DYSPHONATIONS IN INFANT CRY: A POTENTIAL MARKER FOR HEALTH STATUS
Katlin J. Abbs
A Thesis
Submitted to the Graduate College of Bowling Green
State University in partial fulfillment of
the requirements for the degree of
MASTER OF SCIENCE
MAY 2015
Committee:
Alexander Goberman, Advisor
John Folkins
Ronald Scherer
ii
ABSTRACT
Alexander M. Goberman, Advisor
Sudden infant death syndrome (SIDS) is defined as an unexplained death in an infant’s
first year of life. Risk factors for SIDS include maternal smoking, sex, and infant sleep
positioning, among others. The current study analyzed dysphonations in the cries of 32 infants
24-66 hours after birth. Dysphonations are acoustic characteristics of cries and include
frequency shift (FS), harmonic doubling (HD), biphonation (BP), and noise (N). An interaction
effect was found, male infants whose mothers smoked during pregnancy (maternal smoking
status) had a significantly lower percent of dysphonations than male infants whose mothers did
not smoke during pregnancy (no maternal smoking status). No significant main effects were
found for the factors maternal smoking status, sex, infant positioning, or partition. In addition,
the types of dysphonations were consistently distributed across groups with noise being the most
commonly occurring dysphonation followed by harmonic doubling, frequency shift and then
biphonation. It is hypothesized that differences in number and type of dysphonations may either
be an effect of differences in infant arousal and/or developmental differences. A lower number of
dysphonations seen in male infants with mothers who smoked during pregnancy may suggest a
lowered arousal state, which may be associated with the occurrence of SIDS.
iii
ACKNOWLEDGMENTS
I would like to acknowledge my advisor, Dr. Goberman, along with my committee
members Dr. Folkins and Dr. Scherer, for their guidance and their time spent helping me to
improve my project and learn about research. I would also like to thank Dr. Jason Whitefield, a
doctorate student in Communication Sciences and Disorders, who frequently answered my
questions in the lab and helped further my understanding of my research topic.
iv
TABLE OF CONTENTS
Page
INTRODUCTION
............................................................................................................
1
Acoustics
............................................................................................................
1
SIDS
............................................................................................................
1
Pre-term vs. Full Term ...............................................................................................
3
Infant Positioning .......................................................................................................
5
Maternal Smoking ......................................................................................................
7
Sex
............................................................................................................
8
Partition
............................................................................................................
9
Dysphonations............................................................................................................
9
Goal of Study ............................................................................................................
11
METHODOLOGY
............................................................................................................
12
Participants
............................................................................................................
12
Procedures
............................................................................................................
14
Statistics
............................................................................................................
19
Reliability
............................................................................................................
19
............................................................................................................
21
Comparison of Types of Dysphonations....................................................................
22
RESULTS
DISCUSSION
............................................................................................................
26
Prone versus Supine Position .....................................................................................
27
Male versus Female ...................................................................................................
27
Partition
28
............................................................................................................
v
Effect of Maternal Smoking.......................................................................................
29
Distribution of Dysphonations ...................................................................................
29
SIDS
............................................................................................................
30
Limitations
............................................................................................................
31
Summary and Conclusions ........................................................................................
32
REFERENCES
............................................................................................................
33
APPENDIX A. HSRB APPROVAL .....................................................................................
38
APPENDIX B. STUDY OUTLINE .....................................................................................
40
vi
LIST OF FIGURES
Figure
Page
1
Harmonic Doubling (HD) ..........................................................................................
15
2
Biphonation (BP) .......................................................................................................
16
3
Frequency Shift (FS) ..................................................................................................
17
4
Noise (N)
............................................................................................................
18
5
Interaction Effect of Sex vs. Maternal Smoking Status ............................................
24
6
Distribution of Types of Dysphonations ....................................................................
25
vii
LIST OF TABLES
Table
Page
1
Characteristics of Infants Used in the Study ..............................................................
13
2
Percent Dysphonations ..............................................................................................
23
1
INTRODUCTION
Acoustics
Acoustic analysis of infant cry has been used in a number of different studies. Studies
have compared parental perception of an infant’s distress to acoustic variables such as F0 (e.g.,
LaGasse, Neal & Lester, 2005; Lester, Boukydis, Garcia-Coll, Hole, & Peucker, 1992). Another
way that infant cry can be analyzed is by using acoustics to infer the health status of an infant.
Specifically, acoustic analysis of infant cry has been used to examine the effects of term status,
(e.g., Goberman & Robb, 1999; LaGasse et al., 2005; Robb, 2003), infant positioning
(Goberman, Johnson, Cannizzaro, & Robb, 2008), maternal smoking (e.g., LaGasse et al., 2005),
and sex (e.g., Fuller, 2002). In addition, a number of studies have used infant cries to infer risk
of Sudden Infant Death Syndrome (SIDS; Corwin et al., 1995; Stark & Nathanson, 1975)
SIDS
An unexplained death in an infant’s first year of life is defined as SIDS (Byard & Krous,
2003). SIDS is the leading cause of death in infants between 1 month and 1 year of age (Moon,
Horne, & Hauck, 2007). Risk factors associated with SIDS include preterm birth (<37 weeks),
male sex, prone sleep positioning, maternal smoking during pregnancy or alcohol use during
pregnancy, and neonatal conditions such as jaundice or bradycardia (Hoffman, Damus, Hillman,
& Krongrad, 1988). Infant cry analysis may hold clues that could aid in identifying infants at
risk for SIDS (Goberman et al., 2008).
Acoustic analysis of infant cries has been used by a number of researchers in the
investigation of SIDS. Stark and Nathanson (1975) stated that cry characteristics of infants who
eventually died of SIDS were different compared with healthy infants in regards to the overall
pattern of the cry and the frequency of certain segmental features. The segmental features that
2
occurred at a higher frequency in SIDS infants compared to non-SIDS infants included voiceless
inspiratory snort, constriction of the vocal tract, high and extremely high pitch, and pitch shift.
Suprasegmental features such as a lower mean cry duration in SIDS infants was also observed
(Stark & Nathanson, 1975).
First formant measures may also help identify infants at risk for SIDS. Corwin et al.
(1995) examined the pain cries of 21,880 healthy infants 2 days after birth and tracked the
infants over time. Twelve of the infants later died of SIDS. The study found that high first
formant (F1) values and a high number of mode changes were associated with an increase in risk
of dying of SIDS. There was an even greater increase of an infant dying of SIDS when the high
formant value persisted throughout the cry (Corwin et al., 1995).
Infant arousal may also have implications for SIDS research. Kahn et al. (2002)
describes that infants experiencing respiratory distress may experience reduced arousability. A
decrease in arousability may be detrimental to an infant when encountering a life-threatening
event such as a need to breathe (Kahn et al., 2002). Goberman and Whitfield (2013) used
fundamental frequency (F0) as a means for measuring infant arousal in 58 healthy infants. They
found that F0 was the highest immediately following a pain stimulus, which supports the F0
arousal relationship that an increased F0 may signal infant distress. Therefore, SIDS risk in
apparently healthy infants using the hypothesized relationship between F0 and infant arousal may
help identify SIDS infants (Goberman & Whitfield, 2013).
LaGasse et al. (2005) analyzed cry characteristics of infants with conditions that may be
associated with an increased risk for SIDS. The study examined cry features of infants with low
birth weight, hyperbilirubinemia (jaundice), and infants with drug exposure during pregnancy.
They measured cry latency, hyperphonation, dysphonation, F0, first formant (F1), and second
3
formant (F2). Differences in cry characteristics were observed based on an infant’s medical
condition. For example, premature infants were found to have a higher F0 and a shorter duration
of the cry, whereas infants with prenatal tobacco exposure were observed to have an increased
F0, an increased F2 frequency, and an increase in variability in the amplitude of the cry (LaGasse
et al., 2005). In addition to these factors, other factors associated with SIDS risk have been
investigated using acoustic analysis of infant cry.
Pre-term vs. Full-Term
Pre-term infants often exhibit a greater number of health problems than full-term infants.
A greater number of structural abnormalities can often be found in the cerebrum when compared
to full term infants (Inder, Warfield, Wang, Huppi, & Volpe, 2005). These abnormalities may
lead to an abnormal neurodevelopment in the short-term, in addition to possible longer-lasting
effects. Rona, Gulliford and Chinn (1993) found that shorter lengths of gestation correlated with
an increase in respiratory illness later in life. Term status is also a risk factor for SIDS. Malloy
and Hoffman (1995) analyzed birth/death certificates and found that premature infants were
more likely to die from SIDS than full-term infants. Horne et al. (2001) found that gestational
age is inversely correlated with infant arousability, which likely contributes to the fact that
preterm infants are at a higher risk for SIDS (Horne et al., 2001).
Acoustic differences can also be found in preterm infants when compared with full-term
infants. Past research has looked at acoustical differences in infant cries of healthy full-term vs.
healthy pre-term infants (Goberman & Robb, 1999). Based on an acoustic analysis of crying
behavior that compared 10 full-term and 10 preterm infants, preterm infants were found to
display a higher first spectral peak (i.e., higher F0) than full term infants. Preterm infants also
did not display a significant change in crying behavior across each crying episode whereas full
4
term infants showed a change. Preterm infants’ lack of change across crying episodes may reflect
an immature neurological system because of the lack of organization (Goberman & Robb, 1999).
LaGasse et al. (2005) completed a review of the literature examining pre-term infants and fullterm infants. Based on the review, pre-term infants showed an increased F0, increased F0
instability (biphonation), and a decreased cry duration when compared with full-term infants.
Similar results were found by Goberman and Whitfield (2013) in an examination of 11 pre-term
infants versus 47 full-term infants. In this study, pre-term infants were found to display higher
F0 in the first cry following a pain stimulus, although this finding was only significant in female
infants (Goberman & Whitfield, 2013).
It is unclear whether acoustic differences between full-term and pre-term infants are a
result of a respiratory disadvantage in pre-term infants or if structural differences also may play a
role. Cacace, Robb, Saxman, Risemberg and Koltai (1995) found that the occurrence of
harmonic doubling (HD), a series of harmonics that occur simultaneously with the F0 and its
harmonics, was greatly influenced by the weight and conceptional age of the infants.
Specifically, HD occurred most frequently in infants who weighed between 1501-2500 grams (g)
and occurred less frequently in infants who were less than 1500 g or more than 2500 g. The
presence of HD occurred in infants >31 weeks conceptional age but not in infants <30 weeks.
These findings suggest that acoustical differences could have been a result of factors associated
with age and weight of the infant at the time of the recording (Cacace et al., 1995). Overall,
acoustic differences have been found between full-term and pre-term infants, which may be the
result of decreased arousability, a respiratory disadvantage, or weight differences in pre-term
infants (Goberman & Robb, 1999; Horne et al., 2001; Rona et al., 2003; Cacace et al., 1995).
5
Infant Positioning
Infants placed to sleep in the prone position (belly) are at a higher risk for SIDS
compared to infants placed to sleep in the supine position (back) (Hoffman et al., 1988). Early
research on infant sleep position and SIDS began after a survey that examined whether infants
sleep in the prone or supine position (Beal, 1988). It was found that the proportion of infants
who slept in the prone position increased from 1970 to 1989 and decreased in 1990. SIDS
related deaths were also examined, and it was found that SIDS deaths were highest between
1970-1989 and decreased in 1990 and 1991. These findings revealed a possible relationship
between sleeping position and SIDS, specifically the importance of placing babies in the supine
position (Beal, 1988).
In the late 1980’s and early 1990’s health organizations across the world began a “Back
to Sleep” campaign which emphasized placing infants on their backs (supine) to sleep (Hoffman
et al., 1988). Results of the campaign decreased the prevalence of infants sleeping in the
prone/stomach down position, and the number of SIDS cases decreased (Hoffman et al, 1988).
The United States launched the campaign in 1994, which reduced the number of infants sleeping
in the prone position (Task Force on Sudden Infant Death Syndrome, 2005). Chang, Keens,
Rodriquez and Chen (2008) reported that SIDS deaths decreased 77% in California from 19892004 during the time that the “Back to Sleep” campaign was implemented.
Research has shown that babies sleeping in the prone position may be at an increased risk
for SIDS (Alm et al., 2006; Yiallourou, Walker, & Horne, 2008). Infants sleeping in the prone
position may have a poorer ventilatory response to an increased level of CO2 than infants in the
supine position (Smith, Saiki, Hannam, Rafferty, & Greenough, 2010). Although infants were
not shown to have a mechanical respiratory advantage in the supine position versus the prone
6
position in the study, their reduced ventilatory response to CO2 implies that infants lying in the
prone position may have a disadvantage to responding to adverse stimuli (Smith et al., 2010). It
was also found that infants have a reduction of baroreflex sensitivity when in the prone position
because of a drop in blood pressure (Yiallourou, Sands, Walker, & Horne, 2011). Baroreflex is
the body’s mechanism for regulating blood pressure, and therefore a decrease in sensitivity may
lead to an infant’s lack of control of his/her blood pressure in the prone position. Another theory
on why prone positioning may increase SIDS is that infants may be rebreathing CO2 in the prone
position. This elevates CO2 levels, which may be harmful to the infant (Patel, Harris, & Thach,
2001).
In addition to physiological studies, studies have examined the acoustic differences in
infant cries associated with infant sleep position. Goberman et al. (2008) examined 51 cry
samples. The study included 21 infants recorded in the supine position and 30 infants recorded
in the prone position. Based on a long-time average spectrum (LTAS) analysis, infants in the
supine position displayed a higher mean spectral energy (MSE) and a lower spectral tilt (ST)
than infants in the prone position. Differences in MSE were interpreted to reflect an increased
laryngeal muscle tension in the supine position. Differences in ST were thought to be due to
increased glottal adduction in the supine position. Overall, these data point to the possibility that
the infants in the prone position were demonstrating decreased arousal in response to the pain
stimulus compared to infants in the supine position (Goberman et al., 2008). Lin and Green
(2007) suggest that posture interacts with other variables. When infants were placed in the
upright position from the supine position the F0 increased. However, when the infants were then
laid back into the supine position no change in F0 was observed. This difference in change based
on infant positioning was interpreted as an F0 difference due to an increased arousal and not
7
necessarily just because of the posture change (Lin & Green, 2007). Therefore, both Goberman
et al. (2008) and Lin and Green (2007) found acoustic differences in infants based on positioning
which was interpreted as a difference in arousal.
Maternal Smoking
Exposure to cigarette smoke during and after pregnancy is another risk factor for SIDS
(Byard & Krous, 2003). DiFranza, Aligne, and Weitzman (2004) explain that maternal smoking
during pregnancy can lead to decreased lung growth, increased number of respiratory infections,
and asthma in infants, which negatively impacts their health. Wisborg, Kesmodel, Henriksen,
Olsen and Secher (2000) surveyed mothers of a group of 24,986 children, 30% in which were
categorized as smokers. They found that children of smokers had a 3 times greater chance of
dying of SIDS than children of non-smokers, and concluded that some SIDS cases could be
avoided if the mother stopped smoking during pregnancy (Wisborg et al., 2000). In a comparison
across groups, maternal smoking during pregnancy was more common in a group of infants that
died of SIDS than a group of infants that died of non-SIDS related deaths (Duncan et al., 2007).
This may be because infants of smokers had a reduced arousability during REM sleep, which
displays a respiratory disadvantage (Franco et al., 1999). Chong, Yip, and Karlberg (2004)
assessed data on the prevalence of factors such as maternal smoking on 1,105 infants who died
of SIDS, 2,115 who died of other causes, and 11,050 live control infants. Results show that the
prevalence of SIDS related deaths increased in maternal smokers (Chong et al., 2004). Andres
and Day (2000) describe that maternal smoking is a risk factor for SIDS as a result of impaired
lung function due to in-utero tobacco exposure.
Infant cries have been shown to be different in infants of mothers who smoke compared
to infants of non-smoking mothers. Nugent, Lester, Greene, Wienczorek-Deering, and
8
O’Mahony (1996) obtained cries of 127 infants in the supine position. Overall, 7.9% of the
mothers smoked 20-40 cigarettes a day, 22.8% smoked 10-20 cigarettes a day, and 30 percent
smoked less than 10 cigarettes a day. The rest were classified as non-smokers. When cigarette
smoking increased, acoustic differences were observed. Fundamental frequency increased along
with variability of the second formant when cigarette smoking increased (Nugent et al., 1996).
LaGasse et al. (2005) also observed similar differences in infants with prenatal tobacco exposure.
They found that infants who had been exposed to tobacco had an increased F0, increased F2, and
an increased variability in F2 (LaGasse et al., 2005). It is hypothesized that differences in infant
cries are affected by maternal smoking during pregnancy due to a decreased arousal response of
infants whose mothers smoked during pregnancy.
Sex
In addition to term status, maternal smoking, and infant positioning, sex is also a risk
factor for SIDS. Males are more likely to die from SIDS than females (Hoffman et al., 1988).
Infant arousability may play a factor in sex differences among infants at risk for SIDS (Mitchell
& Stewart, 1997; Richardson, Walker, & Horne, 2010). Male infants often have more immature
sleep-wake organization patterns compared to female infants, which may affect infant arousal
(Mitchell & Stewart, 1997).
Differences in cry characteristics have also been studied between sexes. Acoustic
differences such as general crying behavior, F0, and LTAS variables have been examined. Fuller
(2002) elicited cries from infants between the ages of 2 weeks and 12 months and recorded
acoustic and non-acoustic measures. Infants’ states, behaviors, and facial expressions did not
vary, but younger female infants displayed more general broadcast crying than males.
Fundamental frequency differences were also found at 7-12 months after birth, as male cries
9
were lower in pitch (Fuller, 2002). Time spent crying, however, was similar across genders in
cries elicited 2 weeks after birth (Fuller, 2002). One study found acoustic differences between
51 healthy male and female infants 1-3 days after birth (Goberman et al., 2008). Lower average
mean spectral energy (MSE) and a higher average spectral tilt (ST) were recorded in male
infants, which may indicate a decreased arousal response to the pain stimulus in male infants
(Goberman et al., 2008).
Partition
There have also been differences found in the acoustics of infant cry based on partition,
or more precisely a specific time segment of a cry. Goberman et al., (2008) separated infant cries
into 3 equal segments/partitions. They found a statistically significant effect of partition across
the acoustic variables mean spectral energy (MSE), spectral tilt (ST), and the spectral moment
measures spectral mean, standard deviation (SD), skewness and kurtosis. The MSE, spectral
mean, and spectral SD were significantly higher in the first partition while ST, spectral
skewness, and spectral kurtosis were significantly lower in the first partition than the second and
third partitions. Acoustic differences across partitions were interpreted to be a result of an
increased arousal response immediately following the pain stimulus. Goberman and Whitfield
(2013) also found acoustic differences when comparing the first 30 seconds of an infant’s cry
immediately following a pain stimulus with the last 30 seconds of an infant’s cry. They found
that mean F0 decreased in the second partition, or last 30 seconds of the cry. A decreased F0 over
time demonstrated a decrease in tension over time.
Dysphonations
Although dysphonations are often present in infant cries, Cecchini, Lai, and Langher
(2010) describe that dysphonations may be indicators of infant distress and are often present in
10
at-risk infants. Dysphonic cries occur during the expiratory phase of the cry and they are defined
by noisy or non-harmonic vocal fold and laryngeal tissue vibration and may cause the harmonics
to not be present (Kheddache & Tadj, 2013). Cry characteristics of healthy infants were
compared to infants with various pathologies such as vena cava thrombosis, meningitis,
peritonitis, asphyxia, hyperbilirubinemia, gastroschisis, and respiratory distress syndrome
(Kheddache & Tadj, 2013). They explain that the length of dysphonic segments in relation to
non-dysphonic voiced segments may provide information on the health of an infant. When
comparing healthy preterm infants and healthy full term infants, dysphonic and unvoiced
segments of healthy pre-term infants were larger. Infants with asphyxia showed the highest
number of dysphonations (Kheddache & Tadj, 2013). Although there has been research looking
at the effects of term status on cry dysphonations, limited research has been done to examine
how cry dysphonations are affected by other risk factors for SIDS such as sex, maternal smoking
and infant positioning.
Robb (2003) also examined dysphonations by recording the cries elicited from a pain
stimulus of 11 full-term and 16 preterm-infants. He performed an acoustical analysis on
expiratory cry segments of at least 500 ms and coded the cries using 4 measures that are
characterized as types of dysphonations. The four characteristics he used were: fundamental
frequency shift (FS); harmonic doubling (HD); biphonation (BP); and noise (N). Robb (2003)
found that full term infants displayed more HD and N segments than pre-term infants. However,
no significant differences appeared in the occurrence of FS and BP between full and pre-term
infants (Robb, 2003). In addition, Cacace et al., 1995 examined the dysphonations HD, BP and
FS in pre-term and full-term infants. They found differences in the occurrence of HD based on
term status, which was hypothesized to be a result of differences in the weight of the infants.
11
Overall, very little work has been done examining dysphonations in infant cries (Robb, 2003;
Cacace et al., 1995). However, findings of the studies suggest that there may be promise in
examining dysphonations to predict the health status of an infant.
Goal of Study
The aim of the study was to see if the SIDS risk factors sex, infant positioning, and
maternal smoking status have an effect on the dysphonations of infant cries, in addition to the
effect of partition. Specifically, the goal was to examine if the percent of dysphonations differ
based on these risk factors. Previously, acoustic cry characteristics were found to differ based on
sex, infant positioning, maternal smoking status, and partition although it is unknown how
dysphonations might differ across these factors. By understanding any acoustic cry differences
related to SIDS risk factors, we may be able to better predict which infants are at risk for SIDS
based on the acoustics of their cry.
12
METHODOLOGY
Participants
The measures for this study were taken from a sample of infants born at Wood County
Hospital, in Bowling Green, Ohio. A subset of 32 infants were included in the present study that
met the following criteria: (a) displayed more than 60 seconds of crying; and (b) displayed at
least 10 expiratory cries for each 30 second window.
The sample included 16 males and 16 females. Fourteen of the infants had mothers who
reported smoking during pregnancy (maternal smoking) and 18 infants had mothers who did not
smoke (no maternal smoking). The average gestational age for the infants used in the study was
38.99 weeks with a minimum age of 35.71 weeks and a maximum age of 41.86 weeks. Five of
the babies were considered to be pre-term (<37 week gestational age) and 27 were full-term.
Positioning also differed as 11 infants were recorded in the prone position (belly) and 21 infants
were recorded in the supine position (back). Table 1 below shows the distribution of infants
among the variables of maternal smoking, infant position, and sex.
None of the infants had a medical diagnosis. The infants included in the study had the
following averages and ranges; average weight in pounds of 7.25 with a range of 5.06 lbs-9.14
lbs; average length in inches= 19.57 with a range of 18-22 in.; average head circumference=
13.37 cm with a range of 12.5-14.5 cm. The infants had an average apgar rating of 8.34
immediately following birth (range of 4-9) and an average apgar rating of 8.97 (range of 8-9) 5
minutes after birth. Refer to Table 1.
13
Table 1
Characteristics of Infants Used in the Study
ID#
Maternal
Smoking
Position
Sex
Weight (grams)
Length
(inches)
Gestational Age
(weeks)
20.00
20.25
19.50
19.50
19.00
22.00
19.00
18.50
21.00
20.00
20.50
18.00
19.75
18.75
19.50
18.00
19.00
19.00
21.50
18.50
20.50
21.00
18.50
20.00
19.50
19.50
18.50
18.50
20.00
19.00
19.50
20.50
Head
Circumfe
rence
13.75
13.50
12.50
12.99
13.50
14.50
13.25
13.00
13.50
13.25
13.75
12.50
13.75
12.50
13.75
13.25
13.75
12.50
14.50
13.25
12.75
13.75
13.25
14.00
13.75
13.25
13.50
13.50
13.75
13.25
13.25
12.50
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
No
No
No
No
No
No
No
No
No
No
No
No
No
No
No
No
No
No
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Prone
Prone
Prone
Prone
Supine
Supine
Supine
Supine
Supine
Prone
Prone
Supine
Supine
Supine
Supine
Supine
Supine
Supine
Prone
Prone
Prone
Prone
Supine
Supine
Supine
Prone
Supine
Supine
Supine
Supine
Supine
Supine
Male
Male
Male
Male
Male
Male
Male
Male
Male
Female
Female
Female
Female
Female
Female
Female
Female
Female
Male
Male
Male
Male
Male
Male
Male
Female
Female
Female
Female
Female
Female
Female
3743.00
3930.00
2827.00
3572.00
3222.00
4111.00
3273.00
3203.00
3439.00
3430.00
3659.00
2316.00
3468.00
2370.00
3617.00
2970.00
3313.00
2749.00
3772.00
2905.00
3076.00
3883.00
3148.00
3657.00
3572.00
3479.00
2790.00
3102.00
3462.00
3092.00
3340.00
3005.00
MEAN
N/A
N/A
N/A
3296.71
Apgar Score
(1 minute)
Apgar Score (5
minutes)
39.29
39.57
36.71
39.43
38.71
39.57
36.00
39.14
38.00
38.57
39.43
35.71
40.71
35.71
38.57
36.86
38.43
37.86
40.86
41.86
39.00
39.86
40.40
41.71
39.71
39.29
40.43
41.00
38.71
38.00
39.00
39.71
Age at time of
Recording
(Hours)
28.25
28.33
25.10
24.73
42.80
28.25
37.67
33.00
25.75
66.00
24.16
54.93
29.18
54.47
49.58
53.76
24.10
31.00
30.30
43.10
50.65
27.00
48.75
24.25
33.00
29.72
24.63
27.66
39.08
43.58
24.23
32.65
9.00
9.00
8.00
9.00
9.00
9.00
9.00
9.00
7.00
8.00
9.00
7.00
9.00
8.00
4.00
8.00
9.00
8.00
9.00
9.00
8.00
8.00
8.00
9.00
9.00
7.00
9.00
9.00
9.00
8.00
9.00
8.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
8.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
9.00
19.57
13.37
38.99
35.61
8.34
8.97
14
Procedures
Data were collected immediately following a heel prick procedure as part of a state
mandated metabolic screening procedure. Infants were awake and not crying at the start of the
recording. They were recorded between 24-66 hours after birth with a mean recording of 33.5
hours after birth. A Shure SM58 cardioid microphone coupled with a Marantz PMD430
audiocassette recorder was used to record the cries at a distance of 15 cm.
Analysis was completed on the first 30 seconds of the infant’s cry following the pain
stimulus, and the last 30 seconds of the cry episode. Within each 30-second segment, the
number of expiratory cries was counted. In addition the following dysphonations were counted:
(1) Harmonic doubling (HD), defined as a doubling in the number of harmonics. The
original harmonics continue, but sub-harmonics appear at the mid-point between the
original harmonics. Note that the terms sub-harmonics and harmonic doubling have
both been used in infant and adult acoustic literature. An occurrence of HD was
counted when there were at least 2 HD harmonics of at least 50 ms in length (see
Figure 1).
(2) Biphonation (BP) is defined as when the original harmonics continue but additional
harmonics appear. However, unlike HD, the sub-harmonics are not simply a
doubling of the number of harmonics. Although the term biphonation has been more
commonly used in infant cry literature, biphonation may also be called diplophonia
(Cacace et al., 1995; Robb, 2003). In order for BP to have been counted, there must
have been at least 2 BP harmonics of at least 50 ms in duration (see Figure 2).
(3) Frequency shift (FS) is defined as an abrupt change in frequency at the level of at
least two different harmonics (see Figure 3).
15
(4) Noise (N) is defined as a loss of harmonic structure below 2500 Hz (see Figure 4).
Noise was only counted when it exceeded 50 ms in duration. A spectrum was
viewed if it was unclear whether harmonics were present based on the spectrogram
alone.
Figure 1: Harmonic Doubling (HD)
This figure shows harmonic doubling at frequencies directly in-between harmonics. An
example of harmonic doubling is outlined in red between 10.43 seconds and 10.54
seconds.
16
Figure 2: Biphonation (BP)
This figure shows harmonics at unrelated frequencies relative to the F0. The F0 value is
around 550 Hz, and a harmonic occurs just below and above the harmonics unrelated to
the F0.
17
Figure 3: Frequency Shift (FS):
This figure demonstrates frequency shift as it begins at 523 Hz and quickly moves to a
lower frequency at 25.1 seconds.
18
Figure 4: Noise (N)
This figure demonstrates noise between 9.02 seconds and 9.97 seconds. The noise occurs
below 2500 Hz when viewed through a spectrum.
19
If a dysphonation was not clear, a spectrum was viewed in order to verify its existence.
The acoustic signal was also used to help identify dysphonations if they were unclear from the
spectrogram.
Based on the occurrences of HD, BP, FS and N, percent occurrences were calculated
relative to the total number of expiratory cries. This was done by dividing the number of
expiratory cries containing at least 1 dysphonation by the total number of expiratory cries. In
addition, the relative distribution of each type of dysphonation was also calculated based on the
total number of dysphonations (e.g. # of HD/ Total # of Dysphonations).
Statistics
Prior to statistical analysis, all percentage data were converted to arc-sine, using a
standard conversion formula. To ensure a normal distribution of the percent date, the arc-sine
values were used for all statistical analyses. The arcsine conversion was required because the use
of analysis of variance (ANOVA) requires continuous data (Land, Smith, & Walz, 2012), and
percent data are not continuous. The arcsine formula used was: sin–1√[n/100], where n=
percentage value. Multivariate Analysis of Variance (MANOVA) was completed to examine the
independent variables of partition (first 30 seconds vs. last 30 seconds), maternal smoking
(maternal smoking vs. non-smoking), positioning (supine vs. prone), and sex (male vs. female).
Dependent variables for this test include overall occurrence of dysphonations.
Reliability
Inter-rater and intra-rater reliability were calculated based on re-analysis of 7 of the 32
infants (22%). The Pearson Product Moment Correlation (PPMC) statistic was used to compare
the total number of dysphonations between the original, inter-rater, and intra-rater data. Based
on this analysis, intra-rater reliability was found to be r= 0.975 (p<0.05), with an average
20
percent change of 1.6%. Inter-rater reliability was found to be r= 0.945 (p<0.05), with an
average percent change of 6.5%.
Reliability was also calculated for all of the data (# of expiratory cries, # of cries with
dysphonations, # of total dysphonations, # of expiratory cries with harmonic doubling, # of
expiratory cries with frequency shift, # of expiratory cries with biphonation, and # of expiratory
cries with noise) for both partitions. Intra-rater reliability for all of the data was r=.987
(p<0.05) and inter-rater reliability was r=.977 (p<0.05).
21
RESULTS
The current study investigated differences in percent dysphonations in infant cries based
on four variables (sex, positioning, maternal smoking, partition) related to SIDS risk. Data from
32 infant cries were used.
Before completing any statistical analysis, percent data were converted to arcsine values.
A multivariate repeated measure ANOVA was then conducted to determine if the independent
variables partition, sex, maternal smoking status, or positioning had an effect on the overall
percent of dysphonations. When examining percent dysphonation, there were no significant main
effects for partition [F(1,24)=0.414; p=0.526; µ 2=0.017], with 68.61% dysphonations for the
first partition and 62.41% dysphonations for the second partition (See Table 2). No significant
effect was found for sex [F(1,24)=3.63; p=0.069; µ 2=0.975], with an average of 70.48%
dysphonations for males and 59.86% for females. There was not a significant effect for
positioning [F(1,24)=0.992; p=0.329; µ 2=0.04], with an average of 70.48% dysphonation for
prone position and 62.90% for supine position. There was not a significant main effect for
maternal smoking status [F(1,24)=1.955; p=0.175; µ 2=0.075], with an average of 66.22%
dysphonations across maternal smoking status groups and 63.60% across infants with no history
of maternal smoking during pregnancy.
Contrary to the main effects, there was a significant interaction effect between the
variables sex and maternal smoking status [F(1,24)=13.291; p=0.001; µ 2=0.356]. No other
interaction effects were found. A post-hoc repeated measures ANOVA was completed to
examine the sex versus maternal smoking interaction (see Figure 5). Percent dysphonation was
examined separately in males and females. When males were examined alone, data showed a
significant effect in dysphonations according to maternal smoking status [F(1,12)=11.773;
22
p=0.005]. Males exposed to maternal smoking had significantly smaller percent dysphonation
compared to males not exposed to maternal smoking. Female only results indicated no
significant difference in the number of dysphonations based on maternal smoking status
[F(1,12)=3.861; p=0.073].
Comparison of Types of Dysphonations
The distribution of different dysphonation types (HD, FS, BP, N) was also examined. A
repeated measures ANOVA was completed to compare the relative occurrence of each type of
dysphonation. It was found that percent occurrence of noise (71.63%) was significantly higher
(p<0.05) than other types of dysphonations (HD, FS, BP). Both FS (6.48%) and BP (3.31%)
were significantly smaller than HD and N (p<0.05), but were not different from each other
(p>0.05). The dysphonation type HD (18.57%) was different from all other types of
dysphonations (larger than FS, larger than BP, and smaller than N). See Figure 6.
23
Table 2. Percent Dysphonations
Percent total Dysphonations = Number expiratory cries containing dysphonations/ total number
of expiratory cries. Percent Harmonic Doubling (HD), Frequency Shift (FS), Biphonation (BP),
and Noise (N); and Percent occurrence/total number of dysphonations are also listed. Total %
Dysphonations= HD%+FS%+BP%+N%)
% Total
HD%
FS%
BP%
N%
Total %
Dysphonations
Dysphonations
All Infants
Partition
1:
Partition
2:
68.61
19.83
6.70
3.48
69.96
100%
62.41
19.10
4.61
3.81
72.46
100%
Maternal Smoking Vs. No Maternal Smoking
Partition 1
Maternal 68.44
Smoking
No
68.83
Maternal
Smoking
Partition 2:
Maternal 64
Smoking
No
Maternal 68.83
Smoking
18.21
6.54
1.58
73.65
100%
21.92
6.91
5.92
65.23
100%
18.59
2.09
1.65
77.64
100%
21.92
6.91
5.92
65.23
19.13
20.54
5.49
7.92
4.70
2.26
70.66
69.26
100%
100%
18.59
19.76
2.09
7.84
1.65
6.59
77.64
65.79
100%
100%
71.73
66.97
16.63
21.45
7.90
6.08
6.09
2.12
69.37
70.28
100%
100%
69.24
58.83
11.08
23.31
9.20
2.20
4.08
3.67
75.62
70.80
100%
100%
100%
Male vs. Female
Partition 1:
Male
77.86
Female
59.36
Partition 2:
Male
63.11
Female
60.36
Prone vs. Supine
Partition 1:
Prone
Supine
Partition 2:
Prone
Supine
24
90.000
80.000
Percent Total Dysphonation
70.000
60.000
50.000
No Maternal Smoking
40.000
Maternal Smoking
80.337
66.597
30.000
57.478
54.523
20.000
10.000
0.000
Male
Female
Figure 5: Interaction Effect of Sex vs. Maternal Smoking Status
This figure shows the interaction effect between sex and maternal smoking. Male infants with
maternal smoking status have a lower percentage of dysphonations than male infants with no
maternal smoking status. In female infants, there is not a significant difference on the percent
dysphonations between infants whose mothers reported smoking during pregnancy and mothers
who reported not smoking during pregnancy.
25
80.000
70.000
Percent Dysphonation
60.000
50.000
40.000
71.632
30.000
20.000
10.000
18.570
0.000
HD
6.486
3.313
FS
BP
N
Type of Dysphonation
Figure 6: Distribution of Types of Dysphonations
This figure shows the average distribution of types of dysphonations across an infant’s cry.
Noise (N) is the most commonly occurring type of dysphonation followed by harmonic doubling
(HD). There is not a significant difference between percentage of frequency shift (FS) and
biphonation (BP).
26
DISCUSSION
Cry analysis was completed on 32 awake infants for 30 seconds directly following a pain
stimulus and 30 seconds at the end of their crying episode. The goal of this study was to
determine if sex, maternal smoking during pregnancy, infant positioning, or partition have an
effect on the number of dysphonations. The number and types of dysphonations were recorded,
including noise (N), harmonic doubling (HD), frequency shift (FS), and biphonation (BP) were
counted based on criteria created from Robb (2003). The percent of total dysphonations was
calculated based on the number of expiratory cries containing at least one dysphonation. In
addition, the distribution of dysphonations across type was calculated to determine the
occurrence of each type of dysphonation across an infant’s cry (N, HD, BP, FS).
According to Cacace et al. (1995), the weight and conceptional age of an infant may
affect the frequency of occurrence of dysphonations. Specifically, harmonic doubling (HD)
appeared more frequently in infants that weighed between 1501-2500 grams and occurred much
less frequently in infants who were less than 1500 g or more than 2500 g. Also, HD did not
appear in infants before the conceptional age of 30 weeks, and increased steadily between the
ages of 31-35 weeks. Infants in the current study had an average weight of 3296.71 g and an
average age of 38.99 weeks gestational age and thus on average weighed more and were older
than the infants studied in Cacace et al. (1995). An alternative explanation for dysphonations has
been offered by Robb (2003) finding that occurrences of dysphonations may be affected by
arousability and may be a marker for health status in an infant. Specifically, increased arousal in
response to pain may result in increased occurrence of dysphonations. The current data are
interpreted based on these two hypotheses. Specifically, it is possible that dysphonations are
27
related to (1) weight differences between infants; (2) unstable respiratory control; and/or (3)
arousal of the infants in response to pain.
Prone versus Supine Position
No significant effects were found when percent dysphonation was examined relative to
partition, sex, position, or maternal smoking status. Previous studies have found that when
infants are placed in the supine position, they have a poorer ventilatory response than infants in
the prone position (Smith et al., 2010). This ventilatory disadvantage was predicted to cause
infants in the supine position to have a decreased response to adverse stimuli. However, in this
study infants placed in the prone versus supine position did not display a difference in the
percent of dysphonations. Acoustical differences have also been found in infants when placed in
the prone versus supine position (Goberman et al., 2008). Goberman et al. (2008) found that
infants placed in the supine position displayed differences that were interpreted to be due to
increased arousal/laryngeal tension. This would also indicate that infants in the prone position
had a decreased arousal response/laryngeal tension from the pain stimulus. This may have
resulted from the stimulus not creating enough arousal or the variability in size/gestational age
within each position group. In addition it is possible that the study was underpowered to find
differences in prone versus supine positioning.
Male versus Female
In the current study there was no significant effect of sex on the number of
dysphonations. Previous studies have found sex differences in infant arousability and sleepwake organization patterns (Mitchell & Stewart, 1997). Male infants are said to have immature
sleep-wake patterns, and therefore may have a decreased arousal response. Based on the
previous statement that dysphonations may be related to arousability/laryngeal tension, it was
28
predicted that males would have fewer dysphonations than females (Robb, 2003). Although no
main effect was found in the current study, a sex X maternal smoking effect was found. Male
infants were found to have an effect based on maternal smoking and females were not found to
have such an effect. Acoustical differences have also been found between male and female
infants as males displayed a lower average mean spectral energy and a higher average mean
spectral tilt (Goberman et al., 2008). It was hypothesized that these findings were due to a
decreased arousal in male infants, which was not suggested by the percent dysphonations in the
current study. However, acoustical differences may also have been the result of laryngeal
differences between sexes (Cacace et al., 1995). In the current study there were only 16 males
and 16 females compared to the 20 males and 31 females in Goberman et al. (2008) and over 150
infants in the Cacace et al. (1995) study.
Partition
In the current study no significant effect was found for partition (first 30 seconds of an
infant’s cry vs. last 30 seconds). Previous studies have demonstrated acoustic differences across
time in infant cries (Goberman et al., 2008; Goberman & Whitfield, 2013). Specifically
Goberman and Whitfield (2013) found that the mean F0 decreased across time when comparing
the first 30 seconds of the cry to the last 30 seconds of the cry. Goberman et al. (2008) also
found acoustic differences in mean spectral energy and spectral tilt among others when
comparing three partitions of an infant’s cry. Acoustic differences across time have been
interpreted to display differences in arousal, as infants are more aroused immediately following a
pain stimulus. However, the current study did not show significant difference in the number of
dysphonations across partition. This could be due to a limited sample size or the fact that
dysphonations may not represent arousal as previously hypothesized.
29
Effect of Maternal Smoking
A significant interaction effect was found between the variables sex and maternal
smoking status. Males and female results were examined separately in order to determine the
effect of maternal smoking based on sex. Males who were exposed to maternal smoking were
found to have a significantly smaller percent of dysphonations than males who were not exposed
to maternal smoking. The percent of dysphonations that females exhibited did not differ based
on maternal smoking status. Male infants with maternal smoking status displayed a significantly
smaller percent of dysphonations than all other groups. In previous studies male infants have
displayed acoustic and ventilatory differences due to a decreased arousal response following a
pain stimulus (Mitchell & Stewart, 1997). Similar results were found in infants with prenatal
tobacco exposure as these infants demonstrated a respiratory disadvantage because of reduced
arousability in Franco et al. (1999). Therefore, previous studies have shown that both male
infants and infants with prenatal tobacco exposure have reduced arousability. Assuming
dysphonations are a health marker for arousability, these findings match the current study that
male infants with prenatal tobacco exposure have a decreased number of dysphonations.
Distribution of Dysphonations
In the current study 4 different types of dysphonations were recorded; harmonic doubling
(HD) characterized by a doubling of harmonics; frequency shift (FS) defined as an abrupt change
in frequency; biphonation (BP) defined as harmonics that occur at a frequency that is not directly
in between the original harmonics; noise (N) characterized by a loss of harmonic structure. All
the different types of dysphonations were found to be significantly different than each other
except FS and BP. Noise was the most prominent dysphonation with an average of 71.63%
percent of the dysphonations, followed by HD at 18.57% of the dysphonations. BP and FS were
30
not significantly different in percent of total dysphonation with a mean of 3.31% and 6.48%
respectively. This finding shows that on average, different types of dysphonations are more
prominent than others across a crying episode. Further investigation may be done in order to
determine if similar differences are seen across variables that may help identify SIDS risk such
as sex, infant positioning, and maternal smoking.
SIDS
Although all infants in the current study were normal, the study attempts to find a link
between SIDS risk factors and acoustic variables, specifically the percent of dysphonations.
Male sex, prone sleep position, and maternal smoking during pregnancy are all associated with
increased risk of SIDS (Hoffman, Damus, Hillman & Krongrad, 1988). Acoustic differences
have also been found in infants who later died of SIDS. Stark and Nathanson (1975) found
acoustic differences in infants who eventually died of SIDS including extremely high pitch,
constriction of the vocal tract, lower mean cry duration, and pitch shift. Corwin et al. (1995) also
found acoustic differences such as acoustic mode changes (similar to frequency shift) and high
first formant values in infants who later died of SIDS. In the current study only dysphonations
(specifically N, HD, FS and BP) were examined acoustically, but it was predicted that infants
who were at risk for SIDS would display differences in these variables. Male infants who were
exposed to maternal smoking were found to have a decreased number of dysphonations. These
two variables (male sex and maternal smoking exposure) are known risk factors for SIDS, and
therefore it is implied that an examination of dysphonations may be helpful in identifying infants
at risk for SIDS if there is a link between infant arousability and dysphonations.
31
Limitations
Infant cries were examined for 32 infants across two partitions on the type of
dysphonation in a cry segment of 30 seconds. Because three different variables were examined
(sex, position, maternal smoking), the number of infants in each group was relatively small. For
example, there was only 1 infant who was a female, prone position with maternal smoking status.
Because of exclusion criteria, the groups of infants were not equal.
Due to differences seen in individual infant cries, creating a set definition for each of the
types of dysphonations was a challenge. Subjective analysis through listening and using
spectrum information was used when infant cries did not exactly fit the criteria laid out in the
definitions. However, strong inter-rater and intra-rater reliability show that analysis measures
remained stable.
Dysphonations in infant cry have been examined in few studies (Cacace et al., 1995;
Robb, 2003) and therefore it is still relatively unknown what dysphonations represent.
Goberman et al. (2008) and Robb (2003) explain that infant acoustics can be affected by infant
arousal/laryngeal tension; whereas Cacace et al. (1995) state that dysphonations may be affected
by weight and conceptional age. Therefore, it is unknown if dysphonations are a negative health
marker or if they may not be affected by health status but instead by physiology. Although
Cacace et al. (1995) studied dysphonations, he did not include noise in his study, which was the
predominant type of dysphonation in the current study. Future studies further examine how
dysphonation type and percent differ across different SIDS risk factors. Future research can also
be done using the length of dysphonations as a dependent variable. In the current study a
dysphonation was counted as one dysphonation regardless of the length of time it occurred.
32
Summary and Conclusions
Infant cries have been examined acoustically in the past in order to associate acoustic
characteristics with health status of an infant, specifically term status, (e.g., Goberman & Robb,
1999; LaGasse et al., 2005; Robb, 2003), positioning (Goberman et al., 2008), maternal smoking
(e.g., LaGasse, et al., 2005), and sex (e.g., Fuller, 2002). In the current study cries of 32 infants
were analyzed for the percent and type of dysphonation (harmonic doubling, noise, frequency
shift, and biphonation) across two 30-second partitions. The independent variables in the study
were sex, positioning, maternal smoking status, and partition.
The results of the current study showed no significant main effects across the variables
partition, sex, positioning, or maternal smoking status for the percent of dysphonations.
However, there was a significant interaction effect between sex and maternal smoking status as
the percent dysphonations was significantly lower in males with maternal smoking status than in
males with no maternal smoking status. There was no difference on percent dysphonations for
female infants with maternal smoking status versus no maternal smoking status. It is interpreted
that this significant interaction effect in male infants whose mothers smoked during pregnancy
may be due to a decreased arousal response described in previous studies (Franco et al., 1999;
Mitchell & Stewart, 1997). Therefore, a decreased arousal response may lead to a decrease in
percent of dysphonations. A decreased arousal response is often seen in infants who are also at
risk for SIDS such as males, prone sleep positioning, and prenatal maternal tobacco exposure.
Therefore, the current study begins to connect possible risk factors for SIDS (male infants with
maternal smoking status) with acoustic measures, specifically percent of dysphonations.
33
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APPENDIX A. HSRB APPROVAL
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APPENDIX B. STUDY OUTLINE