energetic arousal (sluggish, tired, energetic, alert).
*
Significance difference at level of significance P=0.05
d
100 mm VAS (visual analog scale) used to measure hunger level, where 0= not hungry
at all, and 100= very hungry.
82
Table 9
The Mean Difference of Food Craving Criteria on a Scale of 100 during the Three
Phases of the Menstrual Cycle
Criteria
Phase
N
M (SD)
P
Restricting craved item
M
F
L
22
18
20
37.18(31.05)
48.83(27.82)
59.00(28.96)
0.064
Strength of craving
M
F
L
23
19
21
64.47(19.3)
65.63(18.90)
62.28(23.59)
0.873
Difficulty to resist craving
M
F
L
23
19
21
49.08(26.61)
60.73(26.87)
57.38(25.06)
0.33
Pleasantness of craved food
M
F
L
16
13
14
72.62(21.63)
79.00(15.64)
56.14(22.36)
0.015*
Quick of disappearance of
craved food
M
22
68.90(20.33)
0.19
F
17
55.11(26.85)
L
20
62.65(23.43)
Note. Food Craving Record adapted from Dieting and food craving. A descriptive,
quasi-prospective study by (Massey & Hill, 2012)
M (Menstrual), F (Follicular), L (Luteal).
*
Significance difference at level of significance P=0.05
83
Discussion
The purpose of this study was to measure the dietary intake and food craving
between different phase of the menstrual cycle (menstrual, follicular, and luteal phase) in
normal menstruating women attending Kent State University in Kent, Ohio. The first
hypothesis was that there are changes in dietary intake between different phases of the
normal menstrual cycle. The second hypothesis was women experience food cravings
during the menstrual cycle. The study results indicated there are no significant
differences between the three phases in energy and macronutrient consumption (P ˃0.
05); therefore, the research hypothesis was rejected. On the other hand, food craving
episodes did exist throughout the menstrual cycle; therefore the second hypothesis was
accepted.
Dietary Intake During the Menstrual Cycle
Previous studies suggested that food intake (energy and macronutrients) was
significantly different between the three phases of the cycle. It was found that the luteal
phase, which occur with the ovulation stage until the beginning of menstruation, this
phase characterized by major increase in dietary intake. It was found to be associated
with significantly high fat intake compared with the follicular phase (Johnson et al.,
1994; Tarasuk & Beaton, 1991). In addition, this phase was characterized by high levels
of carbohydrates in relation to the other phases (Dalvit-McPhillips, 1983), and it was
found to be higher in energy (Kcal) intake (Lissner et al., 1988; Gong, Garrel &
Calloway, 1989; Hill & Heaton-Brown, 1994). In contrary, the results from this study
show no significant difference in energy and macronutrient intake during three phases of
84
the menstrual cycle (P <0.05). Although the result of the study did not show significant
differences in craving between the luteal phase and the other two phases, the craving
screening test that was completed by the participants with each food record, indicated
participants were less relaxed (P ≤0.001) during the luteal phase (M=44.94, SD= 24.63)
when compared with the follicular phase (M= 57.76, SD=23. 29). One of the major
findings in this study was the percentage of energy and macronutrients intake. Although
the selected participants showed normal scores in the initial eating disorder test during
the pre assessment phase, after analyzing the food records and calculating the percentage
of the recommended intake, it was found that theses participants were consuming less
than the recommended intake of energy, carbohydrates and fat.
Food Craving During the Menstrual Cycle
Previous studies found that food craving was related to the menstrual cycle, and
it was found to occur in 74.3 percent of 5549 women (Dye, Warner & Bancroft, 1995).
When the causes of food craving were investigated in women, it was suggested that the
process of food craving is a response from the women’s body to the increased level of
energy expenditure or to dietary deficiency. Also, it is considered to be a result of
hormonal fluctuation during the menstrual cycle, or a response to negative emotions and
stress (Yen et al., 2010). The food craving results for the present study supported the
second hypothesis which indicated that food craving exists during the menstrual cycle in
normal menstruating women. In contrary to studies that suggested craving was higher
during the luteal phase by approximately 67 percent when compared to the menstrual and
follicular phase (Hill & Heaton-Brown, 1994; Hormes & Timko, 2011), the current study
85
findings suggested that food craving existed throughout the cycle, during the three
phases, and was not significantly related to specific phase .The total craving records
(n=63) were completed by the 18 participants during the two months cycle (23 records
during menstrual phase, 19 during the follicular phase, and 21 during the luteal phase),
which resulted in food craving episode that existed at any phase of the cycle and
sometime more than one phase per cycle.
Dietary Restriction During the Menstrual Cycle
In current study, many factors that may influence the dietary intake of our
participants were controlled, such as medications, sport, weight status, eating disorder
test, premenstrual syndrome test. However, it was found that participants who scored
normal in all the pre-assessment tests, and after measuring their diet intake across the
menstrual cycle, the caloric intake was lower than their recommended daily value. The
average caloric intake of participants in all the three phases was 65 percent of the
recommended caloric intake. These participants looked healthy and normal and did not
show signs of eating disorder when tested using the EAT-26, however, food craving was
prevalent across the cycle. While some participants did consume the craved food, some
of them showed restrictive diet behavior, especially when they were asked (what did they
do instead of not consuming the craved food item), some answers were as following:
“Continue shopping, kept driving, go to sleep, did nothing, stopped thinking about it
while walking, closed my eyes and stopped thinking about it, chewed gum and drank
water, ate a snack instead (Greek yogurt instead of pasta), plan to eat it tomorrow, just
drank water, walk around and ate something different”
86
Restricting the regular diet and avoid eating the craved item or simply force
oneself to stop thinking about the food may explain why there was no significant
difference in energy and macronutrient intake between the three phases of the cycle. One
of the questions in the food record was asking the participants (how much they did you
try to restrict the craved food in the past), the average rates for restricting the craved food
were 55.83 percent during the luteal phase, 37.18 percent during the follicular phase, and
48.83 percent during the menstrual phase. It was suggested that people who chronically
restrict their diet are more susceptible to food craving and experience low self-control
when they are exposed to the craved food item (Polivy, Coleman, & Herman, 2005).
Another study also found that food craving was strongly associated with diet restriction
(Massey & Hill, 2012).
Dietary restriction was considered to be one of the risk factors for food craving
(Pelchat, 1997). Restricting specific nutrients was suggested to be related to change
people’s behavior toward this nutrient, this may lead to food craving and binging
(Coelho, Polivy & Herman, 2006). People who restrict carbohydrate intake found to be
more susceptible to carbohydrate craving when compared with nonrestrictive eaters
(Coelho, Polivy & Herman, 2006). Another study found that when people restrict their
favorite foods, they tend to have more craving episodes comparing when they restrict
regular food item (Polivy, Coleman & Herman, 2005). In addition, when restrained eaters
were exposed to the food cues (smell and taste) of some of the restricted food items, they
found that the restricted eater have more tendency to crave and react to the restricted food
item (Fedoroff, Polivy & Peter Herman, 2003).
87
The definition of food restriction is not clear. Some studies classify participants as
restrictor if they reported that they were dieting or controlling their food intake, or if they
were restricted by the investigator. In many studies, investigator is the one who decided
which food to avoid and which not. They give the subjects guidelines of what to restrict
and then they expose them to the specific food item (e.g. chocolate) (Polivy, Coleman &
Herman, 2005) or food category (e.g. high complex carbohydrate) and they measure
participants’ reaction toward the tested/restricted food .Other studies they use some scales
to measure dietary behavior such as the Revised Restraint Scale (Fedoroff, Polivy &
Peter Herman, 2003) in order to categorize the participants to restraint and non-restraint
groups.
In many studies, participants were exposed to the tested food in order to measure
their reaction or level/intensity of craving episode. In this study, one question in the Food
Craving Record was asked to know what stimulates their craving for specific foods. Data
from 53 completed Food Craving Record throughout the cycle shows that 85% of the
cases (n=45) they reported they were “simply thinking about the craved food”. More
craving existed without even being exposed to food cues like smelling or seeing or tasting
the craved food item.
Women participated in this study had normal BMI, normal EAT-26 score, and not
on a diet. These women experienced food craving at least once per cycle. They were
restricting their carbohydrate, fat and total calories, and thinking about the craved food
item and sometimes trying to avoid eating it and to stop thinking about food. This raises
the concern if they were self-depriving themselves or they were experiencing eating
88
behavior problems that were not detected by all the screening measures we used at the
beginning of the study.
In conclusion, despite what was discovered by most previous research about food
intake and menstrual cycle, this study failed to prove that food intake differs during the
three phases of the normal menstrual cycle. In the other hand, it proofs that food craving
is common among women during the reproductive age, and it exists throughout the
normal menstrual cycle.
Application
When dietitians assess women during reproductive age (18-40 years), it is
important to take into account that during this age period, women are predisposed to
many hormonal and psychological changes as a result of their monthly menstrual cycle.
This will impact their food intake and appetite. As a result, food craving and dietary
intake fluctuations may happen at varying levels. Menstrual cravers were characterized
by having more weight fluctuation, more guilt associated with their craving, and more
dietary restriction (Hormes & Timko, 2011).
The main finding in this study was that all women experienced food craving, and
all women were restricting their diet. The women participating in this study were
subconsciously restricting their diet, as when they were asked at the initial stage (preassessment) if they were following weight controlled diet, they answered “No”. Food
restriction is known to be associated with food craving (Coelho, Polivy & Herman, 2006;
Polivy, Coleman & Herman, 2005; Fedoroff, Polivy & Peter Herman, 2003). There are
many psychological consequences associated with food restriction, therefore, may
89
interfere with the intensity and frequency of food craving episodes. Studies found that
food restriction whether it was intentional or non-intentional, it will lead to many
emotional and cognitive problems that will affect the stability of diet and therefore
weight and general health (Polivy, 1996). Self-restriction was lead participants to be
preoccupied with weight and food, also increase food binging (Polivy, 1996).
Using standard measurement techniques may not be applicable for all women.
There are different measurement scales to determine whether the participants were
restricting their regular diet or not, however, our finding indicate that looking in depth at
the actual intake for many days and analyzing each food item will reflect the actual
consumption and whether it meets the recommended intake or not. Looking at women’s
health status from many angels is crucial; they may have the perfect weight while they
follow unhealthy procedures to maintain this weight such as self-restricting their diet.
When counseling a woman with initial signs of eating disorder or for diet
restraining, it is essential to search for the causes of this condition, by treating the causes
this will help to avoid further complication. Women need to take a part in analyzing their
situation and also in setting the goals that help them to overcome the problem. Dietitian
can use the cognitive behavior therapy (CBT) approach, also depending on the severity of
the case and the symptoms, an enhanced cognitive behavior therapy could be used
(CPT-E) if any of the following symptoms was a leading cause for the problem: clinical
perfectionism, low self-esteem, and interpersonal problems (Murphy, Straebler, Cooper
& Fairburn, 2010).
90
It is essential when dietitians need to give advice to the public regarding healthy
eating, not to focus mainly on eating less or decreasing the calories and fat. This message
may not be applied to all women. Because eating disorder and unhealthy eating practices
are common among women and continuously increasing, the dietitian message need to
take a holistic approach to promoting healthy eating, taking into account the importance
of accepting different body sizes and shapes for women and the importance of enjoying
the food. Promoting the caloric restricted diet as the ideal diet for all women during all
the stages in their life is not acceptable, and may have negative consequences on the
community if everyone perceived the restricted caloric diet as the perfect image of
healthy life style.
Approximately 75 percent of the women participated in this study (n=46)
experienced food cravings in the past.The current sample population of normally
menstruating women showed that food craving exists in all phases of the menstrual cycle,
and it could occur more than once per cycle. Experiencing many food carving episodes
was associated with a high level of anxiety and negative mood (Hill, Weaver & Blundell,
1991). When counseling women that have multiple food cravings that negatively affect
her psychological status and weight, dietitian need to look at the whole picture and see
when and where and under what circumstances these cravings occurs. Knowing the
craving triggers will help to solve the problem. It is essential to use the “Intuitive Eating”
approach when dealing with women, especially when food cravings are the result of food
restrain or even when the cravings are associated with feelings of guilt and emotional
distress. Women need to learn to listen to their body and acknowledge the hunger and
91
satiety cues. Intuitive eating is defined as “responding to the internal physiological
hunger and satiety cues coupled with a low preoccupation with food “(Avalos & Tylka,
2006). Unlike the feeling of hunger which results from psychological demand for food
due to low calorie intake (Pelchat, 2002), craving for certain food is mainly results from
psychological purpose to relief intense desire for that food in addition to stress or tension
(Rabinovitz, 2005). However, in this study, women experienced food craving had also
significant difference of the hunger levels pre and post the craving episode with low
hunger level after consuming the craved food, this may raise the question whether the
craved food, which mainly was high in fat and carbohydrate, are substituting healthy and
nutritious food choices, and whether this may lead to binge eating and cause eating
disorder issues. Women who intuitively eat their food are responding to their body and
reacting to the hunger signals by eating the food and not delaying or ignoring it which
lead to trust the body and being less preoccupied with food (Avalos & Tylka, 2006).
Stopping craving or removing the craved item suddenly from women diet is not
recommended. Gradual change is suggested and cooperating with the women to
formulate their own plan and goals is necessary. It is essential to make the body adapt to
a balanced diet routine every day in order to decrease the sudden and multiple craving
episodes and regulate the hunger and satiety cues. If the food craving was a result of
emotional distress, the dietitian should teach the women techniques to relive the stress,
such as doing favorable exercise or yoga or take a walk, instead of using the food as a
way to relive the stress. If the craving was occasional, women need to learn how to enjoy
the food and listen to their body. However, if the craving was persistent, dietitian need to
92
analyze the type and amount the craved food item and to give suggestions for healthier
choices if the craved food was to affect the women's health.
The social media is considered one of the main resources that influence the public
decision regarding to what and where should they eat and what is considered healthy and
what is not, dietitians need to use this tool to increase the awareness about healthy eating,
in addition they need to educate the women of where to get their daily eating tips and the
importance of only use credible resources. They can use the social media as a resource to
spread the idea of intuitive eating and accepting women with different shapes and sizes,
opposing what is commonly seen image in the media as all women need to be in a
standard shape and size. On the other hand, women need to know that not everything
promoted in the media as the healthy way of living and the best diet, not everything fits to
every woman. Balanced diet is essential; each woman should know what is best for her
health and her age.
The consequences of food craving and diet restriction may not appear in the short
term period. However, there are many known physiological and psychological problems
linked to food craving, including eating disorder and emotional pressure, this will lead to
failing to control weight and therefore affect total health and wellness. The main goal is
to maintain the health and well-being for women and to enjoy the food in a balance way.
Limitations
The current study was limited by the use of a convenience sample. The sample
population size may be a limitation as well because out of the 60 women who
participated in the preassessment phase, only 18 were qualified to participate.
93
Strengths
One of the strengths was the length of the study as each woman was measured for
two months to confirm that they have regular cycles. The menstrual cycle was tracked
daily and the food intake and craving were measured in each phase. In addition, using
tight inclusion criteria, as weight and each woman screened for eating disorder,
premenstrual syndrome and confirming the normal menstrual cycle.
Conclusion
In summary, the result of the current study did not find significant differences in
dietary intake, energy and macronutrients (carbohydrate, protein, and fat), during the
three phases of the normal menstrual cycle. The food records show that the participants
all had a low dietary intake. Total calorie, fat and carbohydrate intake was lower than the
recommended intake, with mean energy intake of 1569 Kcal (65.05 percent of the
recommended intake), 208.16 g of carbohydrate (63.19 percent of the recommended
intake), and 64.53 g of fat (71.74 percent of the recommended intake).
On the other hand, the second hypothesis was accepted as the food cravings
results from the present study indicated that food craving exists during menstrual cycle in
normal menstruating women. In contrary to studies that suggested craving was higher
during the luteal phase (Hill & Heaton-Brown, 1994; Hormes & Timko, 2011), the
current study findings suggested that food craving existed throughout the cycle, during
the three phases, and was not significantly related to specific phase .The total craving
records (n=63) were completed by the 18 participants during the two months cycle (23
records during menstrual phase, 19 during the follicular phase, and 21 during the luteal
94
phase), which resulted in food craving episode that existed at any phase of the cycle and
sometime more than one phase per cycle. Data from 53 completed Food Craving Record
throughout the cycle shows that 85 percent of the cases (n=45) they reported they were
“simply thinking about the craved food”. More craving existed without even being
exposed to food cues like smelling or seeing or tasting the craved food item.
Further studies are needed to examine the dietary behaviors of women during
different phases of the cycle. The intensity of food craving in each phase needs to be
measured. The type of the craved foods needs to be analyzed and measured in correlation
with the severity of food restriction. Women during reproductive age need to be
categorized for different age group and the eating behavior and dietary restriction in each
group need to be tested in depth. In addition, the effect of using the intuitive eating
approach and other techniques to increase the awareness about food and body need to be
measured in each group in correlation with menstrual cycle changes.
APPENDICES
APPENDIX A
CONSENT FORM
Appendix A
Consent Form
Dietary Changes and Food Craving During Normal Menstrual Cycling
IRB# 13-521
Introduction
This study attempts to collect information about dietary intake and food cravings during
menstrual cycle.
Procedures
In order to determine your eligibility for participating in this study, you will be asked to
complete four questionnaire surveys. First is the Health history questionnaire which asks
general health questions such as age and weight, and other questions about the menstrual
cycle. Second is the EAT-26 questionnaire which measures the eating behavior. Third is
the Mental and Physical Symptom Daily Rating Scale which measures several symptoms
that you may experience before the menstruation phase. Lastly, is a Food Craving
questionnaire that measures your past food craving experience. Please note that these
surveys are used for screening and determining the qualified participants to continue for
the next part of the study. The average time of participating in this part of the study will
take no longer than 20 minutes. This questionnaire will be conducted with an on-line
Quartics-created survey.
Eligible participants will proceed to the assessment stage. Several measurement methods
and will last for two months (i.e. two menstrual cycles). Participants are expected to
complete daily menstrual track record, 18 food records during all phases of the menstrual
cycle in which they are expected to record all the food they eat during those days,
Craving record that measures the craving experience only when they crave specific food
.Finally, the ovulation phase will be measured by using (LH) urine test, minimum one
and maximum 10 tests will be used per month depending on the ovulation results.
Negative result of the ovulation test or if you choose not to record the ovulation test
result, this will result in withdrawal from the study.
Risks/Discomforts
Discomfort may occur as the study requires precise tracking of the menstrual cycle and
completing the daily menstrual record. In addition, the food records are required to be
filled during specific days distributed throughout the cycle.
97
98
Confidentiality
Participants need to report their names and contact information either phone number,
email, or both. These information will help the investigator to contact each participant
and meet with them during the assessment stage of the study in order to give them the
surveys and give instructions during each phase of the cycle. In addition, the investigator
will send reminders (text message and email) to remind each participant about the days
they need to fill their surveys and food records.
All data obtained from participants will be kept confidential and will only be reported in
an aggregate format (by reporting only combined results and never reporting individual
ones). All questionnaires will be cancelled, and no one other than ten primary
investigator and assistant researches listed below will have access to them. The data
collected will be stored in the HIPPA-compliant, Qualtrics-secure database until it has
been deleted by the primary investigator.
Compensation
upon completing the study, nine participants will be drawn randomly to receive a cash
payment ($20). All participants who pass the screening (pre-assessment) phase and
proceed to the assessment phase will be included in the compensation drawing whether
they continue the assessment phase or not.
Participation
Participation in this research study is completely voluntary. You have the right to
withdraw at any time or refuse to participate entirely. If you desire to withdraw, please
close your Internet browser and notify the investigator at this email:
([email protected]). Or, if you prefer, inform the principal investigator as you leave.
Questions about the Research
If you have questions regarding this study, you may contact the principal investigator:
Dr. Natalie Caine-Bish at 330-672-2148 ([email protected]), or the co-investigator Amal
K.Albeshri at 267-894-8592 ([email protected])
Questions about Your Rights as Research Participants
If you have questions you do not feel comfortable asking the researcher, you may contact
the research supervisor, principal investigator: Dr. Natalie Caine-Bish at 330-672-2148
([email protected]) or the Kent State University Institutional Review Board, at (330) 6722704.
99
Please type your name (First, Last)
I have read, understood, and printed a copy of, the above consent form and desire of my
own free will to participate in this study.
•
Yes
•
No
APPENDIX B
HEALTH HISTORY QUESTIONNAIRE
Appendix B
Health History Questionnaire
First name
Last name
Email
Mobile number
Weight (lb)
Height (in)
Gender
o Male
o Female
Age category
o 18 - 20
o 21-30
o 31-40
o above 40
Last day of menses
o one week ago
o two weeks ago
o three weeks ago
o Four weeks ago
o More than a month
Do you have normal menstrual cycle?
o Yes
o No
How many days your menses lasts
1-4 days
4-7 days
7-10 days
Varies
How many days do you expect between two menstrual cycle
20 24 days
25-29 days
30-35 days
36-40 days
Varies
101
102
Do you exercise?
o Yes
o No
If yes, type how many minutes per week
Do you participate in specific sport that requires regular training
o Yes
o No
If yes, specify type of sport
Do you use ANY of the following HORMONAL contraceptives (Combined oral
contraceptive pills, Progestin-only pills, Contraceptive patch, Injectable birth control,
vaginal rings, Implantable rods, Emergency Contraceptive Pills?)
o Yes
o No
Do you plan to get pregnant in the next two months?
o Yes
o No
Do you take any medications that affect your appetite?
o Yes
o No
Do you take any medications that affect your menstrual cycle?
o Yes
o No
Do you have any medical disorders that affect your appetite
o Yes
o No
Do you have any medical problem that affects your menstrual cycle?
o Yes
o No
APPENDIX C
EATING ATTITUDE TEST -26 (EAT-26)
104
Appendix C
Eating Attitude Test -26 (EAT-26)
Part A
105
Part B
EAT-26 Permission
APPENDIX D
THE MENTAL AND PHYSICAL SYMPTOMS DAILY RATING SCALE
Appendix D
The Mental And Physical Symptoms Daily Rating Scale
Part A
Please rate each of the following symptoms according to your experience before
menstruation
Symptoms
1. Stay at home, avoid social activity
2. Less work (job, house, school), impaired
3. Mood swings
4. Depressed, sad, low, blue, lonely
5. Anxious, jittery, nervous
6. Irritable, angry, impatient
7. Appetite up, eat more, crave foods
8. More sleep, naps, stay in bed
9. Insomnia
10. Accident-prone
11. Suicidal thoughts
12. Low energy, tired, weak
13. Feel bloated, have swelling
14. Constipated
15. Diarrhea
16. Back, joint, or muscle pain
17. Abdominal pain
18. Nauseated
19. Vomiting
20. Breast pain or discomfort or discharge
21. Headache
22. Vaginal bleeding
107
Not at
all
(0)
Slight
(1)
Moderate
(2)
Severe
(3)
108
Part B
The Mental And Physical Symptoms Dailt Rating Scale Permission
APPENDIX E
FOOD CRAVING HISTORY QUESTIONNAIRE
Appendix E.
Food Craving History Questionnaire
Food Craving History
PART A.
Please answer the following questions
Have you ever experienced food craving (i.e an intense desire for specific food)
o Yes
o No
If Yes, please list the most three craved food
Please indicate how often do you experience that craving (times / month)
Type of food
Times/month
When you are experiencing a craving for certain food, is there any other food which would satisfy
that craving?
o Yes
o No
If yes, Please explain
When you are experiencing food craving, how often you follow through and eat that food ( % of
the time)
110
111
How do you feel when you've eaten the food you craved the most
Very
Somewhat
Somewhat
Satisfied
Neutral
satisfied
Satisfied
Dissatisfied
Do you feel that your cravings are related that your menstrual cycle
Always
usually
often
sometimes
Dissatisfied
rarely
Very
Dissatisfied
never
112
Part B
Food Craving History Questionnaire Permission
APPENDIX F
THE MENSTRUAL CYCLE TRACKING RECORD
Appendix F
The Menstrual Cycle Tracking Record
Menstrual Cycle Track Record (Menstrual Phase)
•
•
•
•
Please fill in the dates.
Day 1 is the first day of menstruation
When you mark the last day of menstruation, this means you finished this phase, and the next
day is the beginning of the (Follicular Phase. Please take the Follicular Phase folder and start
tracking the rest of the cycle
Example: Day 1 ( 02-5-2014), Day 2 (02-6-2014)………Day 7 (02-11-2-14), Day 8 No
Bleeding (This will be Day 1 in the Follicular Phase, go to the follicular phase folder and
start recording)
Day 1
Day 2
Day 3
Day 4
Day 5
Day 6
Day 7
Day 8
Day 9
Day 10
Day 11
Day12
Day 13
Day 14
Day 15
Day16
Day17
Day18
Day19
Day20
DATE
DATE
Menstrual Cycle Track Record (Follicular Phase)
•
•
•
•
Please fill in the dates.
Day 1 is the first day of Follicular Phase ( the day after menstruation ends)
Use the ovulation test during this phase
When the result of the ovulation test = positive ( this is the end of the follicular phase, start in
the Luteal Phase folder)
Day 1
Day 2
Day 3
Day 4
Day 5
Day 13
Day 14
Day 15
Day 6
Day 7
Day 8
Day 9
Day18
Day19
Day 10
DATE
DATE
Day 11
Day 12
114
Day16
Day17
Day20
115
Menstrual Cycle Track Record (Luteal Phase)
•
•
•
•
Please fill in the dates.
Day 1 is the first day of Luteal Phase (the beginning of OVULATION)
This phase ends when you start your menstruation
The beginning of the menstruation is the end of this Luteal Phase and the beginning
of the Menstrual Phase
Day 1
Day 2
Day 3
Day 4
Day 5
Day 6
Day 13
Day 14
Day 15
Day 16
Day 7
Day 8
Day 9
Day 10
Day 18
Day 19
Day 20
DATE
DATE
Day 11
Day 12
Day 17
APPENDIX G
FOOD RECORD
Appendix G
Food Record
FOOD RECORD
Reference no. …………
Day……………….
Date……………….
Phase………………….. . Cycle (1/2)
Time
Meal/
Snack
Food
Item
Ingredients
117
Amount
How
Prepared
Brand
Name
Food
Label
APPENDIX H
FOOD CRAVING RECORD
Appendix H
Food Craving Record
Part A
CRAVING RECORD
Date………………/ Phase…………………
Please complete a new record every time you have a food craving, regardless of whether
or not you eat.
1-Where were you when the craving began?
o At home
o At work
o Other. Specify………..
2-Were you ……
o Alone
o In company
3-What time did the craving begin………….
4-Immediately before the craving did you? (check any that apply)
o
o
o
o
o
o
See or smell the food craved
See or smell other food
Simply think about the food craved
Simply think about other food
Eat the food craved
Eat other food
5. Rate how you felt immediately before the craving
(0=Not at all
1=Slightly
2=Moderately
3=Extremely)
Happy
Dissatisfied
Relaxed
Alert
Nervous
Sluggish
Sad
Calm
Tired
Energetic
Tense
Contented
6. How hungry were you immediately before the craving?
Extremely
Hungry
Not at all
Hungry
119
120
7. How strong was the craving?
Not at all
Strong
Extremely
Strong
8. How difficult was the craving to resist?
Not at all
Difficult
Extremely
Difficult
9. What exactly was the craving for?
• ……………………………..
• ……………………………..
• ………………………………
10. Recently, how much have you tried to restrict eating this food?
Not at all
A lot
11. Did you eat as a result of the craving?
o Yes
o No
12. If “NO”, what did you do instead? ……………………………………………………
13. If “YES”, describe in detail what you ate
• …………………………………………….
• …………………………………………….
• …………………………………………….
• …………………………………………….
14. If “YES”, how long did you resist the craving? ………….minutes
15. If “YES”, how pleasant was the taste of what you ate?
Not at all
pleasant
Extremely
pleasant
16. Having experienced the craving, how quickly did it disappear?
Not at all
Quickly
Extremely
Quickly
17. How hungry were you after the craving?
Not at all
Hungry
Extremely
Hungry
121
18. Rate how you felt after the craving
(0=Not at all
1=Slightly
2=Moderately 3=Extremely)
Happy
Dissatisfied
Relaxed
Alert
Nervous
Sluggish
Sad
Calm
Tired
Energetic
Tense
Contented
122
Part B
Food Craving Record Permission
APPENDIX I
THE FLOW OF THE 3 PHASES OF THE CYCLE
(OVERVIEW OF THE ASSESSMENT PHASE PROCESS)
Appendix I
The Flow Of The 3 Phases Of The Cycle
(Overview Of The Assessment Phase Process)
Preassessment :
Health History
Questionnaire
Eat-26
PMS
Mental and Physical
Symptom Daily Rating
Scale
Food Craving History
Menstrual phase
Menstrual cycle track record
Food Record (3 days)
Craving Questionnaire
Follicular Phase
Menstrual cycle track
record
Ovulation test (LH urine
test)
Food Record (3days)
Craving Questionnaire
Luteal Phase
Menstrual cycle track record
Mental and Physical
Symptom Daily Rating Scale
Food Record (3days)
Craving Questionnaire
124
APPENDIX J
KSU IRB PERMISSION
Appendix J
KSU IRB Permission
Amal Albeshri <[email protected]>
IRB approval for protocol #13-521 - retain this email for your records
2 messages
Wed, Dec 4, 2013 at 12:30 PM
E: IRB # 13-521 entitled “Dietary changes and food craving during normal menstrual cycling”
Hello,
I am pleased to inform you that the Kent State University Institutional Review Board reviewed and
approved your Application for Approval to Use Human Research Participants as a Level
II/Expedited, category 4, 7 project. Approval is effective for a twelve-month period:
December 3, 2013 through December 2 2014.
*A copy of the IRB approved consent form is attached to this email. This “stamped” copy is the
consent form that you must use for your research participants. It is important for you to also keep an
unstamped text copy (i.e., Microsoft Word version) of your consent form for subsequent submissions.
Federal regulations and Kent State University IRB policy require that research be reviewed at
intervals appropriate to the degree of risk, but not less than once per year. The IRB has determined
that this protocol requires an annual review and progress report. The IRB tries to send you annual
review reminder notice to by email as a courtesy. However, please note that it is the
responsibility of the principal investigator to be aware of the study expiration date and submit
the required materials. Please submit review materials (annual review form and copy of current
consent form) one month prior to the expiration date.
HHS regulations and Kent State University Institutional Review Board guidelines require that any
changes in research methodology, protocol design, or principal investigator have the prior
approval of the IRB before implementation and continuation of the protocol. The IRB must also be
informed of any adverse events associated with the study. The IRB further requests a final report
at the conclusion of the study.
Kent State University has a Federal Wide Assurance on file with the Office for Human Research
Protections (OHRP); FWA Number 00001853.
126
127
If you have any questions or concerns, please contact the Office of Research Compliance
at [email protected] or 330-672-2704 or 330-672-8058.
Respectfully,
Kent State University Office of Research Compliance
224 Cartwright Hall | fax 330.672.2658
Kevin McCreary | Research Compliance Coordinator | 330.672.8058 |
[email protected]
Paulette Washko | Manager, Research Compliance |330.672.2704| [email protected]
REFERENCES
REFERENCES
Adams, J., Polson, D. W., & Franks, S. (1986). Prevalence of polycystic ovaries in
women with anovulation and idiopathic hirsutism. British medical journal
(Clinical research Ed.), 293 (6543), 355. Retrieved from
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1341046/pdf/bmjcred002460013.pdf
Acosta, T. J., & Miyamoto, A. (2004). Vascular control of ovarian function: ovulation,
corpus luteum formation and regression. Animal reproduction science, 82,
127-140. Retrieved from http://ac.els-cdn.com/S0378432004000697/1-s2.0S0378432004000697-main.pdf?_tid=5d8e2542-9704-11e2-9dab00000aab0f6b&acdnat=1364405758_ade843dac38ff25df829d9126cd184fc
Angst, J., Sellaro, R., Stolar, M., Merikangas, K. R., & Endicott, J. (2001). The
epidemiology of perimenstrual psychological symptoms. Acta Psychiatrica
Scandinavica, 104(2), 110-116. Retrieved from
http://onlinelibrary.wiley.com/doi/10.1034/j.1600-0447.2001.00412.x/pdf
Avalos, L. C., & Tylka, T. L. (2006). Exploring a model of intuitive eating with college
women. Journal of Counseling Psychology, 53(4), 486.
Barron, M. L., Flick, L. H., Cook, C. A., Homan, S. M., & Campbell, C. (2008).
Associations between psychiatric disorders and menstrual cycle
characteristics.Archives of psychiatric nursing, 22(5), 254-265. Retrieved
fromhttp://ac.els-cdn.com/S0883941708000174/1-s2.0-S08839417080001
129
130
74-main.pdf?_tid=160fe84e-a867-11e2-8612-00000aacb362&acdnat=13663
17328_e126610f96890e6074fc8c1638827b4b
Bancroft, J., & Rennie, D. (1993). The impact of oral contraceptives on the experience of
perimenstrual mood, clumsiness, food craving and other symptoms. Journal of
psychosomatic research, 37(2), 195-202.
Brambilla, F., Monteleone, P., Bortolotti, F., Dalle Grave, R., Todisco, P., Favaro, A., ...
& Maj, M. (2003). Persistent amenorrhoea in weight-recovered anorexics:
psychological and biological aspects. Psychiatry research, 118(3), 249-257.
Retrieved from http://ac.els-cdn.com/S016517810300074X/1-s
2.0-S016517810300074X-main.pdf?_tid=37ccfce2-a952-11e2-9c
19-00000aacb35f&acdnat=1366418316_b1fd9a0fe0010eaeed1c187153e84953
Brandes, J. L. (2006). The influence of estrogen on migraine. JAMA: the journal of the
American Medical Association, 295(15), 1824-1830. Retrieved from
http://jama.jamanetwork.com/article.aspx?articleid=202685
Barsom, S. H., Mansfield, P. K., Koch, P. B., Gierach, G., & West, S. G. (2004).
Association between psychological stress and menstrual cycle characteristics in
perimenopausal women. Women's health issues: official publication of the Jacobs
Institute of Women's Health, 14(6), 235. Retrieved from http://ac.elscdn.com/S1049386704000714/1-s2.0-S1049386704000714main.pdf?_tid=abed45ba-a91a-11e2-91ce00000aacb35e&acdnat=1366394459_67f390fe75d1d52bd35c96be18dbd88a
131
Bisdee, J. T., James, W. P. T., & Shaw, M. A. (1989). Changes in energy expenditure
during the menstrual cycle. British Journal of Nutrition, 61(02), 187-199.
Retrieved from
http://journals.cambridge.org/download.php?file=%2FBJN%2FBJN61_02%2FS0
007114589000279a.pdf&code=f64e0a5c63dc106614e1b68b258da7cd
Barr, S. I., Janelle, K. C., & Prior, J. C. (1995). Energy intakes are higher during the
luteal phase of ovulatory menstrual cycles. The American journal of clinical
nutrition,61(1), 39-43. Retrieved from
http://ajcn.nutrition.org/content/61/1/39.full.pdf
Barbieri, R., Jaffe, R., & Yen, S. (1999). Reproductive endocrinology.physiology,
pathology,and clinical management. (4th ed., pp. 191-211). Philadelphia, PA:
W.B.Saunders company.
Berkey, C. S., Gardner, J. D., Frazier, A. L., & Colditz, G. A. (2000). Relation of
childhood diet and body size to menarche and adolescent growth in girls.
American Journal of Epidemiology, 152(5), 446-452. Retrieved from
http://aje.oxfordjournals.org/content/152/5/446.full.pdf+html
Baird, D. T. (1983). Factors regulating the growth of the preovulatory follicle in the
sheep and human. Journal of reproduction and fertility, 69(1), 343-352. Retrieved
from
http://www.reproduction-online.org/content/69/1/343.full.pdf+html
Baerwald, A. R., Adams, G. P., & Pierson, R. A. (2012). Ovarian antral folliculogenesis
during the human menstrual cycle: a review. Human reproduction update, 18(1),
132
73-91. Retrieved from http://humupd.oxfordjournals.org/content/
18/1/73.full.pdf+html
Bates, G. W., & Whitworth, N. S. (1982). Effects of obesity on sex steroid metabolism.
Journal of Chronic Diseases, 35(12), 893-896. Retrieved from http://ac.elscdn.com/0021968182901205/1-s2.0-0021968182901205-main.
pdf?_tid=bd976228-aab9-11e2-85f200000aacb360&acdnat=1366572730_5d9a93a7060f4a33a78063e3274758bd
Brooks-Gunn, J., Warren, M. P., & Hamilton, L. H. (1987). The relation of eating
problems and amenorrhea in ballet dancers. Med Sci Sports Exerc, 19(1), 4144.Retrieved from http://www.setantacollege.com/wpcontent/uploads/Journal_db/The relation of eating problems.pdf
Baird, D., & Van Look, B. (1980). Regulatory mechanisms during the menstrual cycle.
European Journal of Obstetrics & Gynecology and Reproductive Biology, 11(2),
121-144. Retrieved from http://ac.els-cdn.com/0028224380900180/1-s2.0-002
8224380900180-main.pdf?_tid=4a5e701e-cbf0-11e2-86ee00000aab0f6b&acdnat=1370224547_d0f97c48ff5c40b2e4bb262203b9185c
Bulun, S. E., Gurates, B., Fang, Z., Tamura, M., Sebastian, S., Zhou, J., ... & Yang, S.
(2002). Mechanisms of excessive estrogen formation in endometriosis. Journal of
reproductive immunology, 55(1), 21-33. Retrieved from http://ac.els-cdn.
com/S0165037801001322/1-s2.0-S0165037801001322-main.pdf?_tid=d26c41f
2-a0a8-11e2-97cb-00000aab0f26&acdnat=1365465952_6c36038707f44762
faf61184346e7561
133
Baerwald, A. R., Walker, R. A., & Pierson, R. A. (2009). Growth rates of ovarian
follicles during natural menstrual cycles, oral contraception cycles, and ovarian
stimulation cycles. Fertility and sterility, 91(2), 440-449.
doi:10.1016/j.fertnstert.2007.11.054
Baird, D. T. (1992). Luteotrophic control of the corpus luteum. Animal Reproduction
Science, 28(1), 95-102. Retrieved from http://ac.els-cdn.com/03784320
9290096V/1-s2.0-037843209290096V-main.pdf?_tid=6458922c-9704-11
e2-8148-00000aab0f27&acdnat=1364405769_3bd437b5ea5cd9603
dbe286bd8ef8608
Brenner, R. M., Nayak, N. R., Slayden, O. D., Critchley, H. O., & Kelly, R. W. (2002).
Premenstrual and menstrual changes in the macaque and human
endometrium.Annals of the New York Academy of Sciences, 955(1), 60-74.
Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.1749-6632.2002.
tb02766.x/pdf
Buffenstein, R., Poppitt, S. D., McDevitt, R. M., & Prentice, A. M. (1995). Food intake
and the menstrual cycle: a retrospective analysis, with implications for appetite
research. Physiology & behavior, 58(6), 1067-1077. Retrieved from http://ac.
els-cdn.com/0031938495020039/1-s2.0-0031938495020039main.pdf?_tid=40721bba-addb-11e2-b39500000aacb35d&acdnat=1366916976_61a68af84d005edbf1a2e6495a8a492b
Bowen, D. J., & Grunberg, N. E. (1990). Variations in food preference and consumption
across the menstrual cycle. Physiology & behavior, 47(2), 287-291. Retrieved
134
from http://ac.els-cdn.com/003193849090144S/1-s2.0-003193849090144S-main.
pdf?_tid=fde3a7c2-b074-11e2-ac6b-00000aacb35d&acdnat=1367202909_e7
aa5c8a21d7f69eed235c1668ca1fa8
Carr, B., & Blackwell, R. (1993). Textbook of reproductive medicine. (1st ed., pp.
209-216). Norwalk, CT: Appleton & Lange.
Chehab, F. F., Mounzih, K., Lu, R., & Lim, M. E. (1997). Early onset of reproductive
function in normal female mice treated with leptin. Science, 275(5296), 88-90.
Retrieved from http://www.sciencemag.org/content/275/5296/88.full.pdf
Croxatto, H. B. (2008). Female reproductive physiology/function. International
Encyclopedia of Public Health, 603-613. Retrieved from
http://www.sciencedirect.com/science/article/pii/B9780123739605004755
Cohen, I. T., Sherwin, B. B., & Fleming, A. S. (1987). Food cravings, mood, and the
menstrual cycle. Hormones and Behavior, 21(4), 457-470. Retrieved from
http://www.sciencedirect.com/science/article/pii/0018506X87900043
Coelho, J. S., Polivy, J., & Herman, C. P. (2006). Selective carbohydrate or protein
restriction: Effects on subsequent food intake and cravings. Appetite, 47(3), 352360.
Chau, J. P., Chang, A. M., & Chang, A. M. (1998). Relationship between premenstrual
tension syndrome and anxiety in Chinese adolescents. Journal of Adolescent
Health, 22(3), 247-249. Retrieved from http://ac.elscdn.com/S1054139X97002061/1-s2.0-S1054139X97002061-main.pdf?_tid=
135
9727107c-a909-11e2-a10e-00000aab0f27&acdnat=1366387123_
01a483b453ae1a88b1d14256a470def4
Cooper, G. S., Sandler, D. P., Whelan, E. A., & Smith, K. R. (1996). Association of
physical and behavioral characteristics with menstrual cycle patterns in women
age 29-31 years. Epidemiology, 7(6), 624-628. Retrieved from
http://journals.lww.com/epidem/Abstract/1996/11000/Association_of_Physical_a
nd_Behavioral.11.aspx
Collins, A., Eneroth, P., & Landgren, B. M. (1985). Psychoneuroendocrine stress
responses and mood as related to the menstrual cycle. Psychosomatic
medicine,47(6), 512-527. Retrieved from
http://www.psychosomaticmedicine.org/content/47/6/512.full.pdf
Cohen, L. S., Soares, C. N., Vitonis, A. F., Otto, M. W., & Harlow, B. L. (2006). Risk for
new onset of depression during the menopausal transition: the Harvard study of
moods and cycles. Archives of general psychiatry, 63(4), 385. Retrieved from
http://archpsyc.jamanetwork.com/article.aspx?articleid=209471
Casanueva, F. F., Borras, C. G., Burguera, B., Muruais, C., Fernandez, M., & Devesa, J.
(1987). Steroids and neuroendocrine function in anorexia nervosa.Journal of
steroid biochemistry, 27(1), 635-640. Retrieved from http://ac.elscdn.com/0022473187903645/1-s2.0-0022473187903645main.pdf?_tid=fbe67a1e-a947-11e2-b4c300000aab0f01&acdnat=1366413920_3aa2769a5a6259bc2e6c008ef6a9605c
136
Caglar, G. S., Asimakopoulos, B., Nikolettos, N., Diedrich, K., & Al-Hasani, S. (2005).
Recombinant LH in ovarian stimulation. Reproductive biomedicine online,10(6),
774-785. Retrieved from http://ac.els-cdn.com/S1472648310611236/1-s2.0-S147
2648310611236-main.pdf?_tid=119ec44e-a257-11e2-ba18-00000aab0f6b
&acdnat=1365650741_cc083067e6a9ce33ea0fbc64c94a4fdf
Castillo-Martínez, L., López-Alvarenga, J. C., Villa, A. R., & González-Barranco, J.
(2003). Menstrual cycle length disorders in 18-to 40-y-old obese women.
Nutrition,19(4), 317-320. Retrieved from http://ac.els-cdn.com/S0899900
70200998X/1-s2.0-S089990070200998X-main.pdf?_tid=50eaf3f6-aab9-11
e2-a3f8-00000aab0f26&acdnat=1366572547_46f2fd393368d861c298d95
623f4c36a
Dhar, V., & Pearson Murphy, B. E. (1990). Double-blind randomized crossover trial of
luteal phase estrogens (Premarin®) in the premenstrual syndrome
(PMS). Psychoneuroendocrinology, 15(5), 489-493. Retrieved from
http://www.sciencedirect.com/science/article/pii/030645309090072H
Darrow, S. L., Vena, J. E., Batt, R. E., Zielezny, M. A., Michalek, A. M., & Selman, S.
(1993). Menstrual cycle characteristics and the risk of
endometriosis.Epidemiology, 4(2), 135-142. Retrieved from
http://www.jstor.org/stable/pdfplus/3702555.pdf?acceptTC=true
De Lignieres, B., Vincens, M., Mauvais-Jarvis, P., Mas, J. L., Touboul, P. J., & Bousser,
M. G. (1986). Prevention of menstrual migraine by percutaneous oestradiol.
British medical journal (Clinical research ed.), 293(6561), 1540. Retrieved from
137
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1342315/pdf/bmjcred0026
5-0024a.pdf
Devlin, M. J., Walsh, B. T., Katz, J. L., Roose, S. P., Linkie, D. M., Wright, L., ... &
Glassman, A. H. (1989). Hypothalamic-pituitary-gonadal function in anorexia
nervosa and bulimia. Psychiatry research, 28(1), 11-24. Retrieved from
http://ac.els-cdn.com/0165178189901935/1-s2.0-0165178189901935-main.
pdf?_tid=24a93f98-a9d1-11e2-b861-00000aab0f27&acdnat=1366472830_5
8213418fa3481152c108cb0a19e2b24
Dalvit-McPhillips, S. P. (1983). The effect of the human menstrual cycle on nutrient
intake. Physiology & behavior, 31(2), 209-212. Retrieved from http://ac.els-cdn.
com/0031938483901208/1-s2.0-0031938483901208-main.pdf?_tid=6b43aad
4-addb-11e2-b395-00000aacb35d&acdnat=1366917048_3b0eb38e36ea
5c6094eff6c13a5a41bd
Dye, L., Warner, P., & Bancroft, J. (1995). Food craving during the menstrual cycle and
its relationship to stress, happiness of relationship and depression; a preliminary
enquiry. Journal of affective disorders, 34(3), 157-164. Retrieved from
http://ac.els-cdn.com/016503279500013D/1-s2.0-016503279500013D-main.
pdf?_tid=6d1c5b5c-b075-11e2-a99b-00000aacb361&acdnat=1367203096_
6b4f52e484ad23b5280566f1661e3d5b
Devoto, L., Fuentes, A., Kohen, P., Céspedes, P., Palomino, A., Pommer, R., ... & Strauss
III, J. F. (2009). The human corpus luteum: life cycle and function in natural
cycles. Fertility and sterility, 92(3), 1067-1079. Retrieved from http://ac.
138
els-cdn.com/S0015028208032585/1-s2.0-S0015028208032585-main.
pdf?_tid=a69ae6e8-9584-11e2-896c-00000aab0f6b&acdnat=
1364240953_d333c7583834dbc0e3cf55918a345be4
Devoto, L., Kohen, P., Muñoz, A., & Strauss III, J. F. (2009). Human corpus luteum
physiology and the luteal-phase dysfunction associated with ovarian
stimulation.Reproductive biomedicine online, 18, S19-S24. Retrieved from
http://ac.els-cdn.com/S1472648310604440/1-s2.0-S1472648310604440-main.
pdf?_tid=df496d64-9581-11e2-b83e-00000aacb360&acdnat=
1364239760_fc0979cdb93e7128b786a3c62c773ce2
Davies, J., & Kadir, R. A. (2012). Endometrial haemostasis and menstruation.Reviews in
Endocrine and Metabolic Disorders, 13(4), 289-299. Retrieved from
http://link.springer.com/content/pdf/10.1007%2Fs11154-012-9226-4
Dye, L., & Blundell, J. E. (1997). Menstrual cycle and appetite control: implications for
weight regulation. Human reproduction, 12(6), 1142-1151. Retrieved from
http://humrep.oxfordjournals.org/content/12/6/1142.full.pdf
Freedman, D. S., Khan, L. K., Serdula, M. K., Dietz, W. H., Srinivasan, S. R., &
Berenson, G. S. (2002). Relation of age at menarche to race, time period, and
anthropometric dimensions: the Bogalusa Heart Study. Pediatrics, 110(4),
e43-e43. Retrieved from http://pediatrics.aappublications.org/content/
110/4/e43.full.pdf+html
139
Findlay, J. K. (1994). Peripheral and local regulators of folliculogenesis.Reproduction,
fertility and development, 6(2), 127-139. Retrieved from
http://www.publish.csiro.au/?act=view_file&file_id=RD9940127.pdf
Filicori, M., Butler, J. P., & Crowley Jr, W. F. (1984). Neuroendocrine regulation of the
corpus luteum in the human. Evidence for pulsatile progesterone secretion.Journal
of Clinical Investigation, 73(6), 1638. Retrieved from http://www.ncbi.nlm.nih.
gov/pmc/articles/PMC437074/pdf/jcinvest00156-0144.pdf
Frye, C. A., & Demolar, G. L. (1994). Menstrual cycle and sex differences influence salt
preference. Physiology & behavior, 55(1), 193-197. Retrieved from http://ac.
els-cdn.com/0031938494900310/1-s2.0-0031938494900310-main.pdf?
_tid=8a80d6d2-b075-11e2-a118-00000aab0f6c&acdnat=1367203147_33ab1
584e49b63807b3cb2e1cf0c9142
Flowers JR, C. E., & Wilborn, W. H. (1978). New observations on the physiology of
menstruation. Obstetrics & Gynecology, 51(1), 16-24. Retrieved from
http://journals.www.com/greenjournal/Abstract/1978/01000/New_Observations_o
n_the_Physiology_of_Menstruation.3.aspx
Fan, Q. R., & Hendrickson, W. A. (2005). Structure of human follicle-stimulating
hormone in complex with its receptor. Nature, 433(7023), 269-277. Retrieved
from http://www.nature.com/nature/journal/v433/n7023/pdf/nature03206.pdf
Franks, S. (1995). Polycystic ovary syndrome. New England Journal of
Medicine,333(13), 853-861. Retrieved from
http://www.nejm.org/doi/pdf/10.1056/NEJM199509283331307
140
Fedoroff, I., Polivy, J., & Peter Herman, C. (2003). The specificity of restrained versus
unrestrained eaters' responses to food cues: general desire to eat, or craving for
the cued food?. Appetite, 41(1), 7-13.
Fichter, M. M., Pirke, K. M., Pöllinger, J., Wolfram, G., & Brunner, E. (1990).
Disturbances in the hypothalamo-pituitary-adrenal and other neuroendocrine axes
in bulimia. Biological psychiatry, 27(9), 1021-1037. Retrieved from http://ac.
els-cdn.com/0006322390900384/1-s2.0-0006322390900384-main.pdf?_tid=
3d4588d8-a9d9-11e2-829c00000aacb361&acdnat=1366476307_4efa202bba69c6440288d4695b08811b
Fenster, L., Waller, K., Chen, J., Hubbard, A. E., Windham, G. C., Elkin, E., & Swan, S.
(1999). Psychological stress in the workplace and menstrual function. American
Journal of Epidemiology, 149(2), 127-134. Retrieved from
http://aje.oxfordjournals.org/content/149/2/127.full.pdf
Fenster, L., Quale, C., Waller, K., Windham, G. C., Elkin, E. P., Benowitz, N., & Swan,
S. H. (1999). Caffeine consumption and menstrual function. American journal of
epidemiology, 149(6), 550-557. Retrieved from
http://aje.oxfordjournals.org/content/149/6/550.full.pdf
Garner et al. (1982). The Eating Attitudes Test: Psychometric features and clinical
correlates. Psychological Medicine, 12, 871-878
Gendall, K. A., Joyce, P. R., Sullivan, P. F., & Bulik, C. M. (1998). Food cravers:
Characteristics of those who binge. International Journal of Eating Disorders,
23(4), 353-360. Retrieved from
141
http://onlinelibrary.wiley.com/doi/10.1002/(SICI)1098-108X(199805)23:
4%3C353::AID-EAT2%3E3.0.CO;2-H/pdf
Gong, E. J., Garrel, D., & Calloway, D. H. (1989). Menstrual cycle and voluntary food
intake. The American journal of clinical nutrition, 49(2), 252-258. Retrieved from
http://ajcn.nutrition.org/content/49/2/252.full.pdf
Gendall, K. A., Sullivan, P. F., Joyce, P. R., & Bulik, C. M. (1997). Food cravings in
women with a history of anorexia nervosa. International Journal of Eating
Disorders,22(4), 403-409. Retrieved from
Gellersen, B., Fernandes, M. S., & Brosens, J. J. (2009). Non-genomic progesterone
actions in female reproduction. Human reproduction update, 15(1), 119-138.
Retrieved from http://humupd.oxfordjournals.org/content/15/1/119.full.pdf
Georgopoulos, N., Markou, K., Theodoropoulou, A., Paraskevopoulou, P., Varaki, L.,
Kazantzi, Z., ... & Vagenakis, A. G. (1999). Growth and pubertal development in
elite female rhythmic gymnasts. Journal of Clinical Endocrinology &
Metabolism,84(12), 4525-4530. Retrieved from http://jcem.endojournals.
org/content/84/12/4525.full.pdf+html
Gougeon, A., & Lefèvre, B. (1983). Evolution of the diameters of the largest healthy and
atretic follicles during the human menstrual cycle. Journal of reproduction and
fertility, 69(2), 497-502. Retrieved from http://www. reproductiononline.org/content/69/2/497.full.pdf+html
Goodman, H. M. (2003). Basic medical endocrinology. (3rd ed., pp. 393-417).
Worcester, MA: Academic Press.
142
Gregory, S. J., & Kaiser, U. B. (2004). Regulation of gonadotropins by inhibin and
activin. In Seminars in reproductive medicine (Vol. 22, No. 03, pp. 253-267).
Copyright© 2004 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New
York, NY 10001, USA. Retrieved from https://www.thieme-connect.com/
ejournals/pdf/10.1055/s-2004-831901.pdf
Ha, E. J., & Caine-Bish, N. (2009). Effect of nutrition intervention using a general
nutrition course for promoting fruit and vegetable consumption among college
students. Journal of Nutrition Education and Behavior, 41(2), 103-109.
Herrera, E., Gómez-Amor, J., Martínez-Selva, J., & Ato, M. (1990). Relationship
between personality, psychological and somatic symptoms, and the menstrual
cycle. Personality and individual differences, 11(5), 457-461. Retrieved from
http://ac.els-cdn.com/019188699090058Y/1-s2.0-019188699090058Ymain.pdf?_tid=538a9780-a832-11e2-8c91-00000aab0f26
&acdnat=1366294667_dd459177917bef44027dc4c69f615f3e
Harlow, B. L., Wise, L. A., Otto, M. W., Soares, C. N., & Cohen, L. S. (2003).
Depression and its influence on reproductive endocrine and menstrual cycle
markers associated with perimenopause: the Harvard Study of Moods and
Cycles.Archives of general psychiatry, 60(1), 29. Retrieved from
http://archpsyc.jamanetwork.com/article.aspx?articleid=207048
Hart, R., Hickey, M., & Franks, S. (2004). Definitions, prevalence and symptoms of
polycystic ovaries and polycystic ovary syndrome. Best practice & research.
Clinical obstetrics & gynaecology, 18(5), 671. Retrieved from http://ac.els-cdn.
143
com/S1521693404000914/1-s2.0-S1521693404000914-main.pdf?_tid=c0023
a6a-aa19-11e2-b030-00000aab0f02&acdnat=1366504014_1
fa02f14da1e80499dd6596d03fcafb0
Hormes, J. M., & Timko, C. A. (2011). All cravings are not created equal. Correlates of
menstrual versus non-cyclic chocolate craving. Appetite, 57(1), 1-5. Retrieved
from http://ac.els-cdn.com/S0195666311001127/1-s2.0-S019566631100112
7-main.pdf?_tid=5c4804c0-b075-11e2-a99b-00000aacb361&acdnat=
1367203068_3b1e9ab3dd8d77cb76f680953187d718
Howe, J. C., Rumpler, W. V., & Seale, J. L. (1993). Energy expenditure by indirect
calorimetry in premenopausal women: variation within one menstrual cycle. The
Journal of Nutritional Biochemistry, 4(5), 268-273. Retrieved from http://ac.
els-cdn.com/095528639390096F/1-s2.0-095528639390096F-main.pdf?_tid=
b2bb21e4-addb-11e2-bcd5-00000aab0f6b&acdnat=1366917168_
a5fac0bbc0f7acace4f892502b20f13b
Henriet, P., Gaide Chevronnay, H. P., & Marbaix, E. (2012). The endocrine and paracrine
control of menstruation. Molecular and Cellular Endocrinology, 358(2), 197-207.
Hill, A. J., & Heaton-Brown, L. (1994). The experience of food craving: A prospective
investigation in healthy women. Journal of Psychosomatic Research, 38(8),
801-814. Retrieved from http://ac.els-cdn.com/002239999490068X/1-s2.
0-002239999490068X-main.pdf?_tid=fd5902b2-b073-11e2-8714-00000
aacb35e&acdnat=1367202479_cfe55cdc0ba46d5b63076225cc67f410
144
Hormes, J. M., & Timko, C. A. (2011). All cravings are not created equal. Correlates of
menstrual versus non-cyclic chocolate craving. Appetite, 57(1), 1-5. Retrieved
from http://ac.els-cdn.com/S0195666311001127/1-s2.0-S0195666311001127main.pdf?_tid=b5ed7324-b058-11e2-ab01-00000aacb35e&acdnat=
1367190763_2fb9eba94a3b0aee42555ebe30040b81
Hillier, S. G., & Tetsuka, M. (1997). 3 Role of androgens in follicle maturation and
atresia. Baillière's clinical obstetrics and gynaecology, 11(2), 249-260. Retrieved
from http://ac.els-cdn.com/S0950355297800363/1-s2.0-S0950355297800
363-main.pdf?_tid=ae9a0b5a-9f91-11e2-899d-00000aab0f27&acdnat=
1365346062_f1231d36aabb3f0af7a8304bfdbbeca4
Hillier, S. G. (2001). Gonadotropic control of ovarian follicular growth and development.
Molecular and cellular endocrinology, 179(1), 39-46. Retrieved from
http://www.sciencedirect.com/science/article/pii/S0303720701004695
Hazzard, T. M., & Stouffer, R. L. (2000). Angiogenesis in ovarian follicular and luteal
development. Best Practice & Research Clinical Obstetrics & Gynaecology,
14(6), 883-900. Retrieved from http://www.sciencedirect.com
/science/article/pii/S1521693400901330
Hill, A. J., Weaver, C. F., & Blundell, J. E. (1991). Food craving, dietary restraint and
mood. Appetite, 17(3), 187-197. Retrieved from
Hickey, M., & Fraser, I. S. (2000). The structure of endometrial microvessels. Human
Reproduction, 15(suppl 3), 57-66. Retrieved from http://humrep.oxfordjournals.
org/content/15/suppl_3/57.full.pdf
145
Holroyd, E., Katie, F. K. L., Chun, L. S., & Ha, S. W. (1997). “Doing the month”: An
exploration of postpartum practices in Chinese women. Health Care for Women
International, 18(3), 301-313.
Ingamells, S., Campbell, I. G., Anthony, F. W., & Thomas, E. J. (1996). Endometrial
progesterone receptor expression during the human menstrual cycle. Journal of
reproduction and fertility, 106(1), 33-38. Retrieved from
http://www.reproduction-online.org/content/106/1/33.full.pdf
Jakubowska, J., Maciejewska, A., Bielawski, K. P., & Pawłowski, R. (2014). mRNA
heptaplex protocol for distinguishing between menstrual and peripheral blood.
Forensic Science International: Genetics, 13, 53-60.
Jones, R. (1991). Human reproductive biology. (1st ed., pp. 143-156). San Diego,CA:
Academic Press, Inc.
Johnson, W. G., Corrigan, S. A., Lemmon, C. R., Bergeron, K. B., & Crusco, A. H.
(1994). Energy regulation over the menstrual cycle. Physiology & behavior,
56(3), 523-527. Retrieved from http://ac.els-cdn.com/0031938494902968/1-s2.
0-0031938494902968-main.pdf?_tid=acfddd78-addb-11e2-bcd5-00000aab
0f6b&acdnat=1366917158_b36b1c6ac2c68edb55fb8ff3a71b3fb8
Karapanou, O., & Papadimitriou, A. (2010). Determinants of menarche. Reprod Biol
Endocrinol, 8, 115. Retrieved from
http://www.biomedcentral.com/content/pdf/1477-7827-8-115.pdf
146
Kelly, R. W., King, A. E., & Critchley, H. O. (2001). Cytokine control in human
endometrium. Reproduction, 121(1), 3-19. http://www.reproductiononline.org/content/121/1/3.full.pdf+html
Kozlowski, L. T., Pillitteri, J. L., Sweeney, C. T., Whitfield, K. E., & Graham, J. W.
(1996). Asking questions about urges or cravings for cigarettes. Psychology of
Addictive Behaviors, 10(4), 248. Retrieved from http://psycnet.apa.org/
journals/adb/10/4/248.pdf
Kozlowski, L. T., & Wilkinson, D. A. (1987). Use and misuse of the concept of craving
by alcohol, tobacco, and drug researchers. British journal of addiction,82(1),
31-36. Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.
1360-0443.1987.tb01430.x/pdf
Kuohung, W., Borgatta, L., & Stubblefield, P. (2000). Low-dose oral contraceptives and
bone mineral density: an evidence-based analysis. Contraception, 61(2), 77-82.
Leibowitz, S. F., Weiss, G. F., Walsh, U. A., & Viswanath, D. (1989). Medial
hypothalamic serotonin: role in circadian patterns of feeding and macronutrient
selection. Brain research, 503(1), 132-140. Retrieved from http://ac.
els-cdn.com/0006899389917137/1-s2.0-0006899389917137-main.pdf?_
tid=7f04f9ca-b811-11e2-a723-00000aab0f02&acdnat=1368039786_
439140220f77305e304bdfbbe9fc1c0b
Leibowitz, S. F., Weiss, G. F., & Suh, J. S. (1990). Medial hypothalamic nuclei mediate
serotonin's inhibitory effect on feeding behavior. Pharmacology Biochemistry and
Behavior, 37(4), 735-742. Retrieved from http://ac.els-cdn.com/00913057
147
9090556W/1-s2.0-009130579090556W-main.pdf?_tid=968c83ce-b811-11e
2-beda-00000aab0f6b&acdnat=1368039825_3df11a3f22d018a4182a6bf
725ef9c59
Lassek, W. D., & Gaulin, S. J. (2007). Brief communication: menarche is related to fat
distribution. Am J Phys Anthropol, 133, 1147-1151. Retrieved from
http://onlinelibrary.wiley.com/doi/10.1002/ajpa.20644/pdf
Levy, A., & Lightman, S. (1997). Endocrinology. (1st ed., pp. 106-108, 120-137). New
York,NY: Oxford university press.
Levi-Setti, P. E., Cavagna, M., Baggiani, A., Zannoni, E., Colombo, G. V., & Liprandi,
V. (2004). FSH and LH together in ovarian stimulation. European journal of
obstetrics, gynecology, and reproductive biology, 115, S34. Retrieved from
http://ac.els-cdn.com/S0301211504000168/1-s2.0-S0301211504000168-main.
pdf?_tid=ae859d7c-a258-11e2-9308-00000aab0f6b&acdnat=1365651434_
a13d6b0055e2eef90a41cba04aea1a87
Liu, Y., Gold, E. B., Lasley, B. L., & Johnson, W. O. (2004). Factors affecting menstrual
cycle characteristics. American journal of epidemiology, 160(2), 131-140.
Retrieved from http://aje.oxfordjournals.org/content/160/2/131.full.pdf
Lioyd, T., Lin, H. M., Matthews, A. E., Bentley, C. M., & Legro, R. S. (2002). Oral
contraceptive use by teenage women does not affect body composition. Obstetrics
& Gynecology, 100(2), 235-239.
148
Leon, G. R., Phelan, P. W., Kelly, J. T., & Patten, S. R. (1986). The symptoms of bulimia
and the menstrual cycle. Psychosomatic medicine, 48(6), 415-422. Retrieved from
http://www.psychosomaticmedicine.org/content/48/6/415.full.pdf
Lyons, P. M., Truswell, A. S., Mira, M., Vizzard, J., & Abraham, S. F. (1989). Reduction
of food intake in the ovulatory phase of the menstrual cycle. The American
journal of clinical nutrition, 49(6), 1164-1168. Retrieved from
http://ajcn.nutrition.org/content/49/6/1164.full.pdf
Lissner, L., Stevens, J., Levitsky, D. A., Rasmussen, K. M., & Strupp, B. J. (1988).
Variation in energy intake during the menstrual cycle: implications for
food-intake research. The American journal of clinical nutrition, 48(4), 956-962.
Retrieved from http://ajcn.nutrition.org/content/48/4/956.full.pdf
Livingstone, M., & Fraser, I. S. (2002). Mechanisms of abnormal uterine
bleeding.Human reproduction update, 8(1), 60-67. doi: 10.1093/humupd/8.1.6
Mansour, A. A., & Hassan, S. A. (1994). Factors that influence women's nutrition
knowledge in Saudi Arabia. Health care for women international, 15(3), 213-223.
DOI: 10.1080/07399339409516113
Massey, A., & Hill, A. J. (2012). Dieting and food craving. A descriptive, quasiprospective study. Appetite, 58(3), 781-785. Retrieved from
http://www.sciencedirect.com/science/article/pii/S0195666312000219
Matkovic, V., Ilich, J. Z., Skugor, M., Badenhop, N. E., Goel, P., Clairmont, A., ... &
Landoll, J. D. (1997). Leptin is inversely related to age at menarche in human
females. Journal of Clinical Endocrinology & Metabolism, 82(10), 3239-3245.
149
Retrieved from
http://journals.lww.com/obgynsurvey/Citation/1998/03000/Leptin_Is_Inversely_
Related_to_Age_at_Menarche_in.18.aspx
Messinis, I. E., Messini, C. I., & Dafopoulos, K. (2010). The role of gonadotropins in the
follicular phase. Annals of the New York Academy of Sciences, 1205(1), 5-11.
Retrieved from http://onlinelibrary.wiley.com /doi/10.1111/j.17496632.2010.05660.x/pdf
McGee, E., Spears, N., Minami, S., Hsu, S. Y., Chun, S. Y., Billig, H., & Hsueh, A. J.
(1997). Preantral ovarian follicles in serum-free culture: suppression of apoptosis
after activation of the cyclic guanosine 3′, 5′-monophosphate pathway and
stimulation of growth and differentiation by follicle-stimulating hormone.
Endocrinology, 138(6), 2417-2424. Retrieved from http://endo.endojournals.
org/content/138/6/2417.full.pdf+html
McVay, M. A., Copeland, A. L., Newman, H. S., & Geiselman, P. J. (2012). Food
cravings and food cue responding across the menstrual cycle in a non-eating
disordered sample. Appetite.Retrieved from
http://www.sciencedirect.com/science/article/pii/S0195666312002358
Millier, S. G., Whitelaw, P. F., & Smyth, C. D. (1994). Follicular oestrogen synthesis: the
‘two-cell, two-gonadotrophin’model revisited. Molecular and cellular
endocrinology, 100(1), 51-54. Retrieved from
http://www.sciencedirect.com/science/article/pii/030372079490278X
/jcem.endojournals.org/content/82/10/3239.full.pdf+html
150
Mayorga, M. P., Gromoll, J., Behre, H. M., Gassner, C., Nieschlag, E., & Simoni, M.
(2000). Ovarian response to follicle-stimulating hormone (FSH) stimulation
depends on the FSH receptor genotype. Journal of Clinical Endocrinology &
Metabolism,85(9), 3365-3369. Retrieved from
http://jcem.endojournals.org/content/85/9/3365.full.pdf
Modell, J. G., Glaser, F. B., Cyr, L., & Mountz, J. M. (1992). Obsessive and compulsive
characteristics of craving for alcohol in alcohol abuse and
dependence.Alcoholism: Clinical and Experimental Research, 16(2), 272-274.
Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.15300277.1992.tb01375.x/pdf
Martini, M. C., Lampe, J. W., Slavin, J. L., & Kurzer, M. S. (1994). Effect of the
menstrual cycle on energy and nutrient intake. The American journal of clinical
nutrition, 60(6), 895-899. Retrieved from http://ajcn.nutrition.org/
content/60/6/895.full.pdf
Milewicz, A., & Jedrzejuk, D. (2006). Premenstrual syndrome: from etiology to
treatment. Maturitas, 55, S47-S54. Retrieved from http://ac.elscdn.com/S0378512206002386/1-s2.0-S0378512206002386-main.pdf?_tid=
d5c59294-aa09-11e2-a44b-00000aab0f26&acdnat=1366497179
_ceabb6d48cee37f402da681cbac97d60
Mitan, L. A. P. (2004). Menstrual dysfunction in anorexia nervosa. Journal of pediatric
and adolescent gynecology, 17(2), 81-85. Retrieved from http://ac.els-cdn.com
/S108331880400004X/1-s2.0-S108331880400004X-main.pdf?_tid=02b8e
151
026-a947-11e2-831a-00000aab0f6b&acdnat=1366413502
_32971ba9324eb7ca2ab55e5eb2bab9ab
Mendelson, J. H., & Mello, N. K. (1988). Chronic alcohol effects on anterior pituitary
and ovarian hormones in healthy women. Journal of Pharmacology and
Experimental Therapeutics, 245(2), 407-412. Retrieved from
http://jpet.aspetjournals.org/content/245/2/407.full.pdf
Monk, T. H. (1989). A visual analogue scale technique to measure global vigor and
affect. Psychiatry Research, 27(1), 89-99.
Møller, U. K., við Streym, S., Mosekilde, L., & Rejnmark, L. (2012). Changes in bone
mineral density and body composition during pregnancy and postpartum. A
controlled cohort study. Osteoporosis International, 23(4), 1213-1223.
Murphy, R., Straebler, S., Cooper, Z., & Fairburn, C. G. (2010). Cognitive behavioral
therapy for eating disorders. The Psychiatric Clinics of North America, 33(3),
611.
Muallem, M. M., & Rubeiz, N. G. (2006). Physiological and biological skin changes in
pregnancy. Clinics in dermatology, 24(2), 80-83.
National Academy Press: Dietary Reference Intakes for Energy, Carbohydrates, Fiber,
Fat, Protein, and Amino Acids (Macronutrients), 2002.
Norman, R. J., Hickey, T., Moran, L., Boyle, J., Wang, J., & Davies, M. (2004, April).
Polycystic ovary syndrome—diagnosis and etiology. In International Congress
Series (Vol. 1266, pp. 225-232). Elsevier. Retrieved from http://ac.els-cdn.
com/S0531513104001104/1-s2.0-S0531513104001104-main. pdf?_tid=fc9a
152
7456-aa32-11e2-8765-00000aab0f26&acdna t=1366514853_c1b664623f770
c84a5b1906601fe1aaf
Niswender, G. D., Juengel, J. L., Silva, P. J., Rollyson, M. K., & McIntush, E. W. (2000).
Mechanisms controlling the function and life span of the corpus
luteum.Physiological reviews, 80(1), 1-29. Retrieved from
http://physrev.physiology.org/content/80/1/1.full.pdf+html
Oonk, R., Krasnow, J., Beattie, W., & Richards, J. (1989). Cyclic amp-dependent
and -independent regulation of cholesterol side chain cleavage cytochrome-p-450
(p-45os,,) in rat ovarian granulosa cells and corpora lute. THE JOURNAL OF
BIOLOGICAL CHEMISTRY, 264(36), 21934-21942. Retrieved from
http://www.jbc.org/content/264/36/21934.full.pdf
Otten, et al. Dietary Reference Intakes, National Academy of Sciences, 2006, p. 82.
O'Toole, M. L., Sawicki, M. A., & Artal, R. (2003). Structured diet and physical activity
prevent postpartum weight retention. Journal of Women's Health, 12(10), 991998.
Owen, J. A. (1975). Physiology of the menstrual cycle. The American journal of clinical
nutrition, 28(4), 333-338. Retrieved from http://ajcn.nutrition.org/content/
28/4/333.full.pdf
Silberstein, S. D., & Merriam, G. R. (2000). Physiology of the menstrual
cycle.Cephalalgia, 20(3), 148-154. DOI: 10.1046/j.1468-2982.2000.00034.
153
Palermo, R. (2007). Differential actions of FSH and LH during
folliculogenesis.Reproductive biomedicine online, 15(3), 326-337. Retrieved from
http://www.sciencedirect.com/science/article/pii/S1472648310603471
Pelchat, M. L. (1997). Food cravings in young and elderly adults. Appetite, 28(2), 103113. Retrieved from http://ac.els-cdn.com/S019566639690063X/1-s2
0-S019566639690063X-main.pdf?_tid=f78fee4e-b44d-11e2-9c54-00000
aab0f02&acdnat=1367625953_3020d5d136d173c8bda367413fa08b86
Polivy, J., Coleman, J., & Herman, C. P. (2005). The effect of deprivation on food
cravings and eating behavior in restrained and unrestrained eaters. International
Journal of Eating Disorders, 38(4), 301-309.
Polivy, J. (1996). Psychological consequences of food restriction. Journal of the
American Dietetic Association, 96(6), 589-592.
Pasquali, R., Patton, L., & Gambineri, A. (2007). Obesity and infertility. Current Opinion
in Endocrinology, Diabetes and Obesity, 14(6), 482-487. Retrieved from
http://ac.els-cdn.com/S1471769703000613/1-s2.0-S1471769703000613main.pdf?_tid=a0019148-aab9-11e2-843a-00000aab0f01&acdnat=
1366572680_8a4c1586c2f1f8ec3d1a7db691f6eb7f
Pinkerton, J. V., Guico-Pabia, C. J., & Taylor, H. S. (2010). Menstrual cycle-related
exacerbation of disease. American journal of obstetrics and gynecology, 202(3),
221-231. Retrieved from http://ac.els-cdn.com/S0002937809008540/1-s2.
0-S0002937809008540-main.pdf?_tid=adec5ca8-a9c3-11e2-933b-00000
aacb361&acdnat=1366467047_5505d1398577f7bee7bacd4a8e86ebd4
154
Pasquali, R. (2006). Obesity, fat distribution and infertility. Maturitas, 54(4), 363-371.
Retrieved from http://ac.els-cdn.com/S0378512206001423/1-s2.0-S037851
2206001423-main.pdf?_tid=c7de0ad4-aab9-11e2-85f2-00000
aacb360&acdnat=1366572747_b4a0028da05eee09896c77461556d85b
Pasquali, R., Pelusi, C., Genghini, S., Cacciari, M., & Gambineri, A. (2003). Obesity and
reproductive disorders in women. Human reproduction update, 9(4), 359-372.
Retrieved from http://humupd.oxfordjournals.org/content/9/4/359.full.pdf
Piers, L. S., Diggavi, S. N., Rijskamp, J., Van Raaij, J. M., Shetty, P. S., & Hautvast, J.
G. (1995). Resting metabolic rate and thermic effect of a meal in the follicular and
luteal phases of the menstrual cycle in well-nourished Indian women. The
American journal of clinical nutrition, 61(2), 296-302. Retrieved from
http://ajcn.nutrition.org/content/61/2/296.full.pdf
Pelchat, M. L. (2002). Of human bondage: food craving, obsession, compulsion, and
addiction. Physiology & Behavior, 76(3), 347-352. Retrieved from http://ac.
els-cdn.com/S0031938402007576/1-s2.0-S0031938402007576main.pdf?_tid=c473bd38-b452-11e2-b2e0-00000aab0f27&acdnat=
1367628017_e2846d628af10e16d712360060b0dae5
Reynolds, L. P., Grazul-Bilska, A. T., & Redmer, D. A. (2000). Angiogenesis in the
corpus luteum. Endocrine, 12(1), 1-9. Retrieved from
http://link.springer.com/content/pdf/10.1385%2FENDO%3A12%3A1%3A1
155
Rabinovitz, S. (2005). Stress and Food Craving. In Nutrients, Stress, and Medical
Disorders (pp. 155-164). Humana Press. Retrieved from
http://link.springer.com/content/pdf/10.1385%2F1-59259-952-4%3A155.pdf
Rasgon, N. L., Altshuler, L. L., Fairbanks, L., Elman, S., Bitran, J., Labarca, R., ... &
Mintz, J. (2005). Reproductive function and risk for PCOS in women treated for
bipolar disorder. Bipolar disorders, 7(3), 246-259. Retrieved from
http://onlinelibrary.wiley.com/doi/10.1111/j.1399-5618.2005.00201.x/pdf
Rapkin, A. (2003). A review of treatment of premenstrual syndrome & premenstrual
dysphoric disorder. Psychoneuroendocrinology, 28(Suppl 3), 39-53. Retrieved
from http://ac.els-cdn.com/S0306453003000969/1-s2.0-S0306453003000
969-main.pdf?_tid=e54b7698-a9f0-11e2-a306-00000aacb360&acdnat=
1366486468_0e6c4d3b3a71e619c05421a046166326
Rose, E. A., Porcerelli, J. H., & Neale, A. V. (2000). Pica: Common but commonly
missed . J Am Board Fam Pract, 13, 353-8. Retrieved from http://www.jabfm.org/
content/13/5/353.full.pdf
Rogers, P. J., & Smit, H. J. (2000). Food craving and food “addiction”: a critical review
of the evidence from a biopsychosocial perspective. Pharmacology Biochemistry
and Behavior, 66(1), 3-14. Retrieved from http://ac.els-cdn.com/S009130570
0001970/1-s2.0-S0091305700001970-main.pdf?_tid=f18efed4-b44a-11e2-b2
e0-00000aab0f27&acdnat=1367624654_6667e1dbcadc2bcbff66ef82c9c7f6c2
Regan, L., Owen, E. J., & Jacobs, H. S. (1990). Hypersecretion of luteinising hormone,
infertility, and miscarriage. The Lancet, 336(8724), 1141-1144. Retrieved from
156
http://ac.els-cdn.com/014067369092765A/1-s2.0-014067369092765Amain.pdf?_tid=27dcb9ba-a2ce-11e2-b558-00000aab0f27&acdnat=
1365701889_1a4665eba930c93a6f0ea05199ef120c
Rowland, A. S., Baird, D. D., Long, S., Wegienka, G., Harlow, S. D., Alavanja, M., &
Sandler, D. P. (2002). Influence of medical conditions and lifestyle factors on the
menstrual cycle. Epidemiology, 13(6), 668. Retrieved from
http://journals.lww.com/epidem/Abstract/2002/11000/Influence_of_Medical_Con
ditions_and_Lifestyle.11.aspx
Rogers, P. A. (1996). Structure and function of endometrial blood vessels. Human
reproduction update, 2(1), 57-62. Retrieved from
http://humupd.oxfordjournals.org/content/2/1/57.full.pdf
Rogol, A. D., Clark, P. A., & Roemmich, J. N. (2000). Growth and pubertal development
in children and adolescents: effects of diet and physical activity. The American
journal of clinical nutrition, 72(2), 521s-528s. Retrieved from
http://ajcn.nutrition.org/content/72/2/521s.full.pdf+html
Rudy, Ellen B., and Patricia, E. Professional and lay interrater reliability of urinary
luteinizing hormone surges measured by OvuQuick test. Journal of Obstetric,
Gynecologic, & Neonatal Nursing 21.5 (1992): 407-411.
Stocco, C., Telleria, C., & Gibori, G. (2007). The molecular control of corpus luteum
formation, function, and regression. Endocrine reviews, 28(1), 117-149. Retrieved
from http://edrv.endojournals.org/content/28/1/117.full.pdf+html
157
Strassmann, B. I. (1996). The evolution of endometrial cycles and menstruation.Quarterly
Review of Biology, 181-220. Retrieved from http://www.jstor.org/
stable/pdfplus/3035646.pdf?acceptTC=true
Salamonsen, L. A., & Lathbury, L. J. (2000). Endometrial leukocytes and menstruation.
Human reproduction update, 6(1), 16-27. Retrieved from
http://humupd.oxfordjournals.org/content/6/1/16.full.pdf
Shoham, Z. (2002). The clinical therapeutic window for luteinizing hormone in
controlled ovarian stimulation. Fertility and sterility, 77(6), 1170. Retrieved from
http://ac.els-cdn.com/S0015028202031576/1-s2.0-S0015028202031576-main.
pdf?_tid=9fd61e18-9c9b-11e2-9991-00000aab0f6c&acdnat=1365020479_
6b01b850eaaea290a1fdb0ad00f868c0
Simpson, E. R., & Waterman, M. R. (1988). Regulation of the synthesis of steroidogenic
enzymes in adrenal cortical cells by ACTH. Annual review of physiology, 50(1),
427-440. Retrieved from http://www.annualreviews.org/doi/pdf/
10.1146/annurev.ph.50.030188.002235
Spitzer, W. O., Lewis, M. A., Heinemann, L. A., & Thorogood, M. (1996). Third
generation oral contraceptives and risk of venous thromboembolic disorders: an
international case-control study. Bmj, 312(7023), 83-88.
Sullivan, M. W., Stewart-Akers, A., Krasnow, J. S., Berga, S. L., & Zeleznik, A. J.
(1999). Ovarian responses in women to recombinant follicle-stimulating hormone
and luteinizing hormone (LH): a role for LH in the final stages of follicular
maturation.Journal of Clinical Endocrinology & Metabolism, 84(1), 228-232.
158
Salamonsen, L. A. (1998). Current concepts of the mechanisms of menstruation: a normal
process of tissue destruction. Trends in Endocrinology & Metabolism, 9(8),
305-309. Retrieved from http://ac.els-cdn.com/S1043276098000782/1-s2.
0-S1043276098000782-main.pdf?_tid=0468f4c6-cce5-11e2-89b3-00000
aab0f6b&acdnat=1370329656_c74582be512772d83316c473e4332412
Salamonsen, L. A., Kovacs, G. T., & Findlay, J. K. (1999). Current concepts of the
mechanisms of menstruation. Best Practice & Research Clinical Obstetrics &
Gynaecology, 13(2), 161-179. Retrieved from http://ac.els-cdn.com/S15216934
99900159/1-s2.0-S1521693499900159-main.pdf?_tid=33e7eea0-cce5-11e2-a
374-00000aab0f6c&acdnat=1370329736_5f09768d3e4a9443499ae567184ac3c7
Stark, O., Peckham, C. S., & Moynihan, C. (1989). Weight and age at menarche.Archives
of Disease in Childhood, 64(3), 383-387. Retrieved from http://adc.bmj.com/
content/64/3/383.full.pdf+html
SMITH, S. L., & Sauder, C. (1969). Food cravings, depression, and premenstrual
problems. Psychosomatic medicine, 31(4), 281-287. Retrieved from
http://www.psychosomaticmedicine.org/content/31/4/281.full.pdf
Solomon, S. J., Kurzer, M. S., & Calloway, D. H. (1982). Menstrual cycle and basal
metabolic rate in women. The American journal of clinical nutrition, 36(4),
611-616. Retrieved from http://ajcn.nutrition.org/content/36/4/611.full.pdf
Seli, E., Berkkanoglu, M., & Arici, A. (2003). Pathogenesis of endometriosis.Obstetrics
and gynecology clinics of North America, 30(1), 41. Retrieved from http://ac.
159
els-cdn.com/S1521693404000069/1-s2.0-S1521693404000069-main.pdf?_
tid=d7a40086-aa91-11e2-a072-00000aab0f02&acdnat=1366555594_
9cb65ac3af117128d0e008a357e9dfea
Surbey, M. K. (1987). Anorexia nervosa, amenorrhea, and adaptation. Ethology and
Sociobiology, 8, 47-61. Retrieved from http://ac.els-cdn.com/0162309587900
185/1-s2.0-0162309587900185-main.pdf?_tid=1ad4cc4c-a947-11e2-831
a-00000aab0f6b&acdnat=1366413543_bfc86f54ed49dad0fd28303742b4ba99
Stubbs, R. J., Hughes, D. A., Johnstone, A. M., Rowley, E., Reid, C., Elia, M., ... &
Blundell, J. E. (2000). The use of visual analogue scales to assess motivation to
eat in human subjects: a review of their reliability and validity with an evaluation
of new hand-held computerized systems for temporal tracking of appetite
ratings. British Journal of Nutrition, 84(04), 405-415.
Sleutel, M. R. (2003). Intrapartum nursing: Integrating Rubin's framework with social
support theory. Journal of Obstetric, Gynecologic, & Neonatal Nursing, 32(1),
76-82. Doi: 10.1177/0884217502239803
Tarasuk, V., & Beaton, G. H. (1991). Menstrual-cycle patterns in energy and
macronutrient intake. The American journal of clinical nutrition, 53(2), 442-447.
Retrieved from http://ajcn.nutrition.org/content/53/2/442.full.pdf
Tajnert, K., Tie, W., O’Neill, T. J., & Plavsic, S. K. (2013). Ultrasound assessment of
postpartum fever. Donald School Journal of Ultrasound in Obstetrics and
Gynecology, 7 (2), 219-230.
160
Tai, M. M., Castillo, T. P., & Pi-Sunyer, F. X. (1997). Thermic effect of food during each
phase of the menstrual cycle. The American journal of clinical nutrition, 66(5),
1110-1115. Retrieved from http://ajcn.nutrition.org/content/66/5/1110.full.pdf
Tiggemann, M., & Kemps, E. (2005). The phenomenology of food cravings: the role of
mental imagery. Appetite, 45(3), 305-313. Retrieved from http://ac.els-cdn.com
/S0195666305000826/1-s2.0-S0195666305000826-main.pdf?_tid=94ab7
bda-b075-11e2-a118-00000aab0f6c&acdnat=1367203162_541d0a0b1
5ff8b2d2b1ead9f175d5c65
Tsutsui, K. (2008). Progesterone biosynthesis and action in the developing
neuron.Endocrinology, 149(6), 2757-2761. Retrieved from
http://endo.endojournals.org/content/149/6/2757.full.pdf
Turnbull, K. E., Braden, A. W. H., & Mattner, P. E. (1977). The pattern of follicular
growth and atresia in the ovine ovary. Australian Journal of Biological
Sciences,30(3), 229-242. Retrieved from http://www.publish.csiro.au/?
act=view_file&file_id=BI9770229.pdf
Towne, B., Czerwinski, S. A., Demerath, E. W., Blangero, J., Roche, A. F., & Siervogel,
R. M. (2005). Heritability of age at menarche in girls from the Fels Longitudinal
Study. American journal of physical anthropology, 128(1), 210-219. Retrieved
from http://journals.ohiolink.edu/ejc/pdf.cgi/Towne_
Bradford.pdf?issn=00029483&issue=v128i0001&article=210_hoaamigftfls
161
Teirney, R., & Prentice, A. (2002). The medical management of endometriosis.Reviews
in Gynaecological Practice, 2(1), 91-98. Retrieved from http://ac.els-cdn.com
/S1471769702000035/1-s2.0-S1471769702000035-main.pdf?_tid=8e585
f16-aa92-11e2-bbe3-00000aacb360&acdnat=1366555900_
b8629a89493ae85d5ba4be2dacaef619
Theintz, G. E., Howald, H., Weiss, U., & Sizonenko, P. C. (1993). Evidence for a
reduction of growth potential in adolescent female gymnasts. The Journal of
pediatrics, 122(2), 306-313. Retrieved from http://www.sciencedirect.
com/science/article/pii/S0022347606801393
Tetsuka, M., & Hillier, S. G. (1997). Differential regulation of aromatase and androgen
receptor in granulosa cells. The Journal of steroid biochemistry and molecular
biology, 61(3), 233-239. Retrieved from http://ac.els-cdn.com/S09600
76097800179/1-s2.0-S0960076097800179-main.pdf?_tid=2d646be6-9f48-11
e2-b90a-00000aab0f26&acdnat=1365314492_e04ddfd12aa9cd1ba
8307e0181dacf76
Usman, S. A. B., Indusekhar, R., & O'Brien, S. (2008). Hormonal management of
premenstrual syndrome. Best practice & research. Clinical obstetrics &
gynaecology, 22(2), 251. Retrieved from http://ac.els-cdn.com
/S1521693407001253/1-s2.0-S1521693407001253-main.pdf?_tid=5d1505
fa-aa09-11e2-bc5a-00000aab0f02&acdnat=1366496976_280866b
067947173863e0620fd626dea
162
Van Eijkeren, M. A., Christiaens, G. C. M. L., Sixma, J. J., & Haspels, A. A. (1989).
Menorrhagia: a review. Obstetrical & Gynecological Survey, 44(6), 421-429.
Warren Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001). Theories of
endometriosis.European Journal of Obstetrics & Gynecology and Reproductive
Biology, 96(1), 21-34. Retrieved from http://ac.elscdn.com/S030121150000405X/1-s2.0-S030121150000405Xmain.pdf?_tid=870ae2e8-aa91-11e2-a116-00000aab0f6b&acdnat=
1366555458_7973aac08172509b5e922f952e56a29c
Viganò, P., Parazzini, F., Somigliana, E., & Vercellini, P. (2004). Endometriosis:
epidemiology and aetiological factors. Best Practice & Research Clinical
Obstetrics & Gynaecology, 18(2), 177-200. Retrieved from http://ac.els-cdn.com
/S1521693404000082/1-s2.0-S1521693404000082-main.pdf?_tid=899
bafa6-aa91-11e2-a116-00000aab0f6b&acdnat=1366555463_
7e9ec206299bcbf500854c9bff250906
, M. P., & Perlroth, N. E. (2001). The effects of intense exercise on the female
reproductive system. Journal of Endocrinology, 170(1), 3-11. Retrieved from
http://joe.endocrinology-journals.org/content/170/1/3.full.pdf+html
Wuttke, W., Theiling, K., Hinney, B., & Pitzel, L. (1998). Regulation of steroid
production and its function within the corpus luteum. Steroids, 63(5), 299-305.
Retrieved from http://ac.els-cdn.com/S0039128X98000373/1-s2.0-S0039128
X98000373-main.pdf?_tid=82e96c9c-9584-11e2-896c-00000aab0f6b
&acdnat=1364240893_93f363aabf8437ed63079f45f1c23e3c
163
Warren, M. P., & Perlroth, N. E. (2001). The effects of intense exercise on the female
reproductive system. Journal of Endocrinology, 170(1), 3-11. Retrieved from
http://joe.endocrinology-journals.org/content/170/1/3.full.pdf
West, R. (1987). Use and misuse of craving. British Journal of Addiction, 82(1), 39-42.
Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.1360-0443.
1987.tb01433.x/pdf
Weingarten, H. P., & Elston, D. (1990). The phenomenology of food cravings.Appetite,
15(3), 231-246. Retrieved from http://ac.els-cdn.com/0195666390900232/1-s
2.0-0195666390900232-main.pdf?_tid=8ce8a83c-b075-11e2-a118-00000
aab0f6c&acdnat=1367203149_2822ffa729d868fc99512e445749c4c0
Weingarten, H. P., & Elston, D. (1991). Food cravings in a college
population.Appetite, 17(3), 167-175. Retrieved fromm
http://www.sciencedirect.com/science/article/pii/019566639190019O
Waters, A., Hill, A., & Waller, G. (2001). Bulimics' responses to food cravings: is
binge-eating a product of hunger or emotional state?. Behaviour Research and
Therapy, 39(8), 877-886. DOI: 10.1016/S0005-7967(00)00059-0
Wurtman, R. J., & Wurtman, J. J. (1995). Brain Serotonin, Carbohydrate‐Craving,
Obesity and Depression. Obesity Research, 3(S4), 477S-480S. Retrieved from
http://onlinelibrary.wiley.com/doi/10.1002/j.1550-8528.1995.tb00215.x/pdf
Wurtman, J. J., Brzezinski, A., Wurtman, R. J., & Laferrere, B. (1989). Effect of nutrient
intake on premenstrual depression. American journal of obstetrics and
164
gynecology, 161(5), 1228-1234. Retrieved from http://dx.doi.org/10.
1016/0002-9378(89)90671-6
Webb, P. (1986). 24-hour energy expenditure and the menstrual cycle. The American
journal of clinical nutrition, 44(5), 614-619. Retrieved from
http://ajcn.nutrition.org/content/44/5/614.full.pdf
Windham, G. C., Elkin, E. P., Swan, S. H., Waller, K. O., & Fenster, L. (1999). Cigarette
smoking and effects on menstrual function. Obstetrics & Gynecology,93(1),
59-65. Retrieved from http://journals.lww.com/greenjournal/Abstract/
1999/01000/Cigarette_Smoking_and_Effects_on_Menstrual.13.aspx
Wei, A., & Pritts, E. A. (2003). Therapy for polycystic ovarian syndrome. Current
Opinion in Pharmacology, 3, 678–682. doi: 10.1016/j.coph.2003.06.004
http://ac.els-cdn.com/S1471489203001292/1-s2.0-S1471489203001
292-main.pdf?_tid=692d44e0-aa15-11e2-bbf6-00000aab0f02&
acdnat=1366502151_2a7f61672fe1a64100db5cfd1ccf7082
Young, S. L., & Lessey, B. A. (2010, January). Progesterone function in human
endometrium: clinical perspectives. In Seminars in reproductive medicine (Vol.
28, No. 1, p. 005). Retrieved from http://www.hapmd.com/home/hapmdcom/
public_html/wp-content/uploads/2009/03/sub/articulos-e-imagenes/20110602
_p4_y_endometrio.pdf
Young, E. A., Midgley, A. R., Carlson, N. E., & Brown, M. B. (2000). Alteration in the
hypothalamic-pituitary-ovarian axis in depressed women. Archives of General
165
Psychiatry, 57(12), 1157. Retrieved from http://archpsyc.jamanetwork.
com/article.aspx?articleid=481685
Yen, J. Y., Chang, S. J., Ko, C. H., Yen, C. F., Chen, C. S., Yeh, Y. C., & Chen, C. C.
(2010). The high-sweet-fat food craving among women with premenstrual
dysphoric disorder: Emotional response, implicit attitude and rewards
sensitivity.Psychoneuroendocrinology, 35(8), 1203-1212. Retrieved from
http://ac.els-cdn.com/S030645301000051X/1-s2.0-S030645301000051
X-main.pdf?_tid=561d1342-b075-11e2-a99b-00000aacb361&acdnat=
1367203057_c6bf302a0649c051fd386af0d457256f
Zeleznik, A. J. (2004). The physiology of follicle selection. Reprod Biol Endocrinol,2,
31. Retrieved from http://www.rbej.com/content/pdf/1477-7827-2-31.pdf
Zhu, B. T., & Conney, A. H. (1998). Functional role of estrogen metabolism in target
cells: review and perspectives. Carcinogenesis, 19(1), 1-27. Retrieved from
http://carcin.oxfordjournals.org/content/19/1/1.full.pdf