The effects of menstrual cycle on the knee joint position sense

Knee Surg Sports Traumatol Arthrosc
(2005) 13: 649–653
KNEE
DOI 10.1007/s00167-004-0604-7
Sedat Tolga Aydoğ
Zafer Hasçelik
H. Ali Demirel
Onur Tetik
Ece Aydoğ
Mahmut Nedim Doral
The effects of menstrual cycle on the knee
joint position sense: preliminary study
Received: 7 January 2004
Accepted: 16 October 2004
Published online: 3 May 2005
Ó Springer-Verlag 2005
M. N. Doral (&)
Department of Orthopedics
and Traumatology,
Department of Sports Medicine,
Hacettepe University, Sıhhiye,
Ankara, Turkey
E-mail: [email protected]
Tel.: +90-312-3051347
Fax: +90-312-3051347
S. T. Aydoğ Æ H. A. Demirel Æ O. Tetik
Department of Sports Medicine,
Hacettepe University, Sıhhiye,
Ankara, Turkey
Z. Hasçelik
Department of Physical Medicine and
Rehabilitation, Hacettepe University,
Sıhhiye, Ankara, Turkey
E. Aydoğ
Department of Physical Medicine and
Rehabilitation, Ministery of Health,
Ankara Dişkapı Education
and Research Hospital,
Ankara, Turkey
Abstract The purpose of this study
was to determine the effects of
menstrual cycle on proprioception
by using the active knee joint position sense test (JPST). The 19 healthy women (ages between 20 years
and 27 years) who have normal
regular menstrual cycle were
included in the study. We applied
JPSTs at two different directions
throughout the three different phases of the menstrual cycle, i.e. menstrual, follicular, and early luteal in
dominant knees. When we started
Introduction
Sports is, over time, becoming a significantly important
part of people’s daily lives. In the 1900 Olympics Games,
only 3.5% of all participants were women, in 1996 this
percentage has risen to 39.8% [1]. As a result, incidence
of sportive injuries in women is also increasing [2]. In
addition, it has been reported that musculoskeletal
injuries are more common in women athletes than that
of men counterparts [1–5]. Although biomechanical
factors specific to women such as increased Q-angle of
the knee and wide pelvis has been held responsible by
from flexion (90°), target angles were
70°, 50°, and 30° and we started
from extension (0°), target angles
were 20°, 40° and 60°. The absolute
reposition errors from the target
angles have been evaluated. Results
have shown that reposition errors
from the target angle at 40°, 50° and
70° of knee angles were higher in the
menstrual phase than that of the
follicular phase (P<0.05). In addition, higher value of reposition error
from the target angle at 40° was
found in the menstrual phase compared to luteal phase (P<0.05). In
conclusion, we have demonstrated
that active JPST was significantly
reduced in the menstruation period.
Keywords Menstrual cycle Æ
Proprioception Æ Active joint
position sense
some authors [1–8], the reason for this increased incidence of sports injuries in women remain unclear [1–5].
During the course of a woman’s menstrual cycle,
there are some variations in the hormonal levels. At the
beginning of the menstrual cycle, estrogen (E) and progesterone (P) remain close to their minimum levels.
Towards the middle of the cycle, estrogen levels rise and
in the middle of the luteal stage both E and P levels
increase [9–11]. The changes in the levels of these hormones have some effects on bones, soft tissues, central
nervous system and connective tissues [9]. Indeed, both
animal and human studies have shown that higher
650
estrogen levels resulted in increased knee laxity [12–17].
Although hormonal changes might result in increased
injury risk for women athletes [7, 8], the effects of hormonal level on occurrence of injury in female athletes
are not fully understood [7, 8].
Proprioception is an important part of neuromuscular performance, and can be defined as the individual’s
awareness of his or her extremities’ position and motion
in space. Proprioception can be quantified by different
tests and mostly used tests are joint position sense
(JPST), threshold to detection of passive movement and
balance tests [18–24]. Because of its simple application,
JPST is the one of the most popular tests among the
above mentioned three tests. On the other hand, one
needs to consider both direction of movement and angle
of position when using JPST. For example, with symptomatic ACL-deficient knees, information of passive
movements in the nearly extended knee position was
found to be more sensitive towards extension than towards flexion in this test procedure [20].
The purpose of this study was to determine the effect
of hormonal changes on proprioception throughout the
menstrual cycle by using JPST. We applied JPST both
towards extension to flexion and flexion to extension at
three different angles in dominant knees.
Material and methods
To begin with, fifty young women (age: 20–27 years)
who perform daily living activities and are free of any
medical problems, were considered for this study. No
one in the group had used oral contraceptives within the
last 6 months. All subjects were nulliparous and not
pregnant at the time of the study. To be sure that they
had regular menstrual cycles of 26–32 days as they had
stated, they were followed for last three menstrual cycles. During this period, 28 females who had at least
3 days’ alteration in the anticipated menstruation dates
were excluded from the study. At the end of the experimental period, three more women were excluded from
the study (two had delays in their menstruations and the
third one had to use oral contraceptives because of an
ovarian cyst). The first day of the menstrual bleeding
was accepted as day 1. The subjects were tested three
times: during the menstrual phase (2nd–4th days), follicular phase (9th–11th days) and early luteal phase
(16th–18th days).
Participants’ eyes were closed during the active
JPST to eliminate visual stimulants [18]. In the test, the
subjects’ dominant knees were connected to a Biodex
System 3 dynamometer (Biodex Inc., Shirley, New
York), and they were in a semi-horizontal position
with their bodies at 70° of flexion [23]. Total extension
of the knee was defined as zero degrees. Since results
of JPSTs depend on angles and direction of the JPSTs
application [22, 24], we employed JPST at two different
directions (flexion towards extension, and vice versa)
with three different target angles. When we started
flexion (90°), target angles were 70°, 50°, 30° and we
started from extension (0°), target angles were 20°, 40°
and 60°. The Biodex moved the knee joint from a
starting angle to a given target angle. After the subject
had held her knee at the target angle for 5 s, it was
passively brought back to the starting angle. The
subject then reproduced the target angle, ending the
test by pressing a button at the moment that she
thought she reached that angle. The test was conducted
three times for each of the target angles, a total of 18
times for each measurement. The difference between
the passively given angle and the angle the subject
found was evaluated as the absolute reposition error
from the target, and the mean of the three trials at
every angle was accepted [21, 22]. Each subject performed the entire test at three different phases of the
cycle, and the order of the direction and target angle
of the test as well as phases of the cycle were chosen
randomly.
In statistical analysis, we compared mean absolute
reposition error from the target angles of JPSTs for each
phase. The significance level for statistical evaluation of
the measurements obtained from three different phases
of the menstrual cycle was P<0.05. Non-parametric
tests (Friedman two-way ANOVA) were used for the
groups without normal distribution characteristics and
Bonferonni for post hoc testing.
Because this study was designed to investigate changes in JPST with menstrual cycle in women, to make the
study more reliable, the JPST was performed on 13 male
subjects. In order to teach the tests to subjects, the same
JPSTs procedures were applied to all the subjects a day
before the day of test. For the reliability evaluation, the
tests were applied twice on the subjects with a week’s
interval in between tests. The correlation between the
measurements on two different dates and intraclass
correlation coefficient (ICC) were determined. Since the
results of the measurements had normal distribution,
they were evaluated with paired samples t-test at
P<0.05 significance level.
Results
Reliable results for all flexion and extension JPSTs are
shown in Table 1. In the reliability part of the study for
the JPSTs, there was no difference between two measurements among the male subjects (P>0.05), and the
ICC factor was between 0.62 and 0.83.
The results of the three phases of the menstrual cycle
for all flexion and extension JPSTs are shown in Fig. 1.
In the 40° JPST, there was a statistically significant
651
Table 1 Results of JPST on males at two different time points
20°
40°
60°
70°
50°
30°
JPST
JPST
JPST
JPST
JPST
JPST
First test
Second test
ICC
3.51°±1.89
4.41°±2.13
4.33°±2.25
2.56°±1.30
3.44°±1.84
3.61°±2.01
3.23°±1.55
3.82°±2.26
3.93°±1.77
2.87°±1.72
2.82°±1.81
3.18°±1.36
0.74
0.77
0.68
0.74
0.62
0.83
P>0.05
difference between early luteal phases and the menstrual
and follicular phases (P<0.05). In the 70° and 50°
JPSTs, the subject’s ability to correctly find the target
angle was best during the follicular phase (P<0.05).
During menstrual phase, the subject’s ability to find the
target angle was relatively poor compared to the other
phases of the menstrual cycle.
Fig. 1 Results of JSPT at different phases of the menstrual cycle.
Asterisks P<0.05. A Statistically significant differences were found
between three different phases; menstrual, follicular and early luteal
phases
Discussion
In this study, we investigated the effect of menstrual
cycle on proprioception by using JPST, which is one of
the most popular tests to evaluate proprioception. This
study has shown that different phases of menstrual cycle
resulted in different degree of reposition error from
target angle in JPSTs. Following is a brief discussion of
our findings.
The main observation of this study was that reposition errors from the target angle at 40°, 50° and 70° of
knee angles were higher in the menstrual phase than in
the follicular phase. In addition, higher value of reposition error from the target angle at 40° was found in the
menstrual phase compared to luteal phase. By using
other evaluation methods of proprioception, postural
sway and deficit in knee-joint kinesthesia in women close
to menstrual period has been reported [25]. Considering
of these two studies, female hormone levels may have
some effect on proprioception.
Although in our study we did not measure the hormonal values, we excluded the subjects who did not have
regular menstrual cycle for 3 months period just before
the study and subjects who had menstrual irregularity
during the experimental period. Therefore, only subjects
who had regular menstrual cycle were included in this
study. In addition, to reduce possible fluctuations of
hormonal levels during the menstrual cycle we examined
menstrual cycle in three phases.
Most of the studies about the effect of sex hormones,
especially estrogens, on sports injuries have been focused
on the laxity of the ACL [13–17]. On the other hand, the
effects of increased ACL laxity on injury rate of athletes
are controversial [1, 3, 8]. In the literature, there are
conflicting results regarding attribution of different
phases of menstrual cycle to sports related injuries.
There are some reports showing increased sports injuries
during the menstruation. [6, 26]. In contrast, Wojtys
et al. have shown increased sports injuries during the
ovulatory phase [9, 27]. Beyond that, it is proposed that
oral contraceptives may decrease the sports injuries
independent of different phases of the menstrual cycle
[26]. Nevertheless, all of those studies imply that level of
female hormones may change the rate of sports injury.
Although our study did not intend to evaluate the
effects of menstrual phases on the risk of sportive injuries in women, there are several reports showing that
deficiency in the proprioception may result in more
sports related injuries. Indeed, improvement of proprioception by conditioning and training has been shown
to provide protection against knee injury [28, 29]. By
using different proprioceptive tests, our study and study
by Friden et al. [25], have demonstrated proprioseptive
defects around menstruation. Therefore, these studies
are suggesting that hormonal level, by implementing
652
proprioception, may effect on sports injuries. Although
it is not clear how female hormones effects on proprioception, some studies suggest relationship between the
menstrual cycle and evoked potential measurements,
which may explain the changes in the proprioception
[30–32]. Changes in proprioception might be a consequence of changes in distal latency or of excitability of
the mechanoreceptors.
In our study significant decrement in JPST were
only evident in certain degrees of knee angles in both
flexion and extension of knee. Higher flexion angles,
except the target angles of 60°, especially ended with
significantly higher reposition error for JPSTs in menstrual phase as compared to the other phases. We do
not have an explanation for these findings. In our
preliminary study, we have shown that the reliability of
the JPST was sufficient for all target angles. One possible explanation could be that different knee positions
might be more sensitive to the evaluation of JPST [25].
Alternatively, there may not be enough difference in
the deviations at low flexion angles for JPST (20° and
30°).
In conclusion, we have demonstrated that active
JPST was significantly reduced during menstruation
period.
Acknowledgements Special thanks to the medical staff of Acıbadem
_
Hospital, Istanbul,
for their contributions.
References
1. International Medical Commission
Sports Medicine Manual (1990) Issues
specific to women. Lausanne, pp 133–
146
2. Hosea TM, Carey CC, Harrer MF
(2000) The gender issue: epidemiology
of ankle injuries in athletes who participate in basketball. Clin Orthop 372:45–
49
3. Arendt EA (1996) Common musculoskeletal injuries in women. Physician
Sports Med 24(7):39–48
4. Slauterbeck JR, Hardy DM (2001) Sex
hormones and knee ligament injuries in
female athletes. Am J Med Sci
322(4):196–199
5. Harmon KG, Ireland ML (2000) Gender differences in noncontact anterior
cruciate ligament injuries. Clin Sports
Med 19(2):287–302
6. Myklebust G, Maehlum S, Holm I,
Bahr R (1998) A prospective cohort
study of anterior cruciate ligament
injuries in elite Norwegian team handball. Scand J Med Sci Sports 8(3):149–
153
7. Ireland ML, Ballantyne BT, Little K,
McClay IS (2001) A radiographic analysis of the relationship between the size
and shape of the intercondylar notch
and anterior cruciate ligament injury.
Knee Surg Sports Traumatol Arthrosc
9(4):200–205
8. Huston LJ, Greenfield ML, Wojtys EM
(2000) Anterior cruciate ligament injuries in the female athlete potential risk
factors. Clin Orthop 372:50–63
9. Wojtys EM, Huston LJ, Lindenfeld TN,
Hewett TE, Lou M, Greenfield VH
(1998) Association between the menstrual cycle and anterior cruciate ligament injuries in female athletes. Am J
Sports Med 26(4):614–619
10. Hewett TE (2000) Neuromuscular and
hormonal factors associated with knee
injuries in female athletes. Strategies for
intervention. Sports Med 29(5):313–327
11. Speroff L, Glass RH, Kase NG (1999)
Chapter six: Regular menstrual cycle.
In: Clinical gynocologic endocrinology
and infertility, 6th edn. Lipincott Williams, Maryland
12. Liu SH, Al-Shaikh RA, Panossian V,
Finerman GAM, Lane JM (1997)
Estrogen affects the cellular metabolism
of the anterior cruciate ligament. Am J
Sports Med 25(5):704–709
13. Belanger MJ, Moore DC, Crisco JJ III,
Fadale PD, Hulstyn MJ, Ehrlich MG
(2004) Knee laxity does not vary with
the menstrual cycle, before or after
exercise. Am J Sports Med 32(5):1150–
1157
14. Van Lunen BL, Roberts J, Branch JD,
Dowling EA (2003) Association of
menstrual-cycle hormone changes with
anterior cruciate ligament laxity measurements. J Athl Train 38(4):298–303
15. Deie M, Sakamaki Y, Sumen Y, Urabe
Y, Ikuta Y (2002) Anterior knee laxity
in young women varies with their menstrual cycle. Int Orthop 26(3):154–156
16. Arnold C, Van Bell C, Rogers V, Cooney T (2002) The relationship between
serum relaxin and knee joint laxity in
female athletes. Orthopedics 25(6):669–
673
17. Karageanes SJ, Blackburn K, Vangelos
ZA (2000) The association of the menstrual cycle with the laxity of the anterior cruciate ligament in adolescent
female athletes. Clin J Sport Med
10(3):162–168
18. Sharma L, Paı YCP, Holtkamp K,
Rymer WZ (1997) Is knee joint proprioception worse in the arthritic knee
versus the unaffected knee in unilateral
knee osteoarthritis? Arthritis Rheum
40(8):1518–1525
19. Pai YC, Rymer WZ, Chang RW,
Sharma L (1997) Effect of age and
osteoarthritis on knee proprioception.
Arthritis Rheum 40(12):2260–2265
20. Koralewicz LM, Engh GA (2000)
Comparison of proprioception in arthritic and age-matched normal knees. J
Bone Joint Surg Am 82(11):1582–1588
21. Pincivero DM, Bachmeier B, Coelho AJ
(2001) The effects of joint angle reliability on knee proprioception. Med Sci
Sports Exerc 33(10):1708–1712
22. Friden T, Roberts D, Zatterstrom R,
Lindstrand A, Moritz U (1996) Proprioception in the nearly extended knee.
Measurement of position and movement in healthy individuals and in
symptomatic anterior cruciate ligament
injured patients. Knee Surg Sports
Traumatol Arthrosc 4(4):217–224
23. Birmingham TB, Kramer JF, Kirkley
A, Inglis JT, Spaulding SJ, Vandervoot
AA (2001) Knee bracing after ACL
reconstruction: effects on postural control and proprioception. Med Sci Sports
Exerc 33(8):1253–1258
24. Beynon BD, Renstrom PA, Konradsen
L, Elmqvist LG, Gottlieb D, Dirks M
(2000) Chapter 12: Validation of techniques to measure knee proprioception.
In: Lephart SM, Fu FH (eds) Proprioception and neuromuscular control in
joint stability. Human Kinetics, Champaign
653
25. Friden C, Hirshberg AL, Saartok T,
Backström T, Leanderson J, Renström
P (2003) The influence of premenstrual
symptoms on postural balance and
kinesthesia during the menstrual cycle.
Gynecol Endocrinol 17:433–439
26. Möller-Nielsen J, Hammar M (1989)
Women’s soccer injuries in relation to
the menstrual cycle and oral contraceptive use. Med Sci Sports Exerc
21(2):126–129
27. Wojtys EM, Huston LJ, Boynton MD,
Spindler KP, Lindenfeld TN (2002) The
effect of the menstrual cycle and anterior cruciate ligament injuries in women
as determined by hormon levels. Am J
Sports Med 30(2):182–188
28. Heidt RS Jr, Sweeterman LM, Carlonas
RL, Traub JA, Tekulve FX (2000)
Avoidance of soccer injuries with preseason conditioning. Am J Sports Med
28(5):659–662
29. Caraffa A, Cerulli G, Projetti M, Aisa
G, Rizzo A (1996) Prevention of anterior cruciate ligament injuries in soccer.
A prospective controlled study of proprioceptive training. Knee Surg Sports
Traumatol Arthrosc 4(1):19–21
30. Yilmaz H, Erkin EF, Mavioglu H,
Sungurtekin U (1998) Changes in pattern reversal evoked potentials during
menstrual cycle. Int Ophthalmol
22(1):27–30
31. Yadav A, Tandon OP, Vaney N (2002)
Auditory evoked responses during different phases of menstrual cycle. Indian
J Physiol Pharmacol 46(4):449–456
32. Kaneda Y, Ikuta T, Nakayama H,
Kagawa K, Furuta N (1997) Visual
evoked potential and electroencephalogram of healthy females during the
menstrual cycle. J Med Invest 44(1–
2):41–46