Journal of the American Academy of Child Psychiatry, Volume 23, Issue 1: Page 34-38, January 1984.
MEGAN R. GUNNAR, PH.D, ROBERT O. FISCH, M.D., AND STEVE MALONE
Eighteen, healthy male newborns, 2-5 days old, were subjects in this study of the effects of a pacifier on the newborn's behavioral and adrenocortical responses to circumcision. Half of the subjects were randomly assigned to a condition in which they were encouraged to suck on a pacifier during circumcision, while half served in a no pacifier, control condition. Behavioral observations were made of 1/2 hour before, during, and after circumcision and 30 minutes later. The results showed that stimulating the newborn with the pacifier reduced crying by about 40%. Reducing crying, however, had no significant effect on adrenocortical response. Elevations of serum cortisol predicted average behavioral state following circumcision, whereas crying during circumcision did not. Furthermore, there was evidence that the neonatal adrenocortical system was sensitive in variations in surgical procedures. The results indicate the importance of obtaining data on both behavioral and hormonal systems in studies of stress and coping in human newborns.
Journal of the American Academy of Child Psychiatry, 23; 1:34-38, 1984.
The pituitary-adrenocortical system plays a major role in an organisms adaptation to traumatic, stressful conditions (Mason, 1968, Selye, 1956). In animals and adult humans, measures of adrenocortical activity have proven to be highly sensitive indices of stress (Frankenhaeuser, 1980, Hennessy and Levine, 1979). Recent work with non-human primates also indicates that this neuroendocrine system is sensitive to stressors early in development (see review by Coe and Levine (1981); but little is known about the response to stress in human infants, or the relationship between adrenocortical activity and infant behavior.
Although it was once believed that in humans the neonatal pituitatry-adrenocortical system was relatively insensitive to stress (Gutai et al., 1972; Hillman and Giroud, 1965), more recent work has demonstrated that stressors, such as circumcision, will produce striking elevations in serum cortisol during the first week of life (Gunnar et al., 1981a; Talbert et al., 1976). Measures of adrenocortical activity have also been shown to be correlated with behavioral state in the newborn. Specifically, elevations in serum cortisol have been found to correlate with behavioral distress or crying (Anders et al., 1970; Gunnar et al., 1981a; Tennes and Carter, 1973). This correspondence between crying and adrenocortical activity suggests that stimuli which effectively reduce crying might also effectively modify the hormonal stress response during the newborn period.
To examine this possibility, in the following study newborn males were given pacifiers and were encouraged to engage in non-nutritive sucking during circumcision. The results of a previous study showed that permitting the newborn to suck on a pacifier was effective in reducing crying during this surgical procedure. (Gunnar et al., 1981a). However, because being given a pacifier was not a controlled aspect of that study, too few subjects were given pacifiers to clearly assess the effects of reduced crying on the adrenocortical response to circumcision. Work with non-human primate infants has shown that contact with mother, of which nipple-contact is an important component, not only reduces behavioral stress, but also reduces the infant's adrenocortical response to stressors such as disruption of the social group, capture and handling, and rehousing in novel environments (Coe et al., 1978; Gunnar et al., 1981b). Thus, it was possible that stimuli which effectively reduced crying in newborns might also modify the newborn's adrenocortical response to circumcision.
Subjects and Conditions
The subjects were 18 healthy, male, 2-5-day-old newborns. The subjects averaged 3594 g at birth, had 1-min Apgar scores greater than 7, and were between 38 and 42 weeks gestation. Three were delivered by elective Caesarean section; the remainder were delivered vaginally. Half the infants were randomly assigned to a pacifier condition, in which they were encouraged to such on a pacifier during circumcision, while half were assigned to a no pacifier, control condition. There were no differences between conditions on any of the subject variables.
Parental consent. Parents of healthy newborn males were contacted on the second day postpartum. The purpose and procedures of the study were described and written consent was obtained. Of the 85 males born in the nursery during the course of this study, 46% met the requirements for this study, and consent was obtained from parents of 50% of those infants. Not all of these infants were included in the sample, however, because of problems in scheduling.
Serum Cortisol. Blood samples for serum cortisol determination were obtained immediately before circumcision (pre-session) and 30 min later (post-session). Each sample was obtained from a scalp vein within 5 min (X=124 sec) from the time the newborn was picked up to be sampled. The samples were immediately centrifuged and the serum separated and stored at -20C. Cortisol was measured by radioimmunoassay using the Amerlex cortisol RIA kit (Amershal Corporation). This assay in highly specific to cortisol; however the values obtained reflect some small amount of cortisone (1.6%) and corticosterone (0.6%) activity.
Behavioral Measures. Two observers recorded the newborn's behavior for the 1/2 hours before, during (first to second blood sample), and following circumcision. Before and after circumcision the newborn's behavioral state was recorded every 30 sec using the 6-point scale shown in Table I. Before circumcision the newborn's behavioral state was observed in the nursery. After circumcision the infants were observed while they were with their mothers being fed and comforted. Estimates of inter-observer agreement were calculated in 2 hours and 52 minutes of observation, using 20 pretest subjects. Agreement estimates were calculated in two ways. First, estimates of percent agreement were obtained for each behavioral state. These averaged 85%. Next, average state scores were computed by summing the state scores for each subject and dividing by the number of coding intervals in the observation. The Pearson correlation coefficient for these values was 0.99.
During circumcision, observers recorded state 6 crying every 30 sec, as well as a combined measure of body tension and activity scored on a 3-point scale (1 = quiet, 2 = moderate, 3 = high). A score of 1 or quiet was recorded when the newborn showed little or no movement during the majority of the 30-sec coding interval, and in addition, did not evidence rigid or tense muscle tone. A score of 3 or high activity was recorded if the newborn strained against the circumstraint straps, evidenced rigid muscle tone, and/or moved his head and upper torso vigorously during the majority of the coding interval. A score of 2 or moderate activity was assigned for movement and body tension midway between these two extremes. Observer agreement estimates calculated on 5 test subjects were all above 75% for these measures. It should be noted that the behavioral state scale was not used to score behavioral state during circumcision because previous work indicated that newborns display a mixture of states during this surgical procedure. Finally, in the pacifier condition, observers also recorded sucking (1 = none, 2 = moderate, and 3 = vigorous) every 30 sec.
Table 1 Definitions of Behavioral States State Descriptor Definition 1 Deep Sleep Eyes shut, no rapid eye movements (REMs), regular respiration, no (or minimal diffuse motor activity 2 Light Sleep Eyes shut, occasional REMs, irregular respiration, occasional gross motor activity 3 Drowsy Eyes open and close, eyes look "dull" un- focussed or "heavy," variable activity, spurts of writhing, may focus on source of stimulation, minimal motor movement. 5 Active awake Eyes open but not shiny bright as in alert, high motor activity with thrusting of extremities, may fuss but does not cry for sustained periods. 6 Crying Sustained crying (more than 15 sec)
Circumcision. The newborns were circumcised between 0700 and 1900 hours on the day of discharge. Seven physicians, including four junior residents, performed the circumcisions using three circumcision methods. The three methods were: (1) Plastibell1 (1 pacifier, 1 control), a procedure involving progressive necrosis of the foreskin over several days; (2) Standard Gomco clamp (7 pacifier, 5 control), a procedure involving clamping the foreskin, then waiting 5 to 6 min before removing the foreskin; and modified Gomco clamp (1 pacifier, 3 control), a procedure involving removing the foreskin as soon as the Gomco clamp was secured. The average duration of circumcision was 17.3 minutes (17.7 pacifier; 16.8 control) from the time the newborn was strapped to the circumstraint board until he was taken off the board. Immediately following circumcision the newborn was dressed, swaddled, and put in his crib where he stayed until the second blood sample was taken. This post-circumcision waiting period averaged 12.7 minutes. It should be noted that the adult diurnal rhythm in adrenocortical activity is not present in the newborn and does not establish itself until the second year of life (see review by Hung et al. (1978)). Thus, the different clock times at which blood samples were obtained could not have influenced the results.
Infants in the pacifier condition were given the pacifier to suck on as they were being strapped to the surgical board. An experimenter continued to stimulate them to suck on the pacifier until the second blood sample was taken. Infants in the control condition were not given pacifiers, but were dressed, swaddled, and otherwise soothed as soon as the circumcision was over. It should be noted that circumcision involved the combination of a number of stressors (e.g., physical restraint, tissue damage, and in the present study, venipuncture). It was not the purpose of this study to determine the relative contributions of each stressor to the newborn's pituitary-adrenal or behavioral response.
Prior to circumcision, infants in the pacifier and control conditions did not differ in either average behavioral state (t(13)=1.63,NS)2 or serum cortisol concentration (t(16)=0.21,NS). Before circumcision the infants were in quiescent states (deep sleep, light sleep or drowsy), exhibiting basal serum cortisol concentrations (X ± S.E. =6.7 ± 1.27 µg/dl). There was no significant relationship between different behavioral states in this quiescent range and pre-session serum cortisol levels (Pearson r(13) = 0.006,NS).
Infants in the pacifier condition sucked moderately to vigorously on the pacifier during 49% of the coding intervals while they were strapped to the surgical board, and during 63% of the intervals during the entire period between the 2 blood samples. Stimulation with the pacifier significantly reduced crying. Newborns in the pacifier condition cried during only 46% of the coding intervals while they were being circumcised, as compared to 81% of the intervals for newborns in the control condition, t(16) = 6.95, p<0.01. Newborns in the pacifier condition were also less active during circumcision, than were newborns in the control condition. The percentage of coding intervals during which moderate activity was recorded was 26% (pacifier) versus 5% (control), t(16) = 2.87, p<0.05. A similar difference was noted for quiet or no activity (pacifier = 24%, control = 10%, t(16) = 2.25, p<0.05. High activity almost always co-occurred with crying and was not analyzed separately.
Once the circumcision was over and the newborns were dressed, swaddled and returned to their cribs, the behavioral differences between groups diminished. Neither the average percentage of coding intervals spent crying (pacifier = 19%, control = 35%, t(16) = 0.87, NS), nor the average percentage of quiet activity (pacifier = 48%, control = 34%, t(16) = 1.31, NS) differed significantly by condition during the waiting period between the end of the circumcision and post-session blood sample, when the newborns were with their mothers being fed (pacifier = X ± = 2.23 ± 0.26; control = 2.53 plus minus 0.25, t(14) = 0.83, NS).
Although behavioral differences were observed during circumcision, these differences were not reflected in the post-session serum cortisol values. Post-session values averaged 24.2 ± 1.32 µg/dl for the pacifier group and 24.7 ± 1.60 µg/dl for the control group, t(16) = 0.24, NS. Additionally, there was no evidence that the failure to observe an effect on post-session serum cortisol values was a function of the different circumcision technique employed.3
Measures of Δ-cortisol (post-session minus pre-session values) were used to examine the relationship between adrenocortical activity and individual differences in behavior. Percent crying during circumcision was not significantly related to Δ-cortisol in either condition, pacifier r(7) = 0.25, NS. Average behavioral state following circumcision was positively related to Δ-cortisol for newborns in both conditions, pacifier r(6) = 0.71, p<0.05. However, in neither condition did crying during circumcision predict behavioral state following circumcision, pacifier r(6) = 0.05, NS) and control r(6) = 0.05, NS.
Finally, exploratory analyses were conducted to examine the sensitivity of the behavioral and hormonal measures to differences in circumcision procedures. Because only two Plastibell circumcisions were performed, the effects of this circumcision procedure were not analysed. Instead, responses to two versions of the Gomco clamp procedure were examined. Elevations in serum cortisol differed significantly as a function of procedure, t(14) = 3.01, p<0.01 (t calculated using the formula for small samples and unequal Ns (Spence et al., 1954). The modified procedure produced higher post-session cortisol values 29.0 ± 1.47 µg/dl., N = 4), than the standard procedure (22.6 ± 1.04 µg/dl., N = 12. This effect appeared to be due to procedure, rather than how long the infant was strapped to the circumstraint board. The correlation between post-session serum cortisol and duration of circumcision (strapped down to pick up) was not significant using all of the subjects in the sample, r(16) = 0.10, NS.
Because only one infant in the pacifier condition was circumcised using the modified procedure, crying during circumcision was examined only for infants in the control condition. The values for percent crying completely overlapped and were 71, 79, and 80% for the control subjects circumcised by the Modified Gomco procedure and 65, 80, 83, 92, and 97% for the control subjects circumcised by the Standard Gomco procedure. Following circumcision, however, the modified procedure was associated with more behavioral arousal (X = 3.38 ± 0.19), than the standard procedure (X = 2.05 ± 0.12, t(14) = 5.54, p<0.01 (formula for small samples and unequal Ns (Spence et al. (1954)).
Permitting the newborn to engage in non-nutritive sucking significantly reduced crying and motor activity during circumcision. It is unlikely that these effects were due to response substitution, as newborns in the pacifier condition cried and rejected the pacifier during parts of the circumcision procedure. Nor were these results solely due to stimulation of an incompatible response. While sucking and crying were incompatible, body tension, straining against the circumcision straps, and other signs of distressed motor activity were not incompatible with sucking. These data are consistent with the results of other studiesv which indicate that non-nutritive sucking has a potent calming effect on behavior during the neonatal period (Burroughs, et al., 1978; Kessen and Leutzendorff, 1963).
Although newborns in the pacifier condition showed less behavioral distress than newborns in the control condition, post-session levels of serum cortisol did not differ by condition. Newborns in both conditions evidenced striking elevations in serum corticoids 30 min after the onset of circumcision. The failure to observe an effect of the pacifier condition could not be due to group differences prior to circumcision. Pre-session serum cortisol did not differ by condition. Nor was there evidence that differences in surgical technique masked effects of the soothing procedures on adrenocortical activity.
There are, however, at least three reasons why reductions in behavioral distress may not have been reflected in measures of the neonates' pituitary-adrenocortical response in this study. First, measuring serum cortisol levels 30 min after the onset of circumcision may have been too early to detect an effect of differences in behavioral distress. There is some evidence that differences in the intensity of highly stressful events may be reflected in the duration, rather than in the peak magnitude of the adreno-corticoid response (Vernikos-Danellis and Heybach, 1980). Similarly, Coe and Levine (1981) have reported that manipulations which reduce the infant squirrel monkey's behavioral reaction to maternal separation are not reflected in serum corticoid levels at 30 min but are apparent in levels measured 60 min after the onset of separation. Thus it is possible that measures of serum cortisol obtained at a later time point might have reflected the differences in behavioral distress observed in the Pacifier and Control conditions. However, the fact that the 30-min time point was sensitive to differences in surgical technique make this explanation of the results less compelling.
Second, the reduction in behavioral stress produced by giving the newborn a pacifier may have been too slight to result in any reduction in the newborn's adrenocortical response. This explanation seems very reasonable, but is difficult to reconcile with the results of our previous study which showed a high positive correlation between serum cortisol elevations and equally small variations in behavioral distress (Gunnar et al., 1981a). In that study, however, even though some of the newborns were given pacifiers by the nursing staff, because that was not a controlled aspect of the study, the nurses did not actively attempt to encourage sucking once the newborn became highly distressed. In the present study we encouraged the newborns to suck on the pacifier throughout the circumcision. Thus in the previous study behavioral distress may have been a more direct expression of the amount of endogenous pain or stress the newborn was experiencing, whereas in the present study differences in behavioral stress were due to exogenous stimulation with the pacifier. In short, encouraging the newborn to suck on the pacifier may have masked the behavioral expression of the newborn's underlying physiological state, without calming the newborn sufficiently to produce a change in physiological arousal. This explanations points to the importance of obtaining both behavioral and physiological measures in studies of stress or coping.
Finally, it may well be that stimuli that calm the newborn behaviorally have little effect on the adrenocortical response when the stressor involves pain or tissue damage. Nothing that we were doing to help calm the newborn in any way altered the fact that the newborn was experiencing an apparently painful event that resulted in tissue damage. Under these circumstances activity of the adreno- cortical system may be less affected or unaffected by CNS activity mediating behavioral arousal. Examining the effects of "pacifying" stimuli on the neonates' adrenocortical response to other types of potentially stressful stimuli should provide insights into which stressors are more directly mediated by behavioral arousal during the newborn period.
Even though post-session serum cortisol values did not reflect an effect of the pacifier manipulation, they did indicate that the neonatal pituitary-adrenocortical system was highly sensitive to variations in surgical procedures. Furthermore, the results showed that measures of individual differences in post session adrenocortical levels were capable of predicting behavioral state following circumcision. During the 1/2 hour following circumcision behavioral state was not a function of whether the newborn had been given a pacifier during circumcision, but was related to the magnitude of the newborn's adrenocortical response to the surgery. Newborns who showed higher elevations in serum corticoids were behaviorally more aroused following circumcision when they were with their mothers being fed. A closer examination of this result suggested that is was due to differences in surgical procedures.
Newborns who were subjected to the modified Gomco procedure both showed greater elevations in serum corticoids and were more behaviorally aroused following circumcision than were newborns subjected to the standard Gomco procedures. It is not clear why these effects were observed, however, one explanation may be the rate at which stressful or painful effects of the circumcision occurred. In informal observations we noted that the newborns often showed intense behavioral distress when the Gomco clamp was put on and when it was taken off. While the clamp was in place newborns in both conditions often calmed down. In the modified Gomco procedure putting the clamp on and taking it off occurred in a relative rapid sequence, whereas in the standard version more than 5 min elapsed between these two events. Work with mature organisms indicates that the adrenocortical system responds more vigorously to stressful events that occur at a more rapid rate (see review by Hennessy and Levine, (1979)). These data may indicate that a similar process plays a role in regulating adreno- cortical activity in the human newborn. However the small sample size involved in the comparison makes all interpretations tentative.
Regardless of the explanation of these findings, however, these data suggest that measures of adrenocortical activity are sensitive to variations in stressful events in the newborn period, and provide information about the newborn's response to stressors that may not be detected when only behavioral measures are obtained. Examining both behavioral and adrenocortical responses, thus appears to be a fruitful avenue through which to explore address and coping processes in the human newborn.
Dr. Megan R. Gunnar is an Assistant Professor, and Steve Malone is a doctoral candidate, both at the Institute of Child Development, University of Minnesota. Dr. Robert O. Fisch is Professor of Pediatrics, University of Minnesota. Reprints may be requested from Dr. Gunnar, Institute of Child Development, University of Minnesota, Minneapolis, MN 55455.
The authors would like to express their appreciation to the staffs of Stations 59 and 68 at the University of Minnesota Hospital, without whose help this research would not have been possible.
0002-7138/84/2301-0034$02.00/0 copyright 1984 by the American Academy of Child Psychiatry.
Is Nonreligious Circumcision Necessary?
To the Editor:
The article by Gunnar et al. (1984) is a major contribution to the discussion of circumcision pain. They suggest that although crying during circumcision may be reduced about 40% by using a pacifier, the underlying stress, as measured by adrenocortical response is not diminished.
The study does not mention the more fundamental question: Why is it necessary to perform nonreligious circumcision almost routinely? Every country, with one exception, that adopted routine neonatal nonreligious circumcision has either abandoned the practice or markedly reduced the rate of performance. This may be noted in the present rates - Britain, 1%; New Zealand, 8%; and Canada and Australia, about 30%.
The stress of circumcision should be reduced by abandoning the practice.
Edward Wallerstein, M.D.
[Dr. Wallerstein is the author of Circumcision: An American Health Fallacy (New York: Springer, 1980. and "Circumcision: The Uniquely American Medical Enigma," In: Urological Clinics of North America (Philadelphia: Saunders, 1985).]
To the Editor:
We thank Dr. Wallerstein for his comments on our article. The intent of our work is to understand stress factors and their effects on the newborns, ultimately with an eye to determining the best modes of helping the newborn to cope with stress. With regard to Dr. Wallerstein's fundamental question, "to circumcise or not to circumcise?" we agree. The most effective way to reduce the stress of circumcision would be to abandon the practice.
Megan R. Gunnar, Ph.D.
Robert O. Fisch, M.D.
University of Minnesota
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