[B] DiPietro JA, Costigan KA, Pressman EK. Fetal state concordance predicts infant state regulation. Early Hum Dev. 2002 68:1-13.

Early Human Development 68 (2002) 1 – 13
www.elsevier.com/locate/earlhumdev
Fetal state concordance predicts infant
state regulation
Janet A. DiPietro a,*, Kathleen A. Costigan b, Eva K. Pressman c
a
Department of Population and Family Health Sciences, Johns Hopkins University, 624 N. Broadway,
Room 280, Baltimore, MD 21205, USA
b
Division of Maternal-Fetal Medicine, Johns Hopkins Medical Institutions, Baltimore, MD, USA
c
Department of Obstetrics and Gynecology, University of Rochester, Rochester, NY, USA
Received 29 July 2001; received in revised form 13 November 2001; accepted 2 January 2002
Abstract
Fetal state organization reflects the development of the central nervous system but may also portend
individual differences in postnatal state organization. The goal of the present study was to determine
the extent to which fetal state regulation, defined as the percentage of an observation period in which
fetal heart rate and movement concordance was displayed, is associated with neonatal state regulation.
Neonatal state regulation was evaluated through a standard neurobehavioral assessment at 2 weeks
postpartum. Biobehavioral concordance was measured in 52 normally developing fetuses at 24, 30 and
36 weeks gestation using an actocardiograph; the neonatal assessment was administered to 41 of these
as infants. Intrafetal stability in biobehavioral concordance did not emerge prior to 36 weeks. Fetuses
with higher concordance at 36 weeks were infants that displayed better state regulation during the
exam, including more alertness and orientation (r(35) = 0.29), less cost of maintaining attention
(r = 0.36), less irritability (r = 0.41), better regulatory capacity (r = 0.47), a greater range of available
states (r = 0.34), and were significantly more likely to maintain control during the most aversive
portions of the exam F(1,31) = 4.63, p < 0.05). These results support fetal state as a stable individual
attribute that is conserved across the prenatal and neonatal periods. D 2002 Elsevier Science Ireland
Ltd. All rights reserved.
Keywords: Fetal state concordance; Infant state regulation; Central nervous system
1. Fetal state concordance predicts infant state regulation
The postconceptional age at which birth normally occurs does not represent a
significant transition in neurobehavioral development [1,2]. An underlying assumption
*
Corresponding author. Tel.: +1-410-955-8536; fax: +1-410-614-0799.
E-mail address: [email protected] (J.A. DiPietro).
0378-3782/02/$ - see front matter D 2002 Elsevier Science Ireland Ltd. All rights reserved.
PII: S 0 3 7 8 - 3 7 8 2 ( 0 2 ) 0 0 0 0 6 - 3
2
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
for both fetal and infant neurobehavioral assessment is that stable individual differences
emerge early in development, and that early functioning predicts generalized or specific
aspects of subsequent development. Studies that attempt to evaluate prenatal to postnatal
consistencies in behavioral functioning within individuals using objective measures of
behavior are scarce. Individual stability from the fetus to infant has been demonstrated for
heart rate through the first year of life [3] and motor activity during active sleep from term
through the early postnatal period [4,5].
One of the hallmarks of development before birth is the coalescence of patterns of fetal
behavioral and cardiac function into behavioral states, which is widely viewed as
reflective of the developing integration of the central nervous system [6]. As the fetus
matures, state parameters (i.e., fetal heart rate, body movements, and eye movements)
gradually begin to cycle together and mature into patterns of coincidence accompanied by
predictable state transitions. Behavioral states are present late in the second trimester, but
coincidence among fetal heart rate, body, and eye movements is infrequent and there are
less well-defined transitions [7,8]. The lack of state coincidence early in gestation is
believed to reflect immaturity in the neural substrate required for integration of state
parameters prior to 36 weeks gestation [9] and prolonged periods without coincidence at
term has been interpreted as indicative of disruption of centrally mediated control
mechanisms [10].
Four fetal behavioral states have been identified in concert with state scoring methods
developed for neonates. Although not isomorphic with newborn states, these approximate
quiet sleep (1F), REM sleep (2F), quiet waking (3F) and active waking (4F), respectively.
Characteristics of electroencephalographic (EEG) activity associated with sleep states in
infants have been documented in baboon fetuses [11]. Analogous studies have not been
conducted in human fetuses, although there is evidence that the heart rate and behavioral
manifestations of 1F, 2F, and 4F in the fetus are comparable to those observed in newborn
infants [12 – 14].
There is wide interfetal variability in the percentage of observation time during which
coincidence of state parameters are exhibited [15]. Nonetheless, within-fetal stability in
fetal state organization has been observed in healthy fetuses between 38 and 40 weeks
gestation [12] and from 36 to 38 weeks gestation [16], supporting the position that aspects
of fetal state index stable individual attributes. To date, two studies have examined
associations between fetal state coincidence and postnatal function. Using the same
methods to characterize fetal state at term and infant state at 2 weeks postpartum, Groome
et al. [12] detected a significant correlation between the duration of quiet sleep from the
fetal to neonatal period; other state-specific correlations were positive but did not attain
significance, perhaps due to limited study power. The other examined the relation between
the percentage of time 36-week fetuses exhibited concordance between fetal heart rate and
movement and maternal reports of later infant temperament. Higher concordance during
the fetal period was associated with fewer night wakings at 3 months and maternal ratings
of better temperamental adaptability at 6 months [16], suggesting that fetal state represents
a broader reflection of underlying regulatory processes. Regulatory control of both arousal
and attention is a core construct in theories of temperament [17] and commonly regarded
as the cornerstone of development during the first few years of life. For neonates and
infants, this translates into the ability to minimize irritable responding to discomfort or
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
3
stimulation, self-soothe or be consoled once crying has begun, demonstrate regularity in
sleep – wake cycles, and maintain an alert, focused state despite competing demands.
Based on the hypothesis that fetal state organization reflects individual differences in
developing state control, the goal of the present study was to evaluate the relation between
fetal and neonatal state regulation. We expected that fetuses who display a higher
frequency of mature patterns of state concordance would become neonates who exhibit
higher levels of state control. Fetal state regulation was defined as the period of time
during which concordance among fetal heart rate and movement patterns was exhibited,
using existing classification strategies; neonatal regulation was ascertained in relation to a
neurobehavioral assessment designed to evaluate state lability and control.
2. Methods
2.1. Participants
Participants were 52 non-smoking women with singleton pregnancies and their
offspring. Inclusion criteria included low risk, uncomplicated pregnancies with strict
gestational age dating criteria. Participants did not use either illicit substances or
therapeutic medications with potential fetal effects. Demographic and medical data were
collected by interview and medical chart review. All infants included in this analysis were
delivered at term and discharged from the regular newborn nursery according to routine
schedules. Maternal and infant characteristics are presented in Table 1. Although there was
range in demographic characteristics, the sample consisted of primarily healthy, welleducated, and employed women. Forty-one neonates (79%) returned for testing at 2 weeks
postnatal age. There were no significant differences in family demographic (e.g., maternal
education), neonatal (e.g., birthweight), or fetal state measures at any gestational age
between tested and untested (n = 11) individuals. This research project was approved by
the Joint Committee on Clinical Investigation, and pregnant women provided informed
consent for themselves and infants.
Table 1
Maternal and infant characteristics
Antenatal
M
N
Maternal age
Maternal education (year)
First prenatal visit (GA)
Gestational age at delivery (weeks)
Infant birth weight (g)
5-min Apgar
% Boys
% Primiparous
52
29.9
16.3
7.8
39.6
3502
8.9
60
64
Neonatal
SD
3.5
2.6
2.0
1.1
470
0.5
M
41
29.9
16.4
7.9
39.6
3525
8.9
56
66
SD
3.3
2.6
2.1
1.1
454
0.6
4
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
2.2. Fetus
Data were collected at 24, 30, and 36 weeks gestational age. To control for potential
diurnal and prandial effects, women were tested at the same time each visit, either at 1:00
or 3:00 pm. Women were instructed to eat 1.5 h prior to testing, but not again before
testing. Participants were monitored for 50 min in a left lateral recumbent position while
resting quietly. Data for all 52 fetuses are available at each gestational age.
2.3. Fetal data collection
Fetal heart rate (FHR) and movement (FM) data were collected from a fetal
actocardiotocograph (Toitu, MT320; Tokyo, Japan) using a single wide array Doppler
transducer positioned on the maternal abdomen with an elastic belt. Standard fetal
cardiotocography is based on Doppler detection of the high frequency fetal heart motions.
Lower frequency signals, produced by maternal and fetal body activity, are typically
filtered out as noise and discarded. Instead of discarding these signals, the actograph
bandpasses both the highest frequency (i.e., FHR) and the lowest frequency signals (i.e.,
maternal movement and respiration). Actograph signals are generated by a change in the
returned Doppler waveform; if there is no movement, the returned signal will retain the
same frequency as the emitted signal. If the fetus is moving, the echo will be returned at a
different frequency which is commensurate with the velocity with which the fetal body
part moves towards or away from the transducer. The validity of this particular monitor to
accurately detect ultrasound-visualized movements has been well-documented, ranging
from 91% to 95% of all fetal movements whether agreement is based on time intervals or
individual movements, and is equally reliable in detecting periods of quiescence [18 – 20].
Most movements undetected by the actograph are small, isolated movements of extremities; virtually all (97 –98%) trunk and sustained ( > 1 s) movements are detected.
Fetal state concordance was based on visually coded fetal heart rate and movement
patterns from the polygraphic tracings generated by the actocardiograph, coded in 3-min
windows. Fetal heart rate patterns were scored in accord with existing protocols [21]
which classify FHR into four patterns of variability, including little or no variability
(FHRP A), moderate variability with episodic accelerations (FHRP B), a rhythmic
oscillatory pattern within a wider bandwidth than as in A (FHRP C), and high variability
during which accelerations may be fused into tachycardia (FHRP D). Actograph-detected
movements were scored using four categories designed to be comparable to those used for
state determination when data are collected through ultrasound visualization. Categories
included no movement or a single, brief, instance of isolated activity (FM 1); mostly
inactive, with sporadic gross movements (FM 2); frequent activity of moderate amplitude
and duration (FM 3); and continuous, high amplitude movement (FM 4). Inter-rater
reliability was achieved by dual independent coding of each polygraphic tracing for the
first 10 fetuses until training criteria (95% agreement or better for heart rate and
movement) were achieved. During coding, reliability was maintained by sampling one
record from each of the remaining cases, stratified by gestational age. On-going inter-rater
agreement was based on these 42 cases, computed incrementally as coding proceeded. The
final FHR pattern data agreement was 98% exact matching of score, Kappa = 0.90% and
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
5
94.5% exact, Kappa = 0.87% for FM patterns. Two coders scored each tracing; disputes
were resolved through consensus.
Four biobehavioral patterns (BBP) were classified based on the following definitions:
FHRP A with FM 1 = BBP A; FHRP B with FM 1, 2, or 3 = BBP B; FHRP C with FM
1 = BBP C; and FHRP D with FM 3 or 4 = BBP D. The percentage of time a fetus displayed
each pattern was calculated, and summed to represent the cumulative percentage of time in
which any biobehavioral pattern was evident. Because we lack eye movement data in
making these classifications, we refer to this measure as fetal biobehavioral concordance,
rather than fetal state. An example of each biobehavioral pattern is presented in Fig. 1.
2.4. Neonate
Infant data collection was conducted in the morning, between anticipated feedings.
Mean age at testing was 14.2 days postpartum (SD = 1.9, range = 9 –18 days). A standard
neurobehavioral assessment, the Neonatal Assessment of the Preterm Infant (NAPI;
Psychological) was administered. This scale was selected because of the rigorous
psychometric testing undertaken for scale development, and its emphasis on sampling
behavioral state [22]. Although the scale was developed for use with preterm infants after
31 weeks postconceptional age, it contains many items that overlap with scales used with
full-term infants due to the relatively limited behavioral repetoire of the newborn.
Moreover, the continuity in neurological functioning that exists from late gestation
through term and beyond provide a solid conceptual basis for its implementation with
full term infants [1] which is becoming more common [23,24].
The exam proceeds in an invariant sequence of manipulations and observations,
beginning with a series of aversive maneuvers to evaluate motor development and tone.
Following this first half of the exam, the infant is brought to a quiet, alert state in order to
evaluate visual and auditory orientation to a series of stimuli. Behavioral state is recorded
at exam onset and 13 points during the exam after the following: undress/position supine,
head in midline; scarf sign; remove diaper; leg recoil; forearm recoil; popliteal angle;
ventral suspension and placement; rediaper; redress; swaddle; orientation assessment;
return to rest; final minute observation. State scoring is based on standard practices and
definitions, including quiet sleep (1), active sleep (2), drowsy (3), quiet alert (4), active
awake (5), and crying (6). A total of 71 items are scored; 22 of these are used to derive 7 a
priori cluster scores. Raw scores are converted to standardized scores before compositing.
The first three clusters are comprised of neuromuscular and motor functioning: Popliteal
Angle; Scarf Sign; and Motor Development. The remaining concern state organization and
control: Cry Quality; Percent Asleep; Alertness and Orientation which is the degree to
which an infant can track vsual and auditory stimuli while maintaining an effortful, alert
state; and Irritability, which measures the extent to which an infant cried during the exam.
The NAPI variables are scored as the exam proceeds and yields objective and specific
scores for infant performance. However, more global scores of the infant’s overall reaction
to the exam as well as their qualties as an interactive partner are also useful. For this,
supplementary items from the Neonatal Behavioral Assessment Scale (NBAS) [25], which
assess the infant’s ability to maintain control in response to the challenges of being
examined, were also scored. This feature of the NBAS does not require any additional
6
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
Fig. 1. Examples of fetal heart rate and movement data used in coding periods of biobehavioral concordance. Note that for clarity of presentation, figures represent
digitized data; actual scoring was based on raw polygraphic data. Reprinted with permission of the Guilford Press.
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
7
maneuvers and examiners rate infants following completion of the exam. The items
selected pertain specifically to the ability of the infant to control state and include: Quality
of attention, referring to the intensity of alert responsiveness; Cost of attention, the degree
to which maintaining an alert state taxes the infant; Regulatory Capacity, the ability to
maintain control even during aversive maneuvers; and State Range, which reflects the
breadth of organized states available to the infant. Higher scores indicate ‘‘better’’
performance or control. All testing was done by a single examiner, unaware of fetal
values, who was certified on scale administration shortly before the study began and had
been previously certified on the NBAS. Certification on each is an intensive process
involving attainment of reliability in administration and scoring with a scale trainer.
2.5. Data analysis plan
Because of the small sample size and relatively explicit hypothesis, data analysis
techniques were kept simple. Potential changes in biobehavioral concordance during
gestation were evaluated using repeated measures analysis of variance. Pearson correlation
coefficients were computed to examine intrafetal stability in concordance among the three
gestational ages, as well as to address the primary study goal regarding the association
between prenatal and postnatal state regulation. Fetuses were then stratified into groups
that exhibited either low or high levels of biobehavioral concordance and repeated
measures analysis of variance was used to determine whether the pattern of infant state
control during the course of the neonatal assessment differed between groups. The
comparability of tested and untested infants, as well as the influence of infant feeding
on neonatal performance, were evaluated using t-tests.
3. Results
3.1. Fetal state development
The amount of time a fetus displayed biobehavioral concordance was 62.1% (SD =
45.9%), 94.0% (SD = 12.1), and 89.6% (SD = 13.8) at 24, 30, and 36 weeks. Results of
repeated measures analysis of variance reveal a significant effect for time ( F(2,102) = 18.72,
p < 0.001); post hoc contrasts indicate this effect is attributed to the change from 24 to 30
weeks; no change was detected from 30 to 36 weeks. The correlations between biobehavioral concordance at each gestational age were not significant (24 – 30 weeks: r = 0.09;
24 –36 weeks: r = 0.02; 30 –36 weeks r = 0.21). At each gestational age, BBP B comprised
the bulk of the observation time: (60.3%, 87.2%, 82.4% at 24, 30, and 36 weeks
respectively), followed by BBP D (1.3%, 6.5%, 12.2%), and BBP A (2.2%, 2.7%, 5.4%).
BBP C was exhibited too infrequently to compute mean incidence.
3.2. Neonatal assessment
Two of the NAPI clusters were not normally distributed (Cry Quality and Percent
Asleep) and were not further analyzed. The normal distribution of the remaining clusters
8
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
confirms the suitability of this scale for use with full-term infants. Means for the remaining
NAPI cluster scores, supplementary items, and averaged state rating values are presented
in Table 2. Most infants began the assessment in an active sleep, drowsy, or quiet awake
state (92.6%). Cluster scores are based on conversions of raw scores into standard scores;
supplementary items can range from 1 to 9 (low to high). There were no significant
differences between participants who were tested as neonates and those who were not on
either fetal state biobehavioral concordance at any gestational age or demographic
variables listed in Table 1. Thirty-one infants were exclusively breast-fed, four were
primarily breast fed but supplemented with formula, and six were exclusively formula fed.
Because feeding method can have pervasive effects on levels of arousal during neonatal
testing and through early infancy [26,27], the latter group was excluded from the analysis.
Consistent with prior reports, the breast-fed group were less alert (t(14; based on unequal
variances) = 1.97, p = 0.07) than the formula fed infants, spent nearly twice as much time
crying (26% vs. 15%) and half the amount of time asleep (9.5% vs. 5.5%). Further,
repeated state ratings during the course of the assessment revealed a significant interaction
in states of breast and formula-fed infants over time ( F(13,494) = 3.43, p < 0.0001), with
breast-fed infants becoming increasingly more aroused, and bottle fed infants becoming
less so. There were no differences between the groups on prenatal state measures; thus the
decision to exclude the bottle fed group was to control for a confounding influence on
postnatal state that is both conceptually and empirically unrelated to fetal state.
There were no significant correlations between either 24 and 30 week fetal biobehavioral concordance and infant NAPI measures. There was significant prenatal to postnatal
consistency beginning at 36 weeks gestation for the clusters related to state regulation but
not those measuring neuromuscular and motor development; these results and p-values
(two-tailed) are presented in Table 3. Higher biobehavioral concordance at 36 weeks was
marginally associated with better orientation performance and significantly associated with
fewer negative effects of maintaining an alert state (Cost of Attention), less irritability,
better regulatory capacity, and a broader range of available states.
The 14 individual state values were averaged over the course of the exam. Two infants
did not have complete state data at all 14 points so are excluded from this analysis. The
Table 2
NAPI cluster scores and supplemental NBAS item ratings used in data analysis
NAPI Clusters
Scarf Sign
Popliteal Angle
Motor Development
Alertness and Orientation
Irritability
NBAS Supplementary ratings
Quality of Alertness
Cost of attention
Regulatory capacity
State range
NAPI state values
M
SD
70.3
66.3
69.5
61.2
49.8
25.4
15.4
16.6
21.1
22.6
6.3
6.1
6.3
7.2
4.5
1.7
1.6
1.7
1.3
0.7
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
9
Table 3
Correlations between fetal biobehavioral concordance and neonatal state measures (n = 35)
r
p-Value
NAPI clusters
Scarf sign
Popliteal angle
Motor development
Alertness and orientation
Irritability
0.23
0.18
0.13
0.29
0.41
n.s.
n.s.
n.s.
0.09a
0.01
NBAS supplementary ratings
Quality of attention
Cost of attention
Regulatory capacity
State range
0.23
0.36
0.47
0.34
n.s.
0.04
0.005
0.05
a
One-tailed probability test, p < 0.05.
correlation between mean state level and 36 week fetal biobehavioral concordance was
r = 0.34, p < 0.05). In order to capture the nature of infant state response over the course
of the neonatal exam, mean state values for each period in which fetal state was sampled
(see Methods) were computed and plotted in Fig. 2. Over time, infants displayed
increasingly higher levels of state to the aversive procedures (Time 2 through 7), followed
by a lessening of arousal once placed prone (Time 8), which is maintained through
Fig. 2. Infant state values during neonatal neurobehavioral exam plotted for all participants and by low and high
fetal state concordance at 36 weeks gestation.
10
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
redressing, orientation, and the conclusion of the assessment (14). To examine the relations
between fetal state and this trajectory, fetuses were categorized into two levels of
biobehavioral concordance: those that showed evidence of organization 90– 100% of the
observation time (n = 19, range 0.94 – 1.00) vs. those that showed less (n = 14,
range = 0.47– 0.88). Repeated measures analysis of variance by biobehavioral concordance
(high vs. low) indicated a significant time effect over the course of the exam
( F(13,403) = 17.92, p < 0.001), but the overall F for fetal concordance did not attain
significance. However, examination of the data in Fig. 2 indicates convergence in state
measures at Time 8, corresponding to the point at which the aversive procedures are
completed. Separate repeated measures analysis of variance were conducted for the seven
time periods prior to this point (1 through 7) and those afterwards (8 through 14). Analyses
indicated a significant main effect for fetal biobehavioral concordance during the first
( F(1,31) = 4.63, p < 0.05) but not the latter ( F(1,31) = 0.48) part of the exam.
4. Discussion
The results of this study support the position that fetal biobehavioral concordance reflects
a stable individual attribute related to state regulation, that is conserved across the prenatal
and neonatal periods. No evidence of intrafetal stability in the percentage of coincidence
prior to 36 weeks was found, replicating an earlier report using the same methodology on a
different sample [16]. However, our earlier study did discern stability during gestation from
36 weeks on [16] as has another [28], indicating that fetal state becomes a stable
characteristic only once mature states emerge. As such, the lack of predictive validity of
fetal state organization prior to 36 weeks for neonatal state outcomes confirms the on-going
nature of the developmental process of state maturation until close to term.
Higher levels of concordance during the fetal period were associated with lower levels
of irritability and better state regulation during the infant exam in general, and during the
aversive handling procedures in particular. Associations between fetal biobehavioral
concordance and neonatal attentional processes were less robust than those associated
with irritability and state regulation, but evidenced some associations, suggesting that the
modulation of arousal necessary to process environmental stimuli is also related to the
processes underlying fetal state development. Although existing studies have identified
similiarities in fetal and infant state topography by measuring state parameters during
different developmental periods [12 – 14], this is only the second study to utilize an
individual differences approach to determine the extent to which fetal state is associated
with objective measures of infant state within individuals. The first [12] examined this
question within a narrow sleep focus; that is, whether the amount of time fetuses spent in
periods of active or quiet sleep was similar to neonatal sleep patterns. By and large it was
not, although a specific attribute of sleep (duration of quiet sleep epochs) did show
consistency. The current study goes beyond examining similarities in specific sleep states
to regard fetal state organization as an early indicator of an individual’s regulatory control
processes. Thus, it is the first to document that, within individuals, higher levels of
biobehavioral concordance during the late fetal period is associated with a broad array of
state regulatory capacities during the second week of life. This includes less irritability,
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
11
better regulatory control, a broader range of available states, less strain on the infant’s
regulatory system during periods of attention, and a trend towards better visual and
tracking performance, as mediated by the ability to maintain an alert state. In particular,
greater biobehavioral organization during the fetal period was associated with heightened
state regulations during periods of the neonatal assessment that are most likely to elicit
irritable responses.
In contrast, items which measured neuromuscular maturity (popliteal angle and scarf
sign) and motor development were not significantly related to fetal biobehavioral
concordance. This was expected based on our existing hypothesis, but raises questions
concerning the broader implications of fetal state. Because fetal state develops in
predictable ways and is affected by conditions that threaten neurological status (e.g.,
growth retardation), fetal state organziation is regarded as a reflection of the developing
nervous system and neural integrity [6,10]. The results of the current study suggest another
role of fetal state organization; as a pecursor of regulatory control, an attribute that is a core
temperament dimension. These two intepretations are not mutually exclusive. Individual
differences in regulation have neurophysiologic correspondence throughout the nervous
system [29]. However, after birth, motor maturation and regulatory processes are distinct
and unrelated constructs; thus a unitary notion of fetal state as an indicator of overall
neural integrity or maturation may be difficult to support. The developmental trajectory of
the inhibitory processes of the parasympathetic nervous system in particular, which
accelerates over the course of gestation, has been suggested to modulate the integration
between heart rate variability and movement [30]. In infants, individual differences in
parasympathetic innervation are commonly acknowledged as sources of behavioral and
emotional regulatory capacities [31]. Thus, the continuity observed in the transition from
fetus to newborn with respect to state processes may reflect stable attributes of parasympathetic control within individuals and one would expect predictive validity to extend
beyond the neonatal period.
Although we were limited in our identification of fetal concordance patterns to only
heart rate and movement, we believe our 36-week results can be discussed in the broader
context of fetal state for several reasons. First, at 36 weeks, we detected non-concordance
between parameters about 11% of the observation time, which is mid-range of the values
reported by others, e.g., [10,14,32,33]. Second, strong associations between periods of
high FHR variability (patterns B and D) and the presence of eye movements and the lack
of eye movements during low variability (pattern A) have been noted as the fetus nears
term. Discordance between eye movements and FHR variability occurs only 12.5% of the
time [34] and eye movements are present less than 2% of the time during FHR pattern A
[9]. Coincidence between FHR, body and eye movements in normal term fetuses has been
described as so high that FHR monitoring alone is a sufficient indicator of state [35].
However, because the FHR pattern and movement criteria are the least specific and most
common for 2F, actograph data alone has been found to be accurate in identifying 1F and
4F [36], but indeterminate periods in which there are no eye movements tend to be
incorrectly attributed as 2F; thus it is likely that this explains our relatively high
concordance figures prior to 36 weeks. Based on these and other considerations, we
conclude that the actocardiograph data at 36 weeks is comparable to ultrasound-based state
definitions, but this is less likely to be the case earlier in gestation.
12
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
In conclusion, we interpret the current findings as support for fetal state expression at
36 weeks and beyond as a measure of individual differences than provides meaningful
information about state regulatory capacities during early infancy. These relations were
detected despite a variety of issues that conspire to diminish the ability to document fetal
to infant relations. These include maternal factors that may affect the fetus on the day of
assessment, such as dietary and metabolic fluctuations, the wide disparity in the methods
of state measurement available before and after birth, and the relatively transitory nature of
many aspects of neonatal behavior that can jeopardize the validity of one-time assessments. Further research using an individual differences model will serve to elaborate the
nature of continuity from the fetus to child.
Acknowledgements
This research was supported by grant R01 HD27592, National Institute of Child Health
and Human Development, awarded to the first author. The investigators wish to thank the
diligent and generous participation of our study families, without which this research
would not have been possible. Portions of this research were presented at the International
Conference on Infant Studies, Brighton, England, July 2000.
References
[1] Als H. Toward a synactive theory of development: promise for the assessment and support of infant
individuality. Inf Ment Health J 1982;3:229 – 43.
[2] Prechtl HFR. Continuity and change in early neural development. In: Prechtl H., editor. Continuity in neural
functions from prenatal to postnatal life. Philadelphia, PA, USA: J.B. Lippincott Co., 1984. p. 1 – 15.
[3] DiPietro JA, Costigan KA, Pressman EK, Doussard-Roosevelt J. Antenatal origins of individual differences
in heart rate. Dev Psychobiol 2000;37:221 – 8.
[4] Almli CR, Ball RH, Wheeler ME. Human fetal and neonatal movement patterns: gender differences and
fetal-to-neonatal continuity. Dev Psychobiol 2001;38:252 – 73.
[5] Groome L, Swiber M, Holland S, Bentz L, Atterbury J, Trimm R. Spontaneous motor activity in the
perinatal infant before and after birth: stability in individual differences. Dev Psychobiol 1999;35:15 – 24.
[6] Nijhuis JG. Behavioural states: concomitants, clinical implications, and the assessment of the condition of
the nervous system. Eur J Obstet Gynecol Reprod Biol 1986;21:301 – 8.
[7] Arduini D, Rizzo G, Romanini C. Fetal behavioral states and behavioral transitions in normal and compromised fetuses. In: Lecanuet JP, Fifer WP, Krasnegor NA, Smotherman WP, editors. Fetal development: a
psychobiological perspective. Hillsdale, NJ: Lawrence Erlbaum Press; 1995. p. 83 – 99.
[8] Visser GHA, Poelmann-Weesjes G, Cohen TM, Bekedam DJ. Fetal behavior at 30 to 32 weeks of gestation.
Pediatr Res 1987;22:655 – 8.
[9] Nijhuis JG, van-de-Pas M. Behavioral states and their ontogeny: human studies. Semin Perinatol 1992;16:
206 – 10.
[10] Groome LJ, Bentz LS, Singh KP. Behavioral state organization in normal human term fetuses: the relationship between periods of undefined state and other characteristics of state control. Sleep 1995;18(2):77 – 81.
[11] Grieve PG, Myers MM, Stark RI. Behavioral states in the fetal baboon. Early Hum Dev 1994;39:159 – 75.
[12] Groome LJ, Swiber MJ, Atterbury JL, Bentz LS, Holland SB. Similarities and differences in behavioral
state organization during sleep periods in the perinatal infant before and after birth. Child Dev 1997;68(1):
1 – 11.
[13] Junge HD. Behavioral states and state related heart rate and motor activity patterns in the newborn infant and
the fetus antepartum: a comparative study. J Perinatal Med 1979;7:85 – 107.
J.A. DiPietro et al. / Early Human Development 68 (2002) 1–13
13
[14] Pillai M, James D. Are the behavioural states of the newborn comparable to those of the fetus? Early Hum
Dev 1990;22:39 – 49.
[15] Nijhuis IJM, ten-Hof J, Nijhuis JG, Mulder EJH, Narayan H, Taylor DJ, et al. Temporal organisation of fetal
behavior from 24 weeks gestation onwards in normal and complicated pregnancies. Dev Psychobiol 1999;
34:257 – 68.
[16] DiPietro JA, Hodgson DM, Costigan KA, Johnson TRB. Fetal antecedents of infant temperament. Child
Dev 1996;67:2568 – 83.
[17] Derryberry D, Rothbart MK. Arousal, affect, and attention as components of temperament. J Pers Soc
Psychol 1988;6:958 – 66.
[18] Besinger RE, Johnson TRB. Doppler recordings of fetal movement: clinical correlation with real-time
ultrasound. Obstet Gynecol 1989;74:277 – 80.
[19] DiPietro JA, Costigan KA, Pressman EK. Fetal movement detection: comparison of the Toitu actograph
with ultrasound from 20 weeks gestation. J Matern-Fetal Med 1999;8:237 – 42.
[20] Maeda K, Tatsumura M, Utsu M. Analysis of fetal movements by doppler actocardiogram and fetal B-mode
imaging. Clin Perinatol 1999;26:829 – 51.
[21] vanVliet MAT, Martin CB, Nijhuis JG, Prechtl HFR. Behavioural states in growth-retarded human fetuses.
Early Hum Dev 1985;12:183 – 97.
[22] Korner AF, Constantinou J, Dimiceli S, Brown B, Thom V. Establishing the reliability and developmental
validity of a neurobehavioral assessment for preterm infants: a methodological process. Child Dev 1991;62:
1200 – 8.
[23] Brown J, Bakeman R, Coles C, Sexon W, Demi A. Maternal drug use during pregnancy: are preterm and
full-term infants affected differently? Dev Psychol 1998;34:540 – 54.
[24] Korner A, Constantinou J. The neurobehavioral assessment of the preterm infant. New York: The Guilford
Press; 2001.
[25] Brazelton TB. Neonatal behavioral assessment scale. 2nd edn. Philadelphia: J.B. Lippincott; 1984.
[26] DiPietro JA, Larson SK, Porges SW. Behavioral and heart rate pattern differences between breast-fed and
bottle-fed neonates. Dev Psychol 1987;23:467 – 74.
[27] Lucas A, St-James-Roberts I. Crying, fussing and colic behaviour in breast- and bottle-fed infants. Early
Hum Dev 1998;53:9 – 18.
[28] Groome L, Singh K, Bentz L, Holland S, Atterbury J, Swiber M, et al. Temporal stability in the distribution
of behavioral states for individual human fetuses. Early Hum Dev 1997;48:187 – 97.
[29] Fox N, Henderson H, Rubin K, Calkins S, Schmidt L. Continuity and discontinuity of behavioral inhibition
and exuberance: psychophysiological and behavioral influences across the first four years of life. Child Dev
2001;71:1 – 21.
[30] DiPietro JA, Hodgson DM, Costigan KA, Hilton SC, Johnson TRB. Development of fetal movement- fetal
heart rate coupling from 20 weeks through term. Early Hum Dev 1996;44:139 – 51.
[31] Gunnar M. The psychobiology of temperament. Hillsdale, NJ: Lawrence Erlbaum Associates; 1990.
[32] Nijhuis JG, Prechtl HFR, Martin CB, Bots RSG. Are there behavioural states in the human fetus? Early
Hum Dev 1982;6:47 – 65.
[33] vanVliet MA, Martin CB, Nijhuis JG, Prechtl HFR. Behavioural states in the fetuses of nulliparous women.
Early Hum Dev 1985;12:121 – 35.
[34] Groome LJ, Singh KP, Burgard SL, Neely CL, Bartolucci AA. The relationship between heart rate and eye
movement in the human fetus at 38 – 40 weeks of gestation. Early Hum Dev 1992;30:93 – 9.
[35] Visser GHA, Mulder EJH, Stevens H, Verweij R. Heart rate variation during fetal behavioral states 1 and 2.
Early Hum Dev 1993;34:21 – 8.
[36] Arabin B, Riedewald S, Zacharias C, Saling E. Quantitative analysis of fetal behavioural patterns with realtime sonography and the actocardiograph. Gynecol Obstet Invest 1988;26:211 – 8.