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Visual and Auditory Orienting Responses in Preterm Infants: A Comparison of Three Cohorts Over Time Marilyn L. Riese
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Department of Pediatrics , University of Louisville, School of Medicine Published online: 21 Oct 2013.
To cite this article: Marilyn L. Riese (1992) Visual and Auditory Orienting Responses in Preterm Infants: A Comparison of Three Cohorts Over Time, The Journal of Genetic Psychology: Research and Theory on Human Development, 153:2, 155-163, DOI: 10.1080/00221325.1992.10753710 To link to this article: http://dx.doi.org/10.1080/00221325.1992.10753710
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Th e Journal a( Generic Psvchologv. 153(2) . 155- 164
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Visual and Auditory Orienting Responses in Pre term Infants: A Comparison of Three Cohorts Over Time MARILYN L. RIESE Department of Pediatrics University of Louisville School of Medicine
ABST RACT. Visual and auditory orienting responses we re compared in three cohorts of pre term infants (N = 35 1) born between 1977 and 1987 . The infants were divided into one group born between 25 and 34 weeks ges tati onal age (n = 140) and o ne group born between 35 and 37 weeks ges tational age (n = 2 11 ). Ratings were made of the infants ' best orienting respo nses to a bull's-eye , rattle , bell , voice, and face plus vo ice combined . Analyses of covariance were computed to adjust for changes in perinatal variables between 1977 and 1987 . For both groups , there were significant differences between cohorts on orienting to the bull 's-eye, with a trend for the 25- to 34-week group on orienting to the rattle . Behav ioral outcome for preterm infants has improved with changes in neonatal inte nsive care.
RECENT IMPROVEMENTS in neonatal intensive care have led to lower rates of mortality and morbidity in preterm infants as a group , and to an increase in survival rates of earlier born preterm infants . One significant question is whether the behavioral outcome for the preterm infant has improved concurrent with the improved medical outcome. Thi s question was addressed in a study of two cohorts of 2-year-old preterm children by Kitchen et al. This research was supported in part by a grant from the John D. and Cath erine T. Ma cArthur Foundation , Grants HD-14352 and HD-22637 from th e National In stitute of Child Health and Human Development, and a research grant from the graduate school of the University of Louisville . I am grateful to th e parents and th eir infants who participated in the study; to th e administrators and nursing staffs in th e participating hospitals; and to many coworkers who contributed so much to the program , including E . Harpring, M. Hinkle, P. McNulty, B. Moss, P. Murph y, S. Nuss , C. Reader, and M . Riedesel. Address correspondence to Marilyn L. Riese, Child Development Unit, Health Sciences Center, University of Louisville , Louisville , KY 40292. 155
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( 1986) , who fo und th at the later born cohort had signifi cantl y hi gher mental development scores , and less myopia and strabismus , th an the earlier born cohort. The later born co hort , however, had a hi gher incidence of ce rebral palsy In a preliminary neonatal evaluation of low birthweight (less than 1500 g) preterm infants born in one hospital and tested at term on the Neonatal Ne urobehavioral Assess ment Scale (Kurtzberg et al. , 1979) , Wallace, MeCart on, Kurt zberg, and Vaughan ( 1988) studied three cohort s of infants. They fo und that the earl y born cohort had lower means on visual and auditory summary scores th an did the two later born cohort s. Howeve r, the middle cohort had hi gher means th an the earlier and later born cohort s on an active motor summary score . This latter study suggests that the assessment of preterm infants durin g earl y infancy can be used to desc ribe the infants ' statu s. The purpose of the present stud y was to compare res ponses to visual and auditory orienting items in three cohorts of preterm infants. Allen and Capute ( 1986) discussed the importance of auditory and visual abilities for processing environmental stimuli. All en and Capute and others have noted that ex tremely premature infants are especiall y at ri sk for impairment of these systems. For th is st udy, therefore, auditory and visual orienting items were used as an index of behavioral functionin g in medicall y stable preterm infants. The infants were assessed at the time of di scharge from the hospital , so that the assessment corresponded with the time of medical stability as determined by the medical staff. The infants were born at six hospitals within one community that have obstetrical units (three of which have intensive care nurseries) ; thu s, the entire range of socioeconomic statu s was represented in the sample. The three cohort s consisted of 128 infants born between 1977 and 1979 , 129 infants born between 1980 and 1983, and 94 infants born between 1984 and 1987. Ratings were made of orienting responses to a bull 's-eye , rattle, bell, voice , and face plus voice combined . Method Subje cts
The sample included 351 preterm twins (161 male , 190 female) participating in a study of behavioral patterns during the neonatal period as part of the ongoi ng developmental program of the Louisville Twin Study (Ri ese 1983a, 1983 b). Gestational age at birth ranged from 25 to 37 weeks. The infants were assessed when they were medically stable, just before di scharge from the hospital (range, 2 to 159 days old; M = 18 days old ). Five infants were more than 2 month s of age: one was 75 days old , one was 105 days old , one was 136 days old , one was 137 days old , and one was 159 days old .
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Because degree of prematurit y may affect outcome, the infants were divided by gestational age at birth as follows : one group of 140 infants born between 25 and 34 weeks gestational age , and one group of 211 infants born between 35 and 37 weeks gestational age. For technical and psyc hological reasons, tw ins are not bloodtyped until they are 3 years old; therefore , twin analy ses were deferred until zygosity could be verified.
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Procedure
Infant s were tested in a quiet room off the nursery. The test procedures remained the same over the years so that all infants were assessed in the same manner. The orienting items were prese nted to the preterm infants as part of the larger comprehensive assessment of behavior. The orienting assessment was conducted midway between two feeding periods while the infant was in an awake state. Positioning of the infant s for each test item was as follows . For the bull 'seye, infants were held in an upright position with the head and back supported; the infants were seated on the examiner's lap . For the rattle and bell , infants were supported in a se misupine position on the examiner's lap . For vo ice and face plus vo ice, infants were held under the arms in an upright posi ti on. The infant's head was placed in the midline before each trial. Present ation of the items was randomized with the presentation of other items in thi s part of the assessment to prevent habituation to any individual item . The orienting items, adapted from the Neonatal Neurobehavioral Assessment Scale (Kurtzberg et al., 1979) , were as follows. Bul/'s-eye. A black-and-white bull's-eye was presented at the midline, 15 em
in fro nt of the in fant 's face. If the infant fixated , the bull 's-eye was moved 90° to one side and then 90° to the other side. The initial movement was made to the right two times and to the left two times. Possible responses were no following response (I); fixation, brief transient following (2); fixation, intermittent good following (3); or sustained fixation, following with head and eyes (4) . Rattle. A standard rattle from the Bayley (1969) Scales of Infant Develop-
ment was presented three times 30 em to the right side of the infant 's head and out of view, and three times to the left . Possible responses were no orientin g response (I); quieting , eyes brightening and widening, with blinking but no eye movement (2) ; quieting, eyes brightening and widening, some searching movements with eyes only (3); and eyes brightening and searching with head turning to side of sound (4). Bell . A standard bell from the Bayley ( 1969) Scales of Infant Development
was used . Presentation and scoring were the same as for the rattl e.
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Vo ice. For thi s ite m the examiner spo ke to the infant , say ing " Hi baby," '' Hi [baby 's name] ," and so o n . Presentation and scorin g we re the sa me as for the rattl e .
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Fa ce plus vo ice combined. For thi s ite m , the ex aminer he ld the infant in an up rig ht pos itio n , with the in fa nt 's face approx imately IS em fro m the e xaminer 's. The examine r atte mpted to capture the in fa nt 's visual fixa tio n; if successful, the examine r slow ly moved 90° to o ne side of the in fa nt , the n bac k ac ross the m idline 90° to the o ther side, smilin g and talking to the infant the e nti re time. T he initi al mo vement was made to the ri ght two times and to the left two times. Possibl e responses were nofixation on face ( ! );fixa tion, brief transient fo llowing (2) ;fixa tion, intermillent good fo llowing (3); or sustained .fixa tion , steady fo llowing with head and eyes (4). lnterrater reliabilit ies, determined by intracl ass correlations, were as fo llows: bull s-eye, r = .95; rattl e, r = .90 ; bell , r = .92: vo ice, r = .97; face plu s voice , r = . 97 .
Results
Changes in Perinatal Va riables Because there may have been c hanges between 1977 and 1987 in spec ifi c vari abl es associ ated w ith changes in perinatal care occ urring in that time peri od , anal yses first we re computed to determine if there were differences betwee n the cohorts o n several perinatal variables. The vari ables examined included birth we ig ht , 1-min Apgar scores, 5-min Apgar scores, number of days in the hospital , number of days in an iso lette, test weight , test chronolog ical age (numbe r of days since birth), test conceptio nal age (gestational age at birth plu s chronolog ical age ), and mother's age. These variables were used as gross estimates o f pe rin atal complicatio ns and neonatal clinical status. Thi s procedu re was necessary because detail s of neonatal complications were not de termined in the same manner across the stud y time period , similar kinds of in fo rmatio n were not always available, and/o r the sampl e size was not large e nough for detailed analyses by cohort. The results of analyses of variance (ANOVAs) performed separately for the two gestational age groups indicated that there were no differences between the cohorts o n measures of birth weight , !-min Apgar scores , 5-min Apgar scores, and test conceptio nal age . However, for the 25- to 34-week group , there were differences between the cohorts on meas ures of test weight , F(2, 137) = 3 .34 , p < .04 ; test chronological age, F(2, 137) = 3. 13, p < .05; and mother's age , F(2 , 137) = 9 .29 , p < .0002. Further analyses indicated th at in fa nts born be tween 1980 and 1983 and between 1984 and 1987 we ig hed more at the time of tes ting t( Ill ) = - 2 .41 , p < .02, and t(88) = - I. 98 , p < .06 , respective ly, and had older mothers th an infants bo rn be-
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twee n 1977and 1979 , r(l ll ) = - 4.19,p < .OOO I , and r(88) = -3. 13 , p < .003, respectively. In add iti on , infant s born between 1984 and 1987 were chro no log ical ly older at the time of testing than were infants born between 1977 and 1979, t(88 ) = - 2.4 7 , p < .02. It is noteworthy that , even though infants born more rece ntl y weighed more and were chronologically older than earli e r born infants when tested , there was no difference in conceptional age betwee n the cohorts at the time of te sting. For the 35- to 37-week group , differences were observed on number of days in hospi tal , F (2 , 208) = 5.33, p < .006; number of days in an isolette , F(2, 208) = 6.26 , p < .003; and mother 's age, F(2 , 208) = 3.88 , p < .03. In fa nt s bo rn between 1980 and 1983 and between 1984 and 1987 spent fewer days in an iso lette tha n infants born between 1977 and 1979 , t(l43) = 2.89, p < .005 , and r( l31 ) = 2.93.p < .004, respectively ; spent fewer days in the hos pital than infants bo rn between 1977 and 1979 , r(l43) = 2.60, p < .01 , and r(l3 1) = 2. 61 , p < . 0 I , respectively ; and had older mothers than infant s born between 1977 and 1979, r( I43 ) = -2.33 , p < .03 , and r(l31 ) - 2.52, p < .02, respective ly.
Orienting Responses To determine whethe r there were differences in orienting responses between the three cohorts of prete rm infants, an ANOVA was computed on the best, or hi ghest, scores for each orienting item : bull 's-eye , rattle , bell , voice , and face plus voice combined . Best scores were used as a measure of the infant 's capability at the time of assessment. As Brazelton (1984) pointed out , measurin g the infant 's best performance is an indicator of the infant 's organizati onal capac ities. Separate analyses were computed for each gestational age group . The results indicated that, for infants born between 25 and 34 weeks gestati o nal age, there were significant differences between the cohorts on orientin g to the bull 's-eye , F(2, 135) = 7 .62 , p < .0007 ; and orienting to the rattle, F(2 , 135) = 3 .62 , p < .03; with a trend for orienting to face plus voice combined , F(2, 135 ) = 2. 72 , p < .07. Further analyses indicated that infants born between 1980 and 1983 and between 1984 and 1987 had higher scores on orienting to the bull's-eye than infants born between 1977 and 1979 did , !( 109) = -3 .24,p < .002 ,andt(86) = -2 .92 , p < .005 , respectively, and hi gher scores on orienting to face plus voice combined than infants born between 1977and 1979did , t(l09) = -2.0l , p < .05 ,andt(86) = -1.89 , p < .07, respectively. In addition, infants born between 1984 and 1987 had higher scores on orienting to the rattle than did infants born between 1977 and 1979 , t(86) = -2. 52 , p < .02. For the 35- to 37-week group , the results of ANOYAs demonstrated a signifi cant difference between cohorts on orienting to the bull 's-eye , F(2 ,
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198) = 4. 33, p < .02. Infants born between 1980 and 1983 and between 1984 and 1987 (trend ) had hi gher scores on orienting to the bull 's-eye th an did infants born between 1977 and 1979 , r(l39) = - 2.27, p < .03, and r( l28 ) = - 1.87 , p < .07, respectivel y. Because changes in specific perinatal variables had been observed across cohorts, it was necessary to control for the potential effect of these changes on the orienting scores. For this reason, an analysis of covariance (ANCOYA) was computed for each of the orienting items , using test weight , test chronological age , and mother's age as covariates for the 25- to 34-week group and using number of days in hospital , number of days in an isolette, and mother 's age as covariates for the 35- to 37-week group. The ANCOYA determines if differences between the group means remain after statistically adjusting for the effects of the covariates by equating each group on the covariates (Winer, 197 1). The results indicated that , for the 25- to 34-week group, a significant difference in group means remained for orienting to the bull's-eye, F(2, 132) = 5.11, p < .007, with a trend remaining for orienting to the rattle , F(2, 132) = 2.54 , p < .08. For the 35- to 37-week group, a significant difference between cohorts remained for orienting to the bull's-eye , F(2, 195) = 2.83, p < .06. Thus , stati stic all y sig nificant differences between cohort scores on the orientin g items, espec ially to visual stimuli , remained even after adjustment was made for the effect of the perinatal variables. Discussion
These findin gs demon strate significant changes in orienting responses for preterm infants assessed between 1977 and 1987. Although this study cannot address cause and effect for these results, such changes in scores concurrent with changes in neonatal intensive care suggest that medical improvements during these years not only have led to increased survival rates for preterm infants but also may be related to improved outcome for these infants in at least one behavioral area . In addition , medical improvements over this time period may include changes in prenatal care that also may have a significant effec t on the behavioral outcome of the preterm infant. The most noteworthy change observed was that for visual following of a black-and-white bull 's-eye. The change in orienting scores for this stimulus was maintained for both groups of preterm infants even after adjustments were made for the potential effects of changing perinatal variables. Clinical assessments of infant development frequently use measures of the infant 's ab ility to visually follow a moving target; this ability is important because of its relation to perceiving and learning about various properties of objects (Ruff, Lawson, Kurtzberg, McCarton-Daum , & Vaughan , 1982) . A change in response to orienting to rattle was observed for the 25- to 34-week group but not for the 35- to 37-week group. After the potential ef-
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fec ts of the relevant covariates were controlled for, the signific ant change ac ross time for the earli er born infant s remained as a trend . Thus, there were no co nsistent changes across cohorts for orienting to auditory stimuli, a finding that may be explained partiall y by changes in knowledge of how preterm infants respond to these kinds of stimuli. Standard prese ntation of these auditory orienting stimuli has been for a period of 5 s, with recordin g of response immediately thereafter. Clarkson, Clifton, and Morrongiello ( 1985) studied response latency to auditory stimuli and found that infants frequentl y show head turning responses seve ral second s after termination of the stimu lus. In the present study, a suffi cie nt period of time may not have bee n provided for all infants to respond before scoring. More signifi cantl y, the findin g that the most consistent change in orienting responses across cohorts were for visual stimuli (i.e ., the bull 's-eye) rather than auditory stimuli (i.e., the rattle and , for combined stimuli , face plus voice) may be due to the relative maturation at birth of the two perceptual systems involved. The auditory system develops before the visual system ; specificall y, at 20 weeks gestati onal age the auditory apparatu s is structurall y comparable to th at of an adult (Eisenberg, 1969), even though maturation of response to all frequencies , for example , continues to develop fo r some time (Rubel, 1985 ). In contrast, responsivity to visual stimuli develops rel ativel y later (Komer, 198 1). Therefore, the auditory apparatus of the infant is not likely to be affec ted as much by premature birth as the visual apparatus , especiall y for those infants born later in gestation. Because the visual system continues to develop after premature birth , thi s system may be more susceptib le to the co mplications assoc iated with prematurity than the auditory system is . One conseq uence of the advances in perinatal medicine over the time span studied may have been the alleviation of the adverse effects of prematurity on the developing visual system. In fa nts born between 25 and 34 weeks were among those for whom improvements in orienting responses were observed , an especial ly significant findi ng because thi s is the age group of most concern . Unfortunately, the sample was too small to divide the groups further by gestational age at birth , so it was not possible to determine if there have been changes for extremely early preterm infants . These results add to those of Wallace et a!. (1988), who found lower means on orienting summary scores for an earlier born cohort of low birth weight in fants when compared with two later born cohorts . The present study, however, defined differences in scores for the cohorts for indi vidu al visual and auditory orienting respon ses, specificall y, orienting to a bull's-eye an d to a rattle . Furthermore , the present study used best responses to individual orientin g items as an index of the preterm infant's ability, whereas Wallace et al. ( 1988) evaluated mean scores for the orienting items . Exam ination of best responses proved to be especially inform ative about changes in scores over
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time. Finally, Wallace et al. ( 1988) assessed infants when they reached term con ceptional age , regardless of medical status or time since hospital discharge (if they were home). In the present study, infants were assessed when it was determined that they no longer needed hospitalization. Though both approaches have merit for addressing the problem of testing time in a specific way, responses were not influenced by home-environment variables in the present study. All infants in this study had been described as medically stable for discharge by medical personnel when tested. It may be that the criteria for "medically stable" changed across cohorts as more advanced medical procedures made it possible to stabilize preterm infants more quickly than the procedures that were available when the study began . In fact, finding no differences between the groups for perinatal variables such as birth weight and Apgar scores indicated that some measures of status at birth had not changed across cohorts . In contrast, for the 35- to 37-week group, infants born in the years 1980 to 1987 spent fewer days in an isolette and fewer days in the hospital than did infants born between 1977 and 1979 . These differences may reflect changes in medical care over time (as well as attempts at medical cost containment). It is possible that, if the most recent cohort of 35- to 37-week infants had remained in the hospital for a similar period of time as the earlier cohort , higher ratings on the orienting items would have been obtained. Finally, other variables that were not assessed in this study also may have changed over time, thereby influencing changes in neonatal responding. For example , measures of socioeconomic status (SES) were not available for the first cohort; however, no differences in either mothers' or fathers' SES were found between the second and third cohorts. As infants were tested at all hospitals throughout the time of the study, it was assumed that the full SES range was included in the first cohort as it was for the second and third cohorts . Longitudinal studies of smaller samples from these three cohort populations have, in fact, confirmed that the full range of SES consistently has been included (Matheny, Riese, & Wilson, 1985; Riese, 1987) . In any event, a significant improvement in pre term infants' orienting scores was observed across these three cohorts. Information may be available from other research to determine whether there are changes in other behavioral areas over time for high-risk infants, providing additional encouragement that the outcome for preterm infants has improved .
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Braze lton, T. B. (1984 ). Ne onatal Behavioral Assessment Scale. London: Spastics International Medical Publications/Blac kwell Sc ientifi c Publications. Clark son, M.G., Cli fton, R. K., & Morro ngiello, B. A. ( 1985). The effects of sound du ration o n newborn s' head orientati on. Journal of Experimental Child Psychology, 39 , 20 - 36 . Eisenberg , R. B. (1969). Auditory behav ior in the human neonate: Functional propert ies of sound and their ontogenetic implications. International Audiology, 8 , 34- 45. Kitchen, W. H. , Rickards, A. L. , Ryan, M . M., Ford , G . W. , Lissenden, J. Y., & Boyle, L. W. (1 986) . Improved outcome to two years of very low-birthweight in fa nts: Fact or artifac t'l Developmental Medicine and Child Neurology, 28, 579588. Korner, A. F. (1 98 1). Sensory responsive ness and soc ial behavior in the neonatal period . In S . L. Friedman & M . Sigman (Eds.) , Preterm birth and psychological development (pp . 207-2 15) . Ne w York : Acade mic Press. Kurt zberg , D . . Vaughan , H. G ., Jr. , Daum , C., Grellong, B. A., Albin , S., & Rotkin , L. (1979). Neurobehav ioral performance of low -birthweight infants at 40 wee ks concepti onal age: Compari son with normal full term infants. Developmental Medicine and Child Neurology, 21, 590- 607. Matheny, A. P. , Jr. , Riese , M. L., & Wilson, R. S. (1 985). Rudiments of infant temperament : Newborn to nine months. Developmental Psychology, 21. 486-494 . Riese , M. L. (1983a) . Assessment of behavioral patterns in neonates. Infa nt Behavior and Development , 6 , 241-246 . Riese , M. L. (1983 b). Behavioral patterns in full-term and preterm twins. Acta Geneticae Medicae et Gemel/ologiae: Twin Research , 32, 209-220 . Riese , M. L. ( 1987) . Longitudinal assess ment of temperament from birth to 2 years: A compari son of full-term and preterm infants. Infant Behavior and Development , 10, 347-363. Rubel, E . W. (1 985). Auditory system development . In G . Gottlieb & N. A. Krasnegor (Eds. ), M easurement of audition and vision in th e first year of postnatal life: A methodological overview (pp . 53-90). Norwood , NJ: Ablex. Ru ff, H. A. , Lawson, K. R. , Kurtzberg, D., McCarton-Daum , C., & Vaughan , H. G ., Jr. (1982). Visual following of mov ing objects by full -term and pre term infants. Journal of Pediatric Psychology. 7, 375- 386. Wall ace , I. F., McCarta n, C. M. , Kurtzberg, D. , & Vaughan, H. G. , Jr. (1988, April). Ne onatalneurobeha vioral p erformance in preterms: Differences over time : Paper presented at the International Conference on Infancy Studies, Washington, DC. Winer, B. J. ( 1971 ). Statistical principles in experim ental design (2nd ed.) . New York : McGraw-Hill .
Received Aug ust 8, 1991