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1999; 79:24-39. PHYS THER. Joyce W Sparling, Julia Van Tol and Nancy C Chescheir Fetal and Neonatal Hand Movement http://ptjournal.apta.org/content/79/1/24 found online at: The online version of this article, along with updated information and services, can be Collections Neonates Motor Development in the following collection(s): This article, along with others on similar topics, appears e-Letters "Responses" in the online version of this article. "Submit a response" in the right-hand menu under or click on here To submit an e-Letter on this article, click E-mail alerts to receive free e-mail alerts here Sign up by guest on June 11, 2013 http://ptjournal.apta.org/ Downloaded from

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1999; 79:24-39.PHYS THER. Joyce W Sparling, Julia Van Tol and Nancy C ChescheirFetal and Neonatal Hand Movement

http://ptjournal.apta.org/content/79/1/24found online at: The online version of this article, along with updated information and services, can be

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Fetal and Neonatal Hand Movement

Background and Purpose. Fetal movement occurs early in humangestation and can be observed by ultrasound imaging. This was adescriptive study of fetal hand movements from 14 weeks of gestationto postnatal day 1. The purpose of the study was to identify specifichand movements and their developmental trends in order to betterunderstand low-risk human development. Subjects. Twenty-onewomen with low-risk pregnancies were identified from a universityobstetrics clinic. Their fetuses or neonates were the focus of this study.Methods. Ultrasound imaging was used at 14, 20, 26, 32, and 37 weeksof gestation, and videotaping was used at 1 day after birth. Between 12and 16 minutes of usable imaging was obtained at each fetal age, and24 minutes of videotape was collected neonatally. The duration andfrequency of 7 hand movements were determined and reliably scored.Nonparametric analyses were used. Results. Fetal and neonatal move-ments did not appear to be random, and they appeared to be directedor aimed at specific targets. Fetal movement was variable throughoutgestation. Differences occurred between fetal and neonatal data.Durations of certain hand movements provided data that exhibitedsome developmental trends, such as decreasing linear trends andregression-type U curves. Fetal movements to or at the head and faceand the observations scored at 32 weeks of gestation were the bestpredictors of neonatal movement. Conclusion and Discussion. Resultssuggest the potential for fetal movement to be observed and scoredreliably, with scores used to further our understanding of the develop-ment of human movement. @Sparling JW, Van Tol J, Chescheir NC.Fetal and neonatal hand movement. Phys Ther. 1999;79:24–39.#

Key Words: Development, Fetus, Movement, Neonate.

24 Physical Therapy . Volume 79 . Number 1 . January 1999

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Joyce W Sparling

Julia Van Tol

Nancy C Chescheir

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Commentary on human fetal movement prior tothe advent of imaging appears to have beenbased historically on myth and conjecture.1 Theapplication of ultrasound imaging to the human

fetus in the 1970s permitted direct visualization of fetalmovements in utero and stimulated the initiation ofnaturalistic studies of the fetus.2 Observation of fetalmovement has the potential for providing insights intothe development of coordinated movement, which maybe associated with neural development.3–5 In addition,delineation of early human motor capabilities may cor-roborate the results of animal research,6 marshalinginterest in the study of early integration of humansystems that promote more adaptive functioning.7 Vari-ables related to environmental effects8–10 may be clari-fied and factors related to joint development11 may beelucidated, possibly providing information for clinicalapplication.4

The purpose of this article is to report on an explorationof human fetal and neonatal movement. Our goal was todetermine (1) the duration and frequency of specificmotor behaviors, (2) changes or trends in the expressionof these behaviors during pregnancy, and (3) the man-ner in which these motor behaviors exist neonatally, asthe environment and the child change.

Background

Fetal MovementQualitative and quantitative approaches have been usedin the study of fetal movement by de Vries and col-leagues in the Netherlands. Using ultrasound imaging,de Vries et al12 focused on the first half of pregnancy.Roodenburg and colleagues13 investigated the secondhalf of pregnancy. Based on their observation of appar-ently typical spontaneous human movements, de Vrieset al14 recorded variations in “general movements” thatthey believed suggested abnormalities of the centralnervous system. Following their lead, other researchershave selected, as a dependent variable, general move-ments or “gross movements involving the whole body. Theymay last from a few seconds to a minute....They wax andwane in intensity, force, and speed, and their onsetand end are gradual....The movement is fluent and elegantand creates the impression of complexity and vari-ability.”15(pp152–153) The lack of definition specificity andlong-term follow-up and of detailed methods and thereliability of descriptions have limited the usefulness ofsome of these studies. In only 2 studies—one on thedevelopment of head position16 and one on handed-ness17—was fetal behavior described. Recently, the descrip-tor of “general movements” has been applied to the

JW Sparling, PhD, PT, OT, was Associate Professor of Human Movement and Project Director of the Maternal and Child Health PostgraduateTraining Grant at the University of North Carolina at Chapel Hill at the time this study was conducted. Address all correspondence to Dr Sparlingat 1444 Center Grove Church Rd, Moncure, NC 27559 (USA) ([email protected]).

J Van Tol, PhD, is Research Assistant, Amsterdam, the Netherlands. At the time of this study, she was a Postdoctoral Fellow with Dr Sparling.

NC Chescheir, MD, is Associate Professor of Obstetrics, School of Medicine, University of North Carolina at Chapel Hill.

This study was supported in part by a grant (MCJ000149) to Dr Sparling from the Maternal and Child Health Bureau, Health Resources andServices Administration, US Department of Health and Human Services.

This study was approved by the Committee on the Protection of the Rights of Human Subjects, School of Medicine, University of North Carolinaat Chapel Hill.

This article was submitted November 10, 1997, and was accepted August 17, 1998.

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movement of preterm newborns.18 The description ofnewborn movement is becoming more detailed withresearch.19

Sparling and Wilhelm20 described spontaneous move-ments in fetuses from 12 to 35 weeks of gestation andrecorded the characteristics of hand movement. Manymovements appeared to be directed to a body part or theuterine wall. The hands of the fetuses moved with avariety of frequencies and apparent force. Joint ranges ofmotion changed throughout movements rather thanremaining the same, as in floating. These movementssuggested primary and secondary circular reactions21 inwhich a movement is repeated, presumably because ithas functional importance to the organism. Sparling andWilhelm observed, for example, that early in fetal devel-opment, quick, progressively larger head flexion move-ments were repeated, resulting in a “somersault” thatenabled the fetus to change position within the uterinecavity. In contrast, during later gestational periods, thefetuses’ hands were directed to and manipulated bodyparts and features of the environment, such as theumbilical cord. Thus, later in pregnancy, the handsexhibited manipulative capability and suggested “inten-tionality,” a term coined by Butterworth and Hopkins22

to describe neonatal hand-to-mouth movement.

Other developmental tendencies in hand movementwere noted in early observations20 and are summarizedin Table 1. In that study, movements such as thumb inmouth and bilateral leg extension against the uterinewall were considered by the authors as functionallyimportant. The frequently observed leg extension

against the uterine wall was believed by the authors to bea possible precursor to later participation in the birthingprocess. Validation of the importance of this movementhas been noted in a similar movement of the chickreadying itself for hatching.23 Early movements of thearms appear to assist the fetus in identifying componentsof its environment. The hands can be observed to crossmidline, with the palms “feeling” the uterine wall. Thefetus’ palms also mold to the occiput, grasp the umbilicalcord, and appear to “reach” for the feet. Attributingfunction to any of these early movements, however, doesnot imply that the assigned function is preliminary to ornecessary for the appearance of a spontaneous behavior.

Fetal movement has a wide range of expression.Although some low-risk fetuses appear to have a uniquestyle of movement that is consistent over the gestationalperiod, other low-risk fetuses have fairly wide fluctua-tions in duration and frequency of movement.24 Study-ing the vagaries of movement of low-risk fetuses mayprovide a clue to understanding the motor behavior offetuses with impairment.25 Such studies are neededbefore movements can be seen as deviations from thenorm and can be used for diagnostic purposes.26

Based on the literature and previous studies, we hypoth-esized that there would be extensive, apparently non-functional hand movements early in the fetal period.After the diminution of quantity of movement at 16weeks of gestation noted previously,27 which we posit wascaused by preprogrammed neuronal cell death,28–30 wewould expect to see an increase in more specific move-ments such as hand to mouth, a movement consideredto be functional for the fetus as well as the newborn.22

The increase in these functional movements wouldsuggest some development in motor behavior and anincreased level of motor control by the fetus. Thedecrease in these behaviors might indicate a develop-mental regression in the behavior.

MethodThe Committee on the Protection of the Rights ofHuman Subjects at the School of Medicine of theUniversity of North Carolina at Chapel Hill requested areview of the safety of diagnostic versus therapeuticultrasound prior to the approval of this study. Ourreview and earlier 3-year follow-up study31 indicated noharmful effects of diagnostic ultrasound when usedaccording to the American Institute of Ultrasound inMedicine regulations.32 The committee approved thestudy, and all 25 low-risk pregnant women approachedagreed to participate. One woman withdrew from thestudy at 26 weeks because of difficulty with her preg-nancy and a preterm birth. Another woman was with-drawn from the study because of her difficulty in keep-ing clinic appointments. Two other women were

Table 1.Developmental Motor Characteristics of Low-Risk Fetuses20

GestationalAge (wk) Description

8 Trunk flexion and extension12 Isolated random-appearing movement of extremities14 All movement patterns present; an increased

frequency of movement that is more “organized”in appearance compared with movement at 12weeks; arms appear to “explore” while legsextend against uterine wall; arm crosses midline,extending palmar surface to opposite uterine wall

16 Decreased frequency of movement from 14 weeks,with pincer grasp, thumb in mouth

20 More bilateral movement (eg, legs extend togetheragainst uterine wall, arms flex, and hands areoften held together near the face)

26–32 Independent movement of extremities to all parts ofthe uterus and specific body parts; nocephalocaudal development, but apparent distal-proximal development in extremities

37–38 Decreased frequency of movement; hands oftenmolded to occiput, or dorsum of hand restsagainst uterine wall

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ultimately eliminated from this study because of prema-ture delivery. The fetuses of the remaining 21 womenwere the subjects of this study. The fetuses were consid-ered to be medically within normal limits, as was thepregnancy, the neonates at birth, and the children at 12months of age. For their participation, the mothers weregiven a copy of the ultrasound images and infantvideotapes.

SubjectsThe women who participated in this study were a con-venience sample of low-risk pregnant women attendingthe University Hospitals’ Obstetric Clinic for pregnancyassessment and follow-up. All women except one wereCaucasian, and all women except one were married andliving with their husbands. We believe that a singlewoman may be under more stress during her pregnancyand that this stress might affect the fetus and its move-ment. This was the first pregnancy for 9 of the 21women. At the start of the study, 8 women had one livingchild, and 4 women had more than one child. The meanmaternal age was 30.6 years (SD55.1, range521–40),and the mean paternal age was 31.7 years (SD54.8,range519–39). The 4-Factor Index of Social Status33 wascomputed by averaging scores on grade level completedand occupation for the mother and father. Maternaleducation ranged from high-school completion to over22 years of education (X514.3, SD52.6), and meanpaternal education was 15.6 years (SD54.4). Occupa-tions ranged from category 3 (housewife) to category 9(professional). The mean score of 42.3 (SD512.1) gavean educational-occupational social status range of 2 to 5(X53.5) out of a possible 5 categories.

The designation of “low risk” for fetuses was madeduring the initial obstetric visit based on maternal med-ical history and health status and was checked at eachsubsequent visit by the obstetrician and the obstetricalnurse. The sex of the fetuses (12 male, 9 female) andtheir birth age, birth weight, length, head circumfer-ence, and Apgar scores at 1 and 5 minutes were recordedat birth. These data and the follow-up of the fetuses(Tab. 2) by examination of their medical records at amean age of 12.3 months (SD55.5, range54–19) indi-cate that we had identified a low-risk sample of pregnantwomen whose pregnancies were within normal limits

and whose infants were functioning within normal lim-its, according to physician report, within the first yearafter birth. There were no multiple births.

InstrumentationBased on our extensive experience observing fetal move-ment clinically and in research, the following criteriawere established for longitudinal measurement of move-ment: (1) Fetal position needed to be recorded prior toidentifying extremity movement, (2) right and left handmovements should be scored separately to gain as muchdata as possible and describe asymmetries, and (3) themovement of one body part (eg, the hand) needed to bescored in order to collect longitudinal data beyond 18 to20 weeks. After 18 to 20 weeks, the whole fetus cannot beseen on the imaging screen. The combined results of thescoring of the right and left hand movements arepresented in this article. The 7 hand movements and asample score sheet are shown in Table 3.

A Phillips P-700 ultrasound imager* and a Panasonic AG185 (38 power zoom lens) videorecorder with tripod†

were used to obtain the fetal and neonatal data. Asuper-VHS tape deck and 38.1-cm (15-in) high-resolution monitor were used for viewing the videotapes.Data were input directly to a computer via a softwarepackage designed for start-stop and continuous scoring.‡

ProcedureEach woman was identified by the clinic nurse duringher initial clinic visit at 12 weeks. Appointments weremade for the first ultrasound imaging at 14 weeksaccording to maternal estimation of pregnancy dura-tion. Biparietal diameter and femoral length were usedto confirm maternal dates. The ultrasound images weretaken at 14 weeks (X514.0 weeks, SD54 days,range513.0–15.6 weeks), 20 weeks (X520.0 weeks,SD56 days, range518.3–20.6 weeks), 26 weeks (X526.1weeks, SD56 days, range524.6–28.5 weeks), 32 weeks(X531.7 weeks, SD53 days, range530.4–32.4), and 37weeks (X537.0 weeks, SD54 days, range536.2–38.1).

*Phillips Medical Equipment, 710 Bridgeport Ave, Shelton, CT 06484.†Panasonic, 1 Panasonic Way, Secaucus, NJ 07094.‡Observational Coding System (OCS), Triangle Research Collaborative Inc, POBox 12167, Research Triangle Park, NC 27709.

Table 2.Birth Data and Mean Time of Follow-up for 21 “Low-Risk” Fetuses

Birth Age (wk) Birth Weight (g) Length (cm)

HeadCircumference(cm)

ApgarScore at1 and 5 min

Age atFollow-up(mo)

X 39.8 3,597 52.4 34.9 8.1, 8.8 12.3SD 0.9 506 2.5 1.4 1.1, 0.6 5.5Range 38.4–41.4 2,710–4,470 50–57.5 33–37.5 5–9, 7–10 4–19

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Each woman was interviewed prior to ultrasound imag-ing to record whether there were any changes in work orfamily stress (ie, stressors that could possibly affect themovement of the fetus) that she may have perceived overthe preceding 6 weeks. The third author obtained theimages in mid-afternoon with the woman in a semi-recumbent position, with diminished lighting, consistentwith clinical obstetrical imaging. People who were signif-icant to each woman were encouraged to attend theimaging. One day after birth (X539.9 weeks, SD57 days,range538.4–41.4 weeks), the newborns were video-taped in 3 randomly assigned positions: right and leftside lying and supine. The prone position was not used

because hand movement was constrained in that posi-tion. The camera was positioned above the infant so thatthe whole body could be viewed. The side-lying positionwas maintained by a bendable positioning aid (BendyBumper§). An overhead heater maintained theunclothed child’s temperature at 37° to 38°C. Super-VHS videotapes were copied with a digital time code.The mean duration of the videotaped images wasrecorded (Tab. 4). The percentages of fetal imaging filmin which either the right or left hand, or both, could be

§Children’s Medical Ventures Inc, 541 Main St S, South Weymouth, MA 02190.

Table 4.Total Duration of Ultrasound Images and Percentage of Videotaped Images Scored at Each Gestational Age and at 1 Day After Birth

14 weeks 20 weeks 26 weeks 32 weeks 37 weeks 1 day

Duration (s)X 978 925 881 934 706 1,437SD 231 137 113 234 226 665Range 469–1,502 788–1,408 481–1,036 565–1,452 281–1,069 107–2,542

Percentage of image scoredX 83 83 91 86 87 76SD 13 15 7 7 11 23Range 49–97 50–98 79–100 69–98 51–96 10–100

Table 3.Fetal and Neonatal Movement System and Sample Computer Printout Showing Hand Movement

Column1. Position (in relation to gravity)

0—Cannot tell 3—Prone1—Right side lying 4—Supine2—Left side lying 5—Sitting (upright)

2. Right hand0—Cannot tell 4—Hand to/at knee/foot1—Hand to/at mouth (on lips or in mouth) 5—Hand to/at uterine wall/mattress2—Hand to/at face/head (excluding lips) 6—Hand near mouth (in fluid/air)3—Hand to/at trunk (from shoulders to hips) 7—Hand away from body (in fluid/air)

3. Left hand0—Cannot tell 4—Hand to/at knee/foot1—Hand to/at mouth (on lips, in mouth) 5—Hand to/at uterine wall/mattress2—Hand to/at face/head (excluding lips) 6—Hand near mouth (in fluid/air)3—Hand to/at trunk (from shoulders to hips) 7—Hand away from body (in fluid/air)

Data Set File: 37–14-JSDescription: Position, right and left hand. Time in hours, minutes, seconds, frames.

Record Time Code Description

1 00:00:04.14 Start2 00:00:04.15 000 Cannot see3 00:00:05.18 366 Prone, hands near mouth in fluid4 00:00:06.09 362 Prone, right hand near mouth, left hand at head5 00:00:10.12 302 Prone, cannot see hand, left hand at head6 00:00:16.20 366 Prone, hands near mouth in fluid7 00:01:36.04 377 Prone, hands away from body in fluid

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visualized and scored were 83%, 83%, 91%, 86%, and87% for the 5 imaging sessions, respectively. A mean of74 minutes of imaging per subject (SD51.8) was avail-able for assessment. The total time that hands could beseen was determined and became the baseline for figur-ing the percentage of time (duration) that the handswere moving to and were at 1 of 7 locations. Thispercentage was calculated for each hand movement, foreach fetus, at each age. The percentage of time availablefor scoring postnatally was 76% because the movementof the infant was not scored in Brazelton-designatedstates 1 (deep sleep) and 6 (crying).34 The frequency wasthe number of times that a specific hand movementoccurred within the total time that the hands could beseen clearly and thus scored accurately.

The scoring was the same for the fetal and neonatalmovements. The position of the fetus was documentedon the videotape by the obstetrician. In each positionobserved, start and stop times for hand movements werescored at 30 frames per second. An extensive scoringprotocol (Appendix) was established to assist in accuracyof scoring.

Videotapes were viewed randomly and scored by the firstauthor. Ten percent of the videotaped images, randomlyselected from all of the images, was scored indepen-dently by the first 2 authors. Percentage of agreementwas determined for the scores for the right and lefthands combined. A kappa statistic was generated tocontrol for chance agreement. Overall mean percentageof agreement was 84% (range565%–95%). The overallmean kappa was .72 (range5.57–.95). To achieve thislevel of reliability on a 2-dimensional viewing of a3-dimensional movement, extensive training with non-subject images over several months prior to scoring ofany subject’s videotapes was necessary. Agreement wassimilar for all movements.

Data AnalysisTwo major approaches were taken to analyze the dura-tion and frequency data: use of the nonparametricFriedman 2-way analysis of variance by ranks and afollow-up of age differences using the Wilcoxon signed-ranks test. Nonparametric tests were selected so that noassumptions were made about the measurement scale orthe distribution of the data. The Friedman 2-way analysisof variance by ranks was used with each fetal subjectacting as its own control. We believe that this approachincreases precision because measurements across thetime points are correlated with one another. With thisnonparametric approach, 2 types of comparisons weremade: (1) the row-mean-score statistic (chi square withnumber of repeated measurements minus 1 degree offreedom) identified overall differences in scores ofmotor responses at different gestational ages for each

movement, and (2) the correlation statistic (chi squarewith 1 degree of freedom) accounted for the ordering ofthe repeated measurements, which was used to identifylinear trends in the data. When overall differences butno trends were observed, pair-wise comparisons wereexamined (P5.01) to detect differences. When trendswere observed, pair-wise comparisons were used (P5.05)to indicate any possible support for the trend. Todetermine the association between fetal and neonatalmeasurements, Spearman rank correlations and aregression were computed. Statistical results are pre-sented in terms of (1) overall differences, (2) trends,and (3) differences over the 6 time periods for data ondurations and data on frequencies. Figures 1 through 6show results of durations only.

ResultsThe movement of the fetuses’ hands appeared to bedirected to specific body parts and uterine locations andwas variable. Because of the variability, medians wereused to describe the duration and frequency of behav-iors. To indicate the large variability in the data, themaximum percentage obtained by one subject on onebehavior is depicted for each age category in Figures 1through 6. Medians and ranges have been used in casesof fetal data variability.12 These maximum scores weredistributed randomly over the 21 subjects, with nooutliers. For essentially all behaviors at all ages, the rangein percentages of duration extended from 0% to themaximum percentage shown for one subject. Movementdurations are depicted in Figures 1 through 6. At eachgestational age and at neonatal day 1, the medianpercentage of duration of the 6 movements for the rightand left hands combined is shown. To permit scoring ofall movements, we scored 7 categories of movement,including the “hand to/at the trunk” movement. Fewinstances of the “hand to/at the trunk” movement wereobserved, so analysis was not conducted on thismovement.

Prenatal and Postnatal Duration of MovementsThere was a difference between prenatal and postnatalduration of movements over the 6 time periods. Thepercentages on which these results are based are shownin Figures 1 through 6.

Overall differences. For all movements (P ,.038)except the “hand to/at uterine wall/mattress” move-ment, overall differences existed (Figs. 1–5).

Trends. Decreasing linear trends, from 14 weeksthrough the postnatal period, were noted in the follow-ing movements: “hand near mouth” (P ,.005) (Fig. 2),“hand to/at knee/foot” (P ,.006) (Fig. 4), and “handaway from body (in fluid)” (P ,.012) (Fig. 5). Throughthe postnatal period, an increasing linear trend was

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noted for the “hand to/at uterine wall/mattress” move-ment (P ,.043) (Fig. 6).

Pair-wise comparisons. There was an increase in the“hand to/at mouth” movement postnatally (Fig. 1) whencompared with each gestational week. Postnatal “handto/at face/head” movement scores were not differentfrom prenatal “hand to/at face/head” movement scores(Fig. 3). In contrast, the “hand to/at knee/foot” move-ment showed a decrease postnatally when comparedwith all gestational ages (Fig. 4).

Prenatal Duration of Movement Alone

Overall differences. There were no overall differencesin prenatal duration of movement for the “hand to/atknee/foot” and “hand away from body (in fluid)” move-ments (Figs. 4 and 5).

Trends. A linear decrease (P ,.001) existed over thegestational period in the “hand to/at mouth” movement(decrease in median duration of movement from 3 to 0,

expressed as percentage of time observed) (Fig. 1) andthe “hand near mouth” movement (decrease in medianduration of movement from 21 to 3, expressed aspercentage of time observed) (Fig. 2). No linear trendsexisted in the following movements: “hand away frombody (in fluid)” (Fig. 5), “hand to/at uterine wall/mattress” (Fig. 6), and “hand at/to knee/foot” (Fig. 4).

Pair-wise comparisons. Comparison of behaviors indi-cated duration of movement in the “hand to/at face/head” movement (Fig. 3) decreased (P ,.002) between14 and 32 weeks and increased (P ,.008) between 32and 37 weeks. The “hand to/at mouth” and “hand nearmouth” movement comparisons were similar, with the37-week data less than the 14-week data (P ,.003) andthe 20-week data (P ,.035) (Figs. 1, 2). For the “handto/at mouth” movement, the 37-, 32-, and 26-week datawere also different from the 14-week data (P ,.025)(Fig. 1).

Although there were small median percentages for the“hand to/at knee/foot” movement over the gestational

Figure 1.Median and maximum durations of movement (expressed as percentage of time observed) for “hand to/at mouth” movement pattern at 5 gestationalages and at 1 day after birth (N521).

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period, there was an extremely wide range of thismovement at 32 weeks and even at 37 weeks of gestation(Fig. 4). Observed decreases in duration of movement inthe “hand away from body (in fluid)” movement at 26weeks were not significant due, in part, to 3 subjectswhose durations were maximum for this movement(Fig. 5). For these same subjects, durations at 26 weeksfor the “hand to/at uterine wall/mattress” movementwere minimum.

PredictionIn an attempt to predict postnatal measurements, Spear-man rank correlations resulted in the “hand to/at face/head” movement showing the only “promising” associa-tion. A regression analysis indicated that scores at 32weeks of gestation were the best predictors of postnatalscores (P5.026).

Prenatal and Postnatal Frequency of MovementWith the postnatal data included, there were overalldifferences in the frequency data in all 6 movements(Tab. 5). Few trends, however, were noted. The onlyfrequency trend confirmed the decreasing durationtrend for the “hand to/at knee/foot” movement from 14weeks of gestation to postnatal day 1. Follow-up pair-wisecomparisons among the time periods showed the influ-ence of the postnatal data on the analysis. The prenataldata, therefore, were evaluated without the postnataldata.

Prenatal Frequency of Movement AloneExcluding the postnatal data, there were overall differ-ences (P ,.003) in all movements throughout gestationexcept for the “hand to/at knee/foot” movement. Adecreasing linear trend (P ,.001) was noted in all fre-

Figure 2.Median and maximum durations of movement (expressed as percentage of time observed) for “hand near mouth” movement pattern at 5 gestationalages and at 1 day after birth (N521).

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quency data throughout the gestational period. In gen-eral, there were high ranks at 14 weeks, decreasing to 37weeks of gestation (Tab. 5).

DiscussionThe aim of this study was to enhance understanding ofhuman movement by addressing an area of developmentthat has been neglected in the physical therapy litera-ture. The beginnings of human movement, which we arenow able to observe naturalistically, provide a window forour study of functional movement, the linkage of fetal tonewborn movement, and the future delineation of aber-rant movement.

Hand DirectednessAt the level of analysis of this study, fetal hand behaviorswere described in terms of movement directed to and ata body part. The apparent goal orientation of fetalmovement from 14 weeks of gestation led us to assume a

functional importance for the movements. Whether themodifier of “function” was incorrectly used in this studyor applied to the wrong behaviors is unclear. A develop-ing sensorimotor system, however, apparently was beingobserved. Movement of the hand occurs around themouth with frequent subsequent sucking, and move-ment of the hand to specific body parts occurs withsubsequent molding of the hand around the body part.Movement of the hand to the uterine wall can beobserved, with subsequent flattening and sliding of thepalm against the uterine wall. Fingering, grasping, andmanipulation of the umbilical cord occurs. Fetal grasp-ing of the umbilical cord can cause variable heart ratedecelerations35 and thus may be a behavior critical toassess in future studies. The functional appearance ofmuch of fetal movement suggests the potential earlyrelationship of sensorimotor status and environmentalconditions that constrain or enhance movement(ie, affordances).36–38

Figure 3.Median and maximum durations of movement (expressed as percentage of time observed) for “hand to/at face/head” movement pattern at 5gestational ages and at 1 day after birth (N521).

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These directed paths of movement are reminiscent of“contact paths” described in the ontogeny of facialgrooming in mice,39 a functional activity achieved bymodifying environmental permissive conditions. Futureintervention by physical therapists as well as obstetricianswith fetuses and neonates may be better contemplatedafter identifying functional correlates of complex behav-ioral repertoires and recording environmental charac-teristics that permit their occurrence.

VariabilityThe wide ranges of scores of the movement of theselow-risk fetuses was anticipated. Some authors12,13 havenoted this variability in young developing fetuses. Vari-ability is a characteristic of “low-skill” movement,40 acategory into which low-risk fetal movement certainlyfalls. This variability may well be modified by a myriad ofas yet unexplored exogenous as well as endogenous

factors. We interpreted the variability that we observedin our study as a dynamic characteristic of humanmovement. Decreased variability, presenting as stereo-typical behavior, may be observed in high-risk fetuses orthose fetuses with a problem with sensorimotor adapta-tion.43 Indeed, the movement of fetuses with neural tubedefects has been observed as lacking in variability. Inaddition to our observations of variability, our resultssuggest that there was an emerging underlying structure.The combination of variations in variability and changesin movement during gestation might provide data toassist in prenatal diagnosis.

Postnatal Period Versus Prenatal PeriodDifferences in the movement scores occurred betweenthe prenatal and postnatal periods. We assumed thatthese differences are based on physiological and envi-ronmental factors known to occur over the transition

Figure 4.Median and maximum durations of movement (expressed as percentage of time observed) for “hand to/at knee/foot” movement pattern at 5gestational ages and at 1 day after birth (N521).

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from the fetal period to the neonatal period. Neuralmaturation over the brief span between 37 weeks ofgestation and 1 day after birth could not be sufficient tobe responsible for these changes. The data show anincrease in the “hand to/at mouth” and “hand nearmouth” movements postnatally, a decrease in the “handto/at knee/foot” and “hand away from body (in air)”movements, and an increase in the “hand to/at uterinewall/mattress” movement. These results are compatiblewith neonates’ participation in control of the regulationof their behavioral state36 and with the increased effectof gravity after birth. It is possible that the differencesnoted between the fetuses and the neonates could beused diagnostically (ie, if no differences were noted,delay or other developmental problems might be sug-gested). Because of the multitude of changes occurringover the birth transition, this interpretation is highlyspeculative at present.

Measurement of changes in movement across this tran-sition have been difficult in the past because of a lack ofan assessment tool that could compare the same behav-iors in 2 totally different environments. The differencesnoted in our study suggest that we are measuring theeffects of differing environmental factors that encourageor restrain movements. At present, extensive analysis ofspecific movements across this transition may providespurious results. Research emphasis may best be placedon further analysis of the uterine environment, anecological approach not unfamiliar to dynamical systemsresearch on movement.41

TrendsOur hypothesis that the “hand to/at mouth” movementwould be performed more frequently as developmentprogressed was not supported. Instead, there was a lineardecrease in the occurrence of this movement through-

Figure 5.Median and maximum durations of movement (expressed as percentage of time observed) for “hand away from body (in fluid)” movement patternat 5 gestational ages and at 1 day after birth (N521).

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out gestation, with the hypothesized increase beingobserved only neonatally. The “hand to/at mouth”movement appeared in the newborn where it could beinterpreted as a more functional activity assisting inneonatal modification of behavioral state and oral feed-ing. This type of developmental trend may be depictingthe adaptedness of the organism to changing environ-mental and intrinsic challenges. The linear decrease inthe occurrence of the “hand to/at mouth” and “handnear mouth” movements during gestation in our study isdifficult to compare with the findings of other studiesbecause of methodological differences. Roodenburget al13 and de Vries et al14 identified a decrease ingeneral movements over the gestational period, a resultthat was consistent in our data with only the “hand to/atmouth” and “hand near mouth” movements.

Other trends (U-shaped, inverted U-shaped) are appar-ent in our data. The decrease in the occurrence of the

“hand to/at face/head” movement at 32 weeks and the“hand near mouth” movement at 37 weeks recalls regres-sion curves described in the human infant,25 in which amovement occurs, disappears, or is of short duration andlater reappears, often in a more advanced pattern. At 32weeks, the “hand away from body (in fluid)” movementwas observed more often than the other hand move-ments. At 37 weeks, the “hand to/at face/head” move-ment was observed more often than the other handmovements. Only neonatally were the “hand to/atmouth” and “hand near mouth” movements observed.Although the fetus is able to move the hands to or at themouth and to other specific locations prenatally, only inthe postnatal period may this movement pattern beconsidered “intentional,” as Butterworth and Hopkins22

have suggested. The tendency for the “hand to/at knee/foot” and “hand away from body (in fluid)” movementsto peak at 32 weeks may reflect some tactile proclivity inthe mid-gestational fetus, gravitational constraint in the

Figure 6.Median and maximum durations of movement (expressed as percentage of time observed) for “hand to/at uterine wall/mattress” at 5 gestationalages and at 1 day after birth (N521).

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newborn, and neural maturation. The potential relation-ship of hand movements and neural status was not adirect focus of this study. Changes in these fetal behav-iors, however, suggest that a developmental processcould have been observed and that underlying thatprocess would be neural, as well as musculoskeletal andphysiological, maturation.

Frequency data indicated that declines occurred overthe course of gestation, with increases in frequencyoccurring neonatally, suggesting possible space limita-tions as gestation progressed. This finding was not truefor the “hand to/at knee/foot” movement data, whichshowed a decreasing trend through day 1, indicating thedifficulty postnatally of antigravity movements of largebody parts, as suggested by Thelen and Ulrich’s work.25

Another difference was the decrease in frequency of the“hand to/at face/head” movement at 37 weeks, coincid-ing with an increase in duration of the “hand to/atface/head” movement during this period. This decreasein frequency at 37 weeks might be attributed to increas-ing energy conservation in preparation for birth, as wellas to decreasing uterine space.

LimitationsScoring based on a 3-dimensional view of a 3-dimen-sional movement threatens the credibility of the data.The achievement of good reliability was based on exten-sive training. Although the observers’ scores were reli-able, it is possible that they were not scoring the truebehaviors or that the behaviors were being modified bythe procedures (eg, the imaging). Three-dimensionalviewing is currently being used to assess patients withbreast cancer, but it has not been commonly available toassess the movement of fetuses. The future availability ofthis technology may assist observers in more validscoring.

The number of subjects in this study was relatively small.Additions to this database might permit further analysis,such as analysis of differences between male and femalefetuses. Achieving significance in some movements usingnonparametric statistics, specifying the actual amount of

data used for analysis, and using a variety of subjects overthe course of pregnancy with follow-up do not lessen theneed for a larger subject pool.

We did not assess fetal behavioral state directly, and wescored neonatal movements only in behavioral states 2through 5.34 Although the initial linkage among thebehavioral state variables of movement, heart rate, andeye movements may appear earlier (ie, at 20 weeks42,43),Swartjes et al44 determined that “true behavioral states”were not found until 32 weeks of gestation. An attemptwas made to consider variability in behavioral statefactors in the following ways: by scoring the movementsof over 20 subjects, by performing ultrasound imaging atleast 2 hours after a meal so that glucose levels would notaffect the movement, and by assessing fetuses at approx-imately the same time of day. Diurnal variation in fetalmovement has been established45 and could affect theduration and frequency of movement.

Concerns about the safety of ultrasound imaging havelimited fetal research in this country. Human subjectreview committees and granting agencies have ques-tioned the risk-benefit ratio of the use of this technology.In our study, identification of additional subjects, ratherthan increasing observation time, was used to obtaindata for analysis. Recent increases in the amount ofimaging time allowed by federal granting agents42 arewelcomed and supported by long-term studies on thesafety of ultrasound imaging.31 Most of the studiesconducted in the Netherlands have used 1-hour imagingsegments for analysis.

The results of studies of nutritional and other environ-mental factors vary. Based on research describing socialinfluences on pregnancy,46,47 there should be consider-ation of the potential effect on fetal movement of theenvironment beyond the uterus. Differences in lifestyle,nutrition, family, work, and stress levels may help toexplain the large variance that all investigators haveobserved in movement duration and frequency. Thedemographics of this sample describe a wide variety ofoccupational and educational experience. These influ-

Table 5.Median Frequencies and Ranges (in Parentheses) of 7 Hand Movements at 5 Gestational Ages and at Postnatal Day 1

Hand Movement 14 weeks 20 weeks 26 weeks 32 weeks 37 weeks 1 day

Hand to/at mouth 3 (0–20) 2 (0–12) 0 (0–2) 0 (0–7) 0 (0–2) 20 (2–56)Hand near mouth 15 (0–12) 12 (0–27) 2 (0–27) 2 (0–32) 2 (0–11) 29 (7–109)Hand to/at face/head 13 (2–26) 10 (0–32) 3 (0–12) 2 (0–14) 3 (0–12) 32 (6–81)Hand to/at knee/foot 4 (0–16) 3 (0–11) 2 (0–12) 2 (0–21) 1 (0–8) 0 (0–5)Hand away from both (in fluid/air) 21 (5–39) 17 (1–38) 5 (0–29) 5 (0–20) 2 (0–14) 43 (3–57)Hand to/at uterine wall/mattress 5 (0–30) 9 (1–24) 3 (0–20) 2 (0–18) 2 (0–13) 28 (0–76)Hand to/at trunk 2 (0–12) 2 (0–7) 0 (0–65) 0 (0–11) 1 (0–5) 16 (2–60)

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ences need to be disentangled in future studies, as theircomponents might affect motor development.

Future DirectionsInvestigation of fetal sensorimotor development maydetect behavioral patterns characteristic of impair-ment4,48–50 and may increase our understanding of dis-orders such as cerebral palsy. Current data suggest that60% of neurodevelopmental disabilities are caused dur-ing the prenatal period.51 Within this category, cerebralpalsy has been reported to be the most “life-limiting” ofchildhood disabilities. Kuban and Leviton have statedthat “efforts to prevent cerebral palsy will require a focuson factors and events during pregnancy, including thosethat predispose the mother and fetus to pretermdelivery.”52(p193) Identification of changes in movementpatterns over gestation may assist in explicating the roleof some of these factors and events.

To address such critical questions, appropriate assess-ments will be necessitated. As the category of “generalmovements” is being further specified, so too may themovement patterns that we studied. Theoretical applica-tions, such as those expressed by Sporns and Edelman,53

will be important guides in this process. Further behav-ioral analysis of the human fetus may provide neededinformation about approaches and equipment that todate have not been fully tested.

ConclusionMovement of low-risk fetuses appears to be nonrandomand is variable across the gestational period. Majordifferences in movement occur between fetuses andneonates. Developmental trends using conservative lev-els of significance in nonparametric analyses were iden-tified in the movement of 21 low-risk fetal subjects. Alinear trajectory decreasing over the pregnancy wasnoted in the “hand to/at mouth” and “hand nearmouth” movements. A regression occurred in the “handto/at face/head” movement pattern observed early ingestation, followed by a diminution in the recordedduration of this movement pattern and then a reappear-ance of this movement pattern neonatally. Other move-ment patterns, such as the “hand to/at knee/foot”movement pattern, were not observed early in gestation,appeared during midpregnancy, and then decreasedacross the perinatal period, apparently awaiting physio-logical stability and environmental support before fur-ther expression. The reciprocal relationship betweenmotor and sensory development is suggested by theapparent goal-oriented and interactive characteristic ofthese movements.

AcknowledgmentsWe are appreciative of the statistical advice and assis-tance of Dr Gary Koch and Wendy Greene, Department

of Biostatistics, School of Public Health, University ofNorth Carolina at Chapel Hill.

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3 Okado N, Kojima T. Onogeny of the central nervous system: neuro-genesis, fiber connection, synaptogenesis, and myelination in thespinal cord. In: Prechtl HFR, ed. Continuity of Neural Functions FromPrenatal to Postnatal Life. Philadelphia, Pa: JB Lippincott Co; 1984:31–45.

4 Koyanagi T, Horimoto N, Maeda H, et al. Abnormal behavioralpatterns in the human fetus at term: correlation with lesion sites in thecentral nervous system after birth. J Child Neurol. 1993;8:19–26.

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7 Krasnegor NA, Blass EM, Hofer MA, Smotherman WP. PerinatalDevelopment: A Psychobiological Perspective. New York, NY: Academic PressInc; 1987.

8 Riegger-Krugh C, Blair A, Sparling JW. Assessment of fetal kneeangular velocity as a possible method to determine the effect ofprenatal exposure to cocaine. Physical and Occupational Therapy inPediatrics. 1996;16(1/2):173–186.

9 Sival DA. Studies on fetal motor behaviour in normal and compli-cated pregnancies. Early Hum Dev. 1993;34:13–20.

10 Smotherman WP, Robinson SR. Tracing developmental trajectoriesinto the prenatal period. In: Lecanuet JP, Fifer WP, Krasnegor NA,Smotherman WP, eds. Fetal Development: A Psychobiological Perspective.Hillsdale, NJ: Lawrence Erlbaum Associates Inc; 1995:15–32.

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18 Geerdink JJ, Hopkins B. Effects of birthweight status and gestationalage on the quality of general movements in preterm newborns. BiolNeonate. 1993;63:215–224.

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27 Long T, McCusker S, Ruble J, Sparling JW. Periods of activity andinactivity in the 12- to 16-week fetus. Physical and Occupational Therapy inPediatrics. 1993;12(2/3):163–179.

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30 Oppenheim RW, Nunez R. Electrical stimulation of hindlimbincreases neuronal cell death in chick embryo. Nature. 1982;295:57–59.

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42 DiPietro JA, Hodgson DM, Costigan KA, et al. Development of fetalmovement: fetal heart rate coupling from 20 weeks through term. EarlyHum Dev. 1996;44:139–151.

43 Drogtrop AP, Ubels R, Nijhuis JG. The association between fetalbody movements, eye movements, and heart rate patterns in pregnan-cies between 25 and 30 weeks of gestation. Early Hum Dev. 1990;23:67–73.

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Appendix.Scoring Protocol

Computer Printout—directions for use of Observational Coding System(OCS) are in the manual from Triangle Research Collaborative Inc.Column 1: Position—it is critical to first designate the hand beingviewed. Check on Dr Chescheir’s designation of view and followthrough with that until a change is noted. If left side lying, then left handwill probably not be observed easily and may not move as much as righthand.Columns 2 and 3 are designed to determine whether the hand is in fluid,interacting with the environment (uterine wall, umbilical cord, mattress)or directed to other body parts. Position is the preliminary essential forscoring right and left hands.

Movement Patterns1. Score “hand to/at mouth” movement (1) when thumb or fingers are

in mouth or touching lips, or hand is touching immediate perioralregion. Contact of mouth is of primary importance. If hand touchesmouth and at the same time touches uterine wall, for example, score“1” for mouth contact. The dorsum of hand may be on the uterinewall, with fingers at the mouth. When hand touches 2 things,however, score what is touched by fingers or the palm of the hand.

2. Score “hand to/at face/head” movement (2) when hand is incontact with the face or head but outside of the perioral regiondescribed for “hand to/at mouth” movement. Note the hand oftenmolds to the occiput, so observe carefully.

3. Score “hand to/at trunk” movement (3) when there is hand contactanywhere on the body from shoulders to hips, including the genitalareas. This movement may initially appear as “hand away frombody (in fluid)” movement, but fingers are contacting genitals.

4. Score “hand to/at knee/foot” movement (4) when hand is in contactwith lower extremity. This movement is almost always contact withknee, with hand molded to knee, or with foot, where fingers are incontact with toes and sometimes ankle.

5. Score “hand to/at uterine wall/mattress” movement (5) when handcontacts placenta or uterine wall and, in the case of the newborn,when hand is in contact with the mattress. The volar surface of thehand is usually the hand part that is contact with the uterine wall.

6. Score “hand near mouth” movement (6) when fingers are in fluidbetween nose and shoulders/nipples or between both shoulders.Hands must be at or below eyes, within ears, and less than a handaway from mouth to be scored.

7. Score “hand away from body (in fluid)” movement (7) when hand isnot in contact with uterine wall, placenta, or body part, nor is it insmall area near mouth.

When neither hand can be seen adequately to score a hand behavior,score “0.”

Common Problems1. Any time image of the hand is lost to view, but no change in position

is observed when image returns within 4 seconds, continue codingas before loss of image.

2. Contact with body part is characterized by no obvious fluid betweenpart and hand. Mark code when hand contacts new part.

3. To score any behavior, it must occur for 15–30 frames/second. Anymovements quicker than 15 frames/second, therefore, are elimi-nated from a change in score or are scored “0.”

4. When 2 hands are present, follow 1 hand only during a movementsegment, then repeat the observation and scoring for the other hand.

5. Must see body part (ie, hand, face, trunk, legs) to score hands, unlessclearly identified just before or just after segment to be scored. Incase of doubt, score fluid rather than contact. For example, when indoubt, assign a score of “6” rather than “5.”

Newborn Scoring1. Film neonate 2–3 hours after feeding. Best time is at 7 AM.2. Do not score state 1 (deep sleep) or state 6 (vigorous crying). Can

gently awaken neonate, or provide calming through voice, touch,and cuddling.

3. Any contact with face predominates over contact with trunk ormattress.

4. Arms appear to be “locked” into a square area around the face.Score “6” when hand is below nose, between ears, and abovenipples.

5. Remember that the hand contact determines the score. However, ifarm is moving, rating a score of “7,” and momentarily rests on thebody, do not assign a score of “3” but a score of “7.” Hand mustmake contact for 15 frames before changing scores.

Using computer program, score hand behaviors each time a newposition, movement, or posture is observed. Cannot score posture ifcannot score columns 1 and either 2 or 3.

Column 1—Body position of fetusColumn 2—Right handColumn 3—Left hand

Scoring for postures:0—Cannot see or identify1—Hand clasp (hand to hand). The following definition from theAssessment of Preterm Individual Behavior9 may be helpful in scoringaccurately: “The infant grasps his own hand or clutches his handsmidline to his own body. The hands each may be closed, but they holdonto each other or actively press against each other. Interdigitation offingers of one hand with those of the other hand is a subcategory ofhand clasp.”a The hand contact can occur from below elbow to includehand. If forearms or hands are crossed, assume they are touching andscore “1.”2—Hand grasp. Als described as “the hand opens and closes.”a Wesuggest that there may be some thumb opposition, as in grasping theumbilical cord or a body part. This is to differentiate grasp from clasp orhand to umbilical cord. Code “2” only for grasp using individual hand.When hand to hand, score “1” even though it may be a hand grasp.3—Hand to cord. Dorsum or ventral hand surface touches umbilicalcord. If grasp of umbilical cord occurs, score “2” first, then immediatelyscore “3” to obtain the duration of the grasp.4—Finger splay. Finger extension and abduction. Als described as “theinfant’s hands open, and the fingers are extended and separated fromeach other.a

5—Wrist drop. Hand flexes at wrist more than 30°. Do not score ifdorsum of hand is pushing against uterine wall or body part. Thisposture is seen in fluid.6—Fist. Full flexion of fingers.7—Finger posturing. Individual finger or thumb movements.

a Als H. Manual for the Naturalistic Observation of Newborn Behavior (Preterm andFull-Term Infants), 1984. Available from author at Children’s Hospital, Boston,Mass.

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1999; 79:24-39.PHYS THER. Joyce W Sparling, Julia Van Tol and Nancy C ChescheirFetal and Neonatal Hand Movement

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