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. 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