Effects of Sleeping Position and Time After Feeding on the

Effects of Sleeping Position and Time After Feeding
on the Organization of Sleep/Wake States in Prematurely
Born Infants
Michael M. Myers, William P. Fifer, Liza Schaeffer, Rakesh Sahni, Kiyoko Ohira-Kist, Raymond I. Stark, and Karl F. Schulze
Departments of Psychiatry and Pediatrics, Columbia College of Physicians and Surgeons, and Division of
Developmental Psychobiology, New York State Psychiatric Institute, New York, NY
Summary: Epidemiologic studies provide strong evidence for the conclusion that sleeping in the prone position places
infants at greater risk for sudden infant death syndrome (SIDS). Prior studies in newborn infants found that in the prone
sleeping position there is less time awake and more quiet sleep, but little change in the amount of active sleep. To determine whether the effects of sleeping position on state distribution vary with time after feeding, we studied prematurely born
infants in both the prone and supine sleeping positions. Sleep states were recorded each minute during interfeed intervals. Results demonstrate expected effects of sleep position on state distribution: prone sleeping is associated with a 79%
increase in quiet sleep and a 71% decrease in time awake. While the decreases in time awake are seen throughout the
interfeed interval, increases in quiet sleep in the prone position are found only within the first hour and again near the end
of the interfeed interval. These results are consistent with the hypothesis that prone sleeping could increase risk for SIDS
by altering the organization of sleep, and that time after feeding may play an important role in the expression of these
effects.
Key words: Sudden infant death syndrome; sleep positions; sleep states; time after feeding
SUDDEN INFANT DEATH SYNDROME is the third
leading cause of infant mortality in the US, and accounts
for nearly 30% of deaths during the postneonatal period.1
However, the physiologic mechanisms that underlie this
tragic syndrome remain unknown. At this time, nearly all
clinical information about SIDS is based on retrospective
data derived from the general population. Although accurate prospective identification of individual babies that are
likely to succumb is not yet possible, a number of factors
have been identified that are reliably associated with SIDS.
These associations continue to provide researchers with
important clues for directing their studies. After accounting
for other major risk factors, low birth-weight associated
with premature delivery is the most significant and consis-
tently reported risk factor for SIDS.2-4 This suggests that
systematic studies of prematurely born infants might provide key information concerning the physiologic disturbances that underlie SIDS.
During the 1970s, the view evolved that newborn
babies and infants should, in general, be placed in a prone
sleeping position. The data to support this recommendation
ranged from fewer occurrences of diaper rash to reports of
lower behavioral and physiological arousal, more sleep
time, and less crying time in the prone position.5 However,
in the late 1980s, retrospective examination of data from
various countries indicated that SIDS infants were much
more likely to be found in the prone sleeping position.6 This
prompted medical communities to advocate a non-prone
sleep position for healthy infants. By 1991, the
Netherlands, Norway, Australia, New Zealand, and the
United Kingdom had joined the worldwide trend of discouraging prone sleeping in babies under one year of age.
In each country, these recommendations were followed by
Accepted for publication February, 1998
Address correspondence and reprint requests to Michael M. Myers, PhD, Unit
40, New York State Psychiatric Institute, 722 West 168th Street, New York, NY
10032
SLEEP, Vol. 21, No. 4, 1998
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Sleeping position and sleep states in premature infants—Myers et al
diet on the rate and composition of weight gain, and on cardiorespiratory and neuroelectric activity. All infants had
normal neurological examinations as well as normal cerebral ultrasound studies. The gestational ages of these
infants ranged from 28 to 33 weeks, and birth weights from
1000 to 1600 g. At the time of study, their post-conceptional ages ranged from 31 to 36 weeks and postnatal ages
from 2 to 6 weeks. Each infant had at least 150 minutes of
sleep/wake state data after each of two consecutive feedings. Recordings of their states began within 10 minutes
after these feedings.
At the time of study, the 23 infants weighed between
1328 and 2311 g. They were all growing appropriately and
exhibited no active medical problems. All babies were on
full enteral feeds of 180 cal/day/kg. They were fed one of
five formulas that contained a fixed level of protein but differed in fat-to-carbohydrate ratios.
Infants were enrolled in this study after we obtained
written consent from their parents. The studies were performed in the Human Infant Physiology Laboratory at
Columbia Presbyterian Medical Center, NY. Infants were
brought to the laboratory, which is adjacent to the nursery,
at approximately 07:30 and electrodes for recording
impedance respiration, electrocardiogram, electroencephalogram, and body temperature were attached. They
were then placed in a radiantly warmed, clear-plastic incubator in which ambient temperature was monitored, and
were maintained under thermoneutral conditions. Subjects
were observed for approximately 6 consecutive hours by
one of three investigators, who coded behavioral state once
each minute. Studies began following an 08:00 feeding
and continued until the 14:00 feeding. The studies were
interrupted for 10 to 20 minutes for the 11:00 feeding, during which time no behavioral state assignments were made.
Otherwise the infants were left undisturbed during the
intrafeed intervals. The starting sleeping position was randomly assigned (10 supine, 13 prone). After the 11:00
feeding, position was reversed.
reports demonstrating sharp decreases in the incidence of
SIDS.7-11 In 1992, after review by the National Institute of
Child Health and Human Development of the international
evidence, the American Academy of Pediatrics (AAP) recommended that healthy term infants be put to sleep on their
sides or backs.12 Within 6 months of publication of the
AAP sleep position guideline, there was a 12% drop in incidence of SIDS in the US, even though the percentage of
infants sleeping on their sides or supine had not reached the
75% to 90% levels reported in other countries.13
Although statistics from many countries confirmed a
correlation between prone sleep positioning and increased
incidence of SIDS,6,14 it remains unclear why prone sleeping has such a profound effect. One possible factor is the
influence of sleeping position on sleep-state organization.
Babies who succumb to SIDS do so in their sleep, and most
deaths occur in the morning.15 Although no information is
available regarding the actual sleep state in which SIDS
deaths occur, abnormal state regulation has long been suspected to be a possible risk factor for SIDS.16-18
Accordingly, the mechanisms that control sleep and factors
that influence sleep organization remain areas of key interest to SIDS researchers.
In prior studies of prematurely born infants,19 full-term
neonates,5,20,21 and older infants,22 it was found that in the
prone sleeping position, babies spend less time awake and
more time in quiet sleep. This suggests the hypothesis that
the risk of prone sleeping may be mediated by changes in
state distribution. However, sleep states can be affected by
many other factors. Relevant to this current study, Harper
and colleagues noted that in normal infants born at term
and studied repeatedly from 1 week to 6 months of age, the
sequence and cyclicity of active or rapid-eye-movement
(REM) sleep followed by quiet or non-rapid eye movement
(NREM) sleep was more predictable following feedings
than following non-feeding periods of wakefulness. Based
on these findings, it was suggested that feeding serves to
reset the mechanisms that regulate the timing of sleep-state
cycles.23
Taken together, these studies suggest that investigating
the effects of prone sleeping in combination with the
effects of feeding could provide new insights into the
understanding of SIDS. Our working hypothesis was that
sleep-state distribution would be altered by sleeping position as in prior studies, but that these effects would differ
with time after feeding.
State Coding
Sleep-state coding began within 10 minutes of the
completion of the 08:00 feeding, continued until the 11:00
feeding, resumed after the completion of this feeding, and
terminated prior to the 14:00 feeding. Behavioral codes
were assigned each minute according to a previously validated coding system.24 Briefly, active sleep (AS) was
coded whenever at least one rapid eye movement was
observed during the minute, and quiet sleep (QS) was
coded when the infant was asleep without rapid eye movements. In addition, QS coding required that the infant
appear “rag-doll” floppy and with few or no movements
apart from brief generalized startles. There was also an
indeterminate state (IND), in which small body movements
Methods
Patient Population and Testing Procedures
Twenty-three preterm infants (9 males, 14 females)
were subjects for this experiment. These infants were
enrolled in an ongoing prospective study of the effects of
SLEEP, Vol. 21, No. 4, 1998
344
Sleeping position and sleep states in premature infants—Myers et al
were more common, but in which there were no rapid-eye
movements. Codes were also assigned for minutes in
which the infant appeared to be awake (AW) and when they
were crying or fussing (CRY). The behavior of the infant
was observed continuously while the study was in progress,
and minute-by-minute codes were logged to the patient
record.
The number of minutes of each state was summed over
the entire study period, within each of the two interfeed
intervals, and for the five half-hour periods within each
interfeed interval. In addition, the minute-by-minute codes
were subjected to a second analysis after applying a
smoothing algorithm. The rules for this 3-minute window
approach to behavioral state coding were similar, though
were not identical, to those used by Prechtl.25 They were as
follows:
(1) AW and CRY were collapsed into a single AW state.
(2) Starting at the beginning of the record (ie, at minute 10
after feeding), each minute was recoded as unscorable until
3 consecutive minutes of QS, AS, or AW were encountered.
(3) QS, AS, or AW codes were maintained as long the
ongoing state did not change for more than 2 minutes.
When changes in original state codes of 2 minutes or less
were encountered, these were recoded to reflect the ongoing state.
(4) When there were changes from one state to another (QS
to AS, AS to AW, etc.) and the transition occurred within 3
minutes or less, the intervening minutes (no matter what
their original code) were recoded as transitions. If changes
between states took longer than 3 minutes, the intervening
minutes were recoded as unscorable.
(5) After applying rules 1 through 4, periods between dissimilar states longer than 3 minutes (ie, too long to be a
transition), and periods between epochs of like-state longer
than 2 minutes (ie, interruptions too long to be smoothed)
were recoded as unscorable.
Several measures of state organization were extracted
from this recoding procedure. In particular, the latency
after feeding to the first epoch of QS and the duration of
this QS period were noted. In addition, for each baby and
in each sleeping position, the original state codes were
compared with the recoded states. The percent agreement
between these two codes was taken as a measure of state
stability. In other words, if a minute of QS in the original
code remained as QS in the new code, that minute was
embedded in a period of QS that lasted at least 3 minutes.
If, on the other hand, that minute changed codes, it must
have occurred either in isolation or in a period of QS that
lasted less than 3 minutes and was not part of a stable state.
Some babies (4 while in the supine position and 13 while
in the prone position) had more than one epoch of QS within the interfeed interval. For these infants, estimate of the
sleep cycle duration was taken as the number of minutes
SLEEP, Vol. 21, No. 4, 1998
from the beginning of one QS epoch to the beginning of the
next.
Data Analysis
For each baby, a total of 300 minutes of data were analyzed, 150 minutes after the completion of feeding in each
sleeping position. Each interfeed interval was divided into
five half-hour periods. The first minute in each data set
was minute 10 after feeding, and the last was minute 160
after the feeding. Thus, what is labeled as the first halfhour period after feeding is that from minute 10 to minute
40.
Statistical analyses were performed using the Systat
statistical-analysis package. All analyses included initial
sleep position as a categorical variable. To determine
effects of sleeping position on the total incidence of each
sleep/wake state, repeated-measures ANOVAs were performed. Analyses with time after feeding as an independent variable were conducted in two steps. First, for each
behavioral state, a repeated-measures ANOVA was run. In
these analyses there were two factors over which repeated
measures of state were recorded—sleeping position and
half-hour interval after feeding. When there was evidence
of a possible interaction between time and sleeping position (ie, p<.10), post-hoc paired t-tests were run to elucidate the nature of the these interactions.
Latency, duration, and stability data were analyzed
using paired t-tests. For records in which there were no
epochs of QS within the 150 minute analysis period, latency was set to 150 minutes and duration to zero.
Results
Effects of Sleeping Position on State
In the combined data set across both sleeping positions,
the distribution of minutes across sleep/wake states was
that expected for a population of prematurely born infants.
The vast majority of minutes were coded as AS (73%), followed by QS (13%), AW (6%), IND (5%), and CRY (3%)
(see Table 1). When the data were divided with regard to
sleeping position, three differences in state distribution
emerged. The two non-sleep states (AW and CRY) were
both significantly increased when babies were placed in the
supine position. In contrast, the incidence of QS was
almost doubled in the prone position.
Table 2 presents results from the analysis of states after
applying the 3-minute smoothing window described in
Methods. There were three significant effects of sleeping
position on sleep structure. First, the latency to the onset of
QS after feeding was decreased from 84.2 minutes in the
supine position to 55.5 minutes when the babies were prone
(F(1,21)=6.64, p<.02). Second, the duration of the first QS
epoch was longer when in the prone position (16.3 vs 8.3
345
Sleeping position and sleep states in premature infants—Myers et al
Table 1.—Number of minutes (mean±sd) coded as one of the five sleep/wake states. Total minutes coded was 300. Also
shown are state distributions (mean number of minutes±sd) within each sleeping position and, the mean(±sem) difference
between sleeping positions along with results (F) from repeated measures ANOVA (df=21) for each state.
State
Total Minutes
Quiet Sleep
Indeterminate
Active Sleep
Cry/Fuss
39±16
15±8
219±27
9±8
Minutes in
Prone
Supine
25±12
8±5
111±17
2±2
Table 2.—Characteristics of sleep architecture by sleeping position
using state codes derived from the application of a 3-minute
smoothing window to the original state codes. All values are
means±SEM. See text for details of how each characteristic was
derived. Results (F) from repeated measures ANOVA (df=21) for
each characteristic are also given.
Characteristic
latencya to onset of
first epoch of QS
durationa of first
epoch of QS
stabilityb of QS
stabilityb of AS
Prone
Supine
ANOVA
p
55.5+8.8
84.2+9.9
4.72
<.05
16.3+1.8
82.0+5.7
97.5+0.5
8.3+1.6
58.8+8.3
96.7+0.7
12.02
6.75
0.62
<.01
<.02
ns
ANOVA
p
11.1±2.6
0.9±1.3
3.0±4.0
-5.2±1.7
22.35
0.49
0.38
10.50
<.001
ns
ns
<.01
of AW and CRY were increased when babies were in the
supine position (AW: F(1,21)=13.84, p<.01; CRY:
F(1,21)=10.50, p<.01). In addition, the number of awakenings (AW or CRY), regardless of duration, were counted
in each sleeping position. There were more than twice as
many awakenings in the supine position as in the prone
position (7.74±1.30 vs 3.26±0.70; F(1,21)=13.46, p<.01).
A different pattern of results was seen for the two sleep
states over the five half-hour periods after feeding (see Fig.
2). For AS, there was no significant effect of sleep position; however, there was a significant effect of time after
feeding. Post hoc polynomial tests indicated that this effect
was due to a cubic trend in the data (p<.05). There was no
significant interaction between sleep position and time
after feeding on the distribution of AS. For QS, there was a
significant main effect of sleeping position with a higher
incidence of QS in the prone position (F(1,21)=22.35,
p<.001). There was also a significant interaction between
sleeping position and time after feeding (F(4,84)=3.50,
p<.02). Post-hoc tests demonstrated that this interaction
was attributed to the effects of sleeping position being significant (p<.05) only in the first, second and fifth half-hour
intervals after feeding.
Further analyses of these data indicated that the differences in QS between sleeping positions are due not only to
increases in the average duration of QS epochs (see Table
2), but also to a greater percentage of babies with extensive
amounts of QS. Specifically, in the prone position there
were many more babies with 10 or more minutes of QS in
the first, second and fifth half-hour intervals (see Fig. 3).
(a) minutes
(b) % of minutes that were unchanged after smoothing
minutes, F(1,21)=12.02, p<.01). Finally, the stability of
QS, as measured by the percentage of minutes unaffected
by state smoothing, was greater in the prone position
(82.0%) than while supine (58.8%, F(1,21)=6.71, p<.02).
In contrast, there was no significant effect of position on
the stability of AS. In the prone sleeping position, 13
infants had two epochs of QS separated by a segment of AS
within the 150 minutes of the postfeed interval. In these
records, the average (±sd) time from the beginning of the
first QS epoch to the beginning of the next was 66±32 minutes. In the supine position, only four infants had two QS
epochs within the 150 minute postfeed interval. For these
four records, the sleep cycle duration was similar to that in
the prone position (73±16 minutes).
Discussion
The working hypothesis for these studies was that in
the prone sleeping position, babies would spend less time
in awake states and more time in QS, but these effects of
prone sleeping would vary with time after feeding. The
overall effects of sleeping in the prone position were as
predicted, and there were effects of time after feeding, but
not for all states. In the prone position there were
decreased amounts of AW and CRY, and this was apparent
Effects of Time After Feeding
Figure 1 shows the incidence of AW and CRY in each
of the five half-hour intervals after feeding with respect to
the two sleeping positions. Repeated-measures ANOVA
indicate there are no significant effects of time after feeding and no significant interaction with time and position.
Consistent with the results shown in Table 1, the incidence
SLEEP, Vol. 21, No. 4, 1998
14±8
7±5
108±16
7±8
Difference
Prone-Supine
346
Sleeping position and sleep states in premature infants—Myers et al
Figure 1.—These graphs display the means of the number of minutes
of Awake (top) and Cry (bottom) that were coded in each of the first 5
half-hour intervals after feeding, for each of the two sleeping positions
(open=supine: black=prone). ANOVAs indicate there are significant
(p<.05) main effects of position on these states, both being increased
in the supine position, but no significant interaction with time after feeding.
Figure 2.—These graphs display the means of the number of minutes of
Quiet sleep (top) and Active sleep (bottom) that were coded in each of
the first 5 half-hour intervals after feeding, for each of the two sleeping
positions (open=supine: black=prone). There is no significant effect of
sleep position on AS butt here is a significant increase in QS in the prone
position over all intervals (p<.001). In addition, for QS, there is a significant interaction with time after feeding and position, with significant
(p<.05) differences during the first, second, and fifth half-hour intervals.
It is not clear why sleeping position leads to differences
in sleep architecture. It has been proposed that in the prone
position there is an increase in arousal threshold to both
internal and external stimuli.5,26 This is supported by a
recent study in which it was found that heart-rate responses of infants to auditory stimulation are decreased in the
prone position.27 Thus, it may be that in the prone sleeping
position, sleep is deeper and the threshold to move from
sleep to states of wakefulness is increased. Increases in
arousal threshold in the prone sleeping position may not
only decrease the likelihood that infants awaken, but also
might promote longer periods of QS. On the other hand,
awakenings are more likely to be followed by AS than
QS.23 Thus, increases in awakenings in the supine position
could indirectly lead to decreases in the amount of QS.
Consistent with this hypothesis, we found an increase
in the number of arousals in the supine position. This
might be due to a decreased arousal threshold linked to factors such as a lower body temperature in the supine position. Alternatively, increases in the number of arousals
might be caused by an increase in physiological events that
promote arousal, such as gastroesophageal reflux.28
However, differences in QS were seen only toward the
beginning and end of the interfeed interval, yet changes in
the amount of time awake due to sleeping position were
seen throughout the interfeed interval. Moreover, there
was no significant change in the amount of AS as a function of sleeping position. This pattern of results suggests
Figure 3.—This figure shows the percentages of the 23 infants studied
that had 10 or more minutes of quiet sleep within each of the half-hour
intervals after feeding. Solid squares are results when the infants were
sleeping in the prone position, solid circles are data obtained when the
infants were in the supine position. The state data were those from the
3-minute smoothing of the original minute-by-minute coding (see
Methods for details).
throughout the interfeed interval. These findings are in
agreement with several prior studies.5,19-22 Also consistent
with this prior work, we found there were increases in QS
in the prone position; however, this effect was significant
only at the beginning and end of the interfeed interval. The
increases in QS in the prone position were attributable to a
greater percentage of babies spending longer times in QS.
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Sleeping position and sleep states in premature infants—Myers et al
that although arousals are more frequent in the supine position, the decreases in QS in the supine sleeping position are
not necessarily a secondary effect of changes in arousal.
Harper and colleagues have proposed that feeding
serves as a stimulus for entraining sleep cycles of infants.23
Their data, obtained from infants during the first 6 months
of life, show a peak probability of QS at about 45 minutes
post-feeding with a second peak about 1 hour later. In our
study, the mean latency to the onset of the first epoch of QS
after feeding was about 55 minutes (see Table 2). In most
of our recordings there was only one epoch of QS during
the 150 minutes postfeed. However, in 17 of these records
(4 in the supine position, and 13 in the prone position), two
epochs of QS occurred. Similar to the findings of Harper
et al,23 in these 17 records the average time from the beginning of the first epoch of QS to the beginning of the second
was 68 minutes. From these results, we would expect to
find two peaks in the incidence of QS during the interfeed
interval, one within the second half-hour after feeding, and
one near the end of the interfeed interval. This pattern of
QS distribution was observed when infants were in the
prone position, but not when supine (see Figs. 2 and 3).
Thus, another possible contribution of sleeping position to
changes in the distribution of QS is that the effects of feeding on resetting the sleep cycle are much less effective
when infants are supine.
Prone sleeping changes not only state distribution, but
fundamental aspects of physiologic function as well. In the
prone position, babies have lower metabolic activity,19 yet
they have higher heart rates.20,21,29,30 Premature infants also
have decreased heart-rate variability, increased respiratory
rates, and lower respiratory rate variability in the prone
position.30 Many of these same physiologic variables
exhibit systematic changes with time after feeding. Abrupt
increases in circulating levels of nutrients, metabolites, and
humoral mediators of anabolic activity occur during the
post-absorptive period. The physiologic correlates of these
anabolic processes include increases in energy, body temperature, heart rate, and respiratory rate.31 There is also evidence that neuroelectric activity and states of sleep are systematically altered by diet.32 Given the pervasive changes
related to the prandial cycle, it is not surprising that time
after feeding interacts with body position in regulating
sleep architecture. However, how these interactions influence vulnerability to SIDS remains largely conjectural.
Perhaps periods of decreased metabolic activity and heart
rate that occur later in the feeding cycle represent a time of
increased risk. Alternatively, it may be that the high
metabolic and autonomic activity following feeding create
a mismatch between the physiologic states associated with
sleep and nutrient processing.
What do these data contribute to our understanding of
the possible mechanisms that underlie the heightened risk
SLEEP, Vol. 21, No. 4, 1998
of SIDS in the prone position? As noted by Gould et al,17
the sleep state in which the cascade of events that leads to
death is initiated is not known. It may be that REM presents the more vulnerable state because of phasic autonomic activity, alterations in thermoregulation, or irregularity
of respiratory control. Alternatively, QS may be the more
vulnerable state because of higher arousal thresholds. Our
results lend indirect support for the hypothesis that QS represents a greater risk, since sleeping in the prone position
increases both the amount of QS and the incidence of
SIDS.
Prone sleeping may confer an immediate risk for SIDS
through acute changes in cardiorespiratory physiology,
sleep state organization, and/or effects of rebreathing.
However, a history of having slept in the prone position
may also be of importance. Chronic prone sleeping may
place demands on key physiological systems that lead to
alterations in the developmental course of these systems.
These alterations may be of little consequence to the vast
majority of infants. However, in some these, changes in
maturation may amplify weaknesses initiated by other factors—such as adverse conditions during fetal life—and
thereby confer an increased risk for SIDS.
Vital statistics from several countries strongly suggest
that changing from the prone to the supine sleeping position has had an enormous impact on the incidence of
SIDS.9,14 Thus, investigation of the effects of prone sleeping may afford new clues about the mechanisms that underlie these deaths. Studying these effects in groups that differ in vulnerability to SIDS is also key. This current investigation focused on the responses of prematurely born
infants to changes in sleep position. Comparing these
results with those obtained from term infants who are at
less risk, as well as with infants at increased risk for other
reasons (eg, exposure to effects of maternal smoking),
would be informative. It is also important to note that our
studies were conducted during the daytime. Since most
SIDS deaths occur at night, in particular during the early
morning hours, it should be determined whether the effects
of sleeping position are dependent upon time of day. It
would also be of interest to determine whether the sidesleeping position has an intermediate effect on sleep organization, since side-sleeping also confers risk for SIDS,
although to a lesser degree than that for the prone position.33 Finally, in order to better link the results of such
studies to SIDS, they should be conducted at a later stage
of development. The physiological responses of prematurely born infants during their stay in the hospital may not
provide the most relevant set of data. Repeating this study
in infants born premature and those born at term when they
reach 2 to 4 months term-adjusted age would be informative, because diurnal rhythms are more mature and this is
the age of greatest vulnerability.
348
Sleeping position and sleep states in premature infants—Myers et al
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18. Thoman EB, Denenberg VH, Sievel J, Zeidner LP, Becker P. State
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ACKNOWLEDGMENTS
This work was supported by Public Health Service
grants HD13063, HD32774, HD27564, and a clinical
research center grant RR00645. We also wish to acknowledge the contributions of Ms. Vivian Reidy at the Bronx
High School of Science. This study was undertaken in partial fulfillment of Liza Schaeffer’s senior research thesis,
and Ms. Reidy was instrumental in promoting this effort.
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