Differential sucking by neonates of depressed versus non-depressed mothers

Infant Behavior & Development 27 (2004) 465–476

Differential sucking by neonates of depressed versus non-depressed mothers Maria Hernandez-Reif∗ , Tiffany Field, Miguel Diego Department of Pediatrics, Touch Research Institutes, University of Miami School of Medicine, P.O. Box 016820 (D-820), Miami, FL 33101, USA Received 6 November 2003; received in revised form 5 April 2004; accepted 9 April 2004

Abstract Forty-two neonates (M = 39-h old) of depressed and non-depressed mothers sucked on cold (50 ◦ F) and warm (78 ◦ F) nipples on alternating trials. Half the infants received the cold nipple on the first of the eight trials (20 s each) and the other half received the warm nipple first. Neonates of depressed mothers sucked twice as much as neonates of non-depressed mothers, suggesting arousal dysregulation, overactivity or greater hedonic behavior in the newborns of depressed mothers. Although the newborns did not show a preference for cold or warm nipples, a temperature order effect revealed that neonates who received the cold nipple on the first trial sucked significantly more on trials 2–8 than those who received the warm nipple on the first trial, suggesting that an initially cold nipple might elicit greater sucking. More research is needed on maternal mood effects and temperature of objects to determine how these factors affect neonatal sucking behaviors. © 2004 Elsevier Inc. All rights reserved. Keywords: Neonate; Depressed, sucking, infant

By 12 weeks gestation, human fetuses open and close their mouths in a manner resembling sucking, and by 15 weeks gestation they can be seen sucking their thumb via ultrasound (De Vries, Visser, & Prechtl, 1985; Hepper, Shahidullah, & White, 1991). As the fetus reaches term, regular mouthing movements are observed as well as rhythmical sucking, which is sometimes followed by swallowing (Van Woerden, van Geijn, Caron, van der Valk, & Swartjes, 1988). Full-term healthy newborns display robust sucking within ∗

Corresponding author. E-mail address: [email protected] (M. Hernandez-Reif).

0163-6383/$ – see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.infbeh.2004.04.002

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hours of birth (Mizuno & Ueda, 2001), perhaps because they come into the world with as much as 5–6 months of inutero sucking experience. Although sucking is defined as an automatic behavior or an elicited reflex (Brazelton & Nugent, 1995; Piaget, 1952), sucking behaviors also appear to come under the control of the neonate. For example, when engaged in nutritive sucking (NS), infants suck at a frequency of about one suck per second in an uninterrupted stream (Van Woerden et al., 1988), with swallowing and breathing periods depending on the maturation of the infant (Katsumi et al., 2002; Lau & Kusnierczyk, 2001; Mizuno & Ueda, 2003). In contrast, during non-nutritive sucking (NNS) on pacifiers or fingers, infants suck in bursts or cycles of 3–12 sucks at a frequency of about two sucks per second with brief rest periods between sucking cycles (Finan & Barlow, 1998; Hill & Rath, 1999; Lau & Kusnierczyk, 2001). NNS has calming effects for infants during painful procedures (Field & Goldson, 1984), has been associated with alerting or orienting responses in the young infant (Carpenter et al., 1974; Clifton, 1974; Sameroff, 1973) and has also been observed during quiet sleep (state 1) (Van Woerden et al., 1988). That sucking behaviors vary depending on the nutritive value of the object being sucked suggests that infants may be exploring objects in their mouths and that sucking and mouthing behaviors may underlie infants’ detection of properties and functions of objects. For example, in a study conducted almost four decades ago, three-day-old newborns showed a sucking preference for rubber nipples over rubber tubes (Lipsitt & Kaye, 1965), although it is not clear if the basis for their preference was the substance (i.e., the object’s rigidity or flexibility), the shape of the object, or both. Perhaps the neonates sucked longer on the nipples because these were soft and round and they were attempting to extract nutrients. A study conducted almost two decades after Lipsitt and Kaye’s classic study similarly revealed differential sucking responses by 2- to 3-day-old newborns (half breastfed and the other half bottle fed) for NNS nipples that varied in shape and material (Rochat, 1983). In the Rochat (1983) study, the neonates sucked longer on a round-shaped nipple with an attached brass element than on a standard rubber nipple. In a second Rochat study (1987), 2- to 4-day-old neonates “squeezed” soft objects more than hard objects placed in their mouth, but in contrast “squeezed” hard objects more than soft ones with their hands. Although this paradoxical difference is difficult to interpret, the differential squeezing by neonates suggests that they discerned the hard and soft properties of the objects they were given to mouth or to handle. Interestingly, neonates show more hand-to-mouth than handto-face contacts (Korner & Beason, 1972), and they open their mouth in anticipation of receiving their own hand (Butterworth & Hopkins, 1988), suggesting that they exert some control over their mouthing behaviors. Young infants also show intermodal oral-to-visual matching abilities. That is, after mouthing an object, they appear to visually recognize properties of the object. In one study following sucking on smooth versus nubby nipples, 4-week-old neonates showed that they discriminated these textures when the nipples were presented visually by looking longer at the nipple texture they had sucked (Meltzoff & Borton, 1979). In another study, 30-day-old infants sucked on a soft plastic or a hard lucite object and then were shown an object undergoing a pliable transformation side-by-side with an identical looking object constructed of wood which remained rigid when manipulated (Gibson & Walker, 1984). In this study, the infants showed a visual preference for the substance they had not sucked, unlike in the Meltzoff and Borton study (1979). Nevertheless, that the infants invariably showed a preference for one over the other substance suggests that they transferred substance information across oral touch and sight. That is, from simply mouthing an object young infants seem to abstract and transfer to the visual mode information about the tactile properties of the object. However, because the infants in these studies were about one month of age, it is

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difficult to determine if their cross-modal transfer abilities related to experiences they made have already acquired with similar object properties. In the current study we recruited newborn infants of depressed and non-depressed mothers and assessed their sucking on cold and warm nipples before they left the hospital nursery. We expected that the neonates of depressed mothers would suck less than the neonates of non-depressed mothers because in a previous sucking study, in which neonates received alternating smooth or nubby rubber objects (page-turner-fingertips) to suck, the neonates of depressed mothers sucked 50% less than the neonates of non-depressed mothers (Hernandez-Reif, Field, Del Pino, & Diego, 2000), and in other perceptual hand studies, the neonates of depressed mothers show less developed motor skills (Hernandez-Reif, Field, Diego, & Largie, 2001, 2003). In the current study, we also hypothesized that both groups of neonates would detect the temperature differences of the nipples because in our neonatal study on temperature perception-by-hand, the neonates of both depressed and non-depressed mothers differentiated cold and warm tubes (Hernandez-Reif et al., 2003).

1. Method 1.1. Participants Mothers who had delivered a singleton neonate (mean hours = 39, S.D. = 20, range: 10–108 h) at the university hospital’s newborn nursery were approached to obtain informed consent to have their baby participate in the temperature study. Consenting mothers were interviewed, and medical records were reviewed. Exclusion criteria included self-report of (1) HIV/AIDS status, (2) other prenatal medical conditions (toxemia, hypertension, diabetes), (3) drug, alcohol or illicit drug use during pregnancy, and (4) psychiatric conditions other than unipolar depression. Inclusion criteria for the infants included (1) born full term (>37 weeks gestation), (2) Apgar scores >7 at 1 and 5 min and (3) appropriate for gestational age (AGA). Infant exclusion criteria included surgery, postnatal complications, anomalies, metabolic disturbances, or medications other than vitamins. After meeting the inclusion/exclusion criteria, the mother was given the CES-D depression scale (see the following for description). A total of 44 mothers (half scoring at or above the cutpoint for depressive symptoms) who consented to having their infants tested and who met criteria were recruited. However, the final sample size consisted of n = 22 newborns of depressed and n = 20 newborn infants of non-depressed mothers as two neonates born to non-depressed mothers did not suck on the nipples. 1.2. Procedure 1.2.1. Assessments The Obstetric Complications (OCS) and Postnatal Complications Scales (PNF) (Littman & Parmelee, 1978) were completed using the infants’ and mothers’ medical records to assess the optimality of the labor and delivery and the neonate. The OCS includes 41 events related to the mother’s health, infant’s gestation, birth, and postnatal events, as well as additional treatment events. Events are scored as optimal or nonoptimal, with summary scores providing an index of the optimality of the pregnancy. The OCS includes Prenatal (22 items), Obstetric (13 items) and Neonatal (6 items) subscales. Examples of non-optimal items for the Prenatal subscale include infections, bleeding during pregnancy, albuminuria, hyperemesis,

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hemoglobin levels under 10 and Rh Antagonism. Non-optimal items for the Obstetrics subscale include duration of first stage of labor <3 or >20 h, duration of second stage of labor <10 or >120 min, fetal heartrate during labor <100 or >160/min, knotted cord and placenta previa or abruption. Less optimal Neonatal items include resuscitation, Apgar scores under 7 at 1 and 5 min, and unstable respiration after 6 min of birth. The PNF includes 10 items and also yields a summary score to rate the optimality of the perinatal period. The items include respiratory distress, infections, ventilator assistance, illness or anomaly, metabolic disturbance, convulsion, temperature disturbance, not feeding within 48 h and surgery. The Center for Epidemiological Studies Depression Scale (CES-D; Radloff, 1977) is a self-report 20-item scale designed to assess depressive symptoms in the general population. The mother answers questions relating to depressive symptoms experienced during the last seven days (including today) on a Likert scale of 0 (never, rarely) to 1 (sometimes) to 2 (often) to 3 (most of the time). Characteristic questions include decreased eating, crying spells, difficulty concentrating, feeling depressed, lonely or sad, restless sleep, and thinking that life had been a failure. CES-D scores range from 0 to 60, with a score of 16 being the cutpoint for depressive symptoms. Infants whose mothers scored 16 or higher on the CES-D were assigned to the depressed group, and those whose mothers scored between 3 and 12 were assigned to the non-depressed group. None of the mothers scored in the faking good range (0–2) or in the borderline range (13–15) (Scafidi, Field, Prodromidis, & Abrams, 1999). The CES-D has been found to correlate with the Beck Depression Inventory (BDI) (Wilcox, Field, Prodromidis, & Scafidi, 1998) and with the Diagnostic Interview Schedule (DIS) (Weissman, Prusoff, & Newberry, 1975), it has acceptable psychometric properties (Carpenter et al., 1998; Roberts, 1980), and has been validated with various ethnic groups, including Hispanic and African American mothers (Walker, Timmerman, Kim, & Sterling, 2002). 1.3. Nipples Sanitized Gerber Nurser rubber nipples (Product No. 76433) detached from their bottles served as the stimuli for this study. Nipples were individually stored in small sterile plastic containers filled with 3 oz distilled water. Half of the containers were placed in a freezer at a temperature of −20 ◦ F over night, and the other half were left at room temperature (78 ◦ F) to comprise the “cold” and “warm” nipples, respectively. Prior to testing, the “cold” nipple containers were removed from the freezer and transferred to a small cooler, while the “warm” nipple containers were placed in a plastic bag separate from the cooler. The cold nipples were thawed to approximately 50 ◦ F prior to testing. 1.4. Temperature detection task Testing occurred between 11.00 a.m. and 3.00 p.m. in a small, quiet hospital room. This time was chosen because by that time the attending physicians had completed their rounds and there were fewer interruptions since the infants were between feedings and the mothers were finished with their activity classes (breastfeeding, learning to bathe the baby, etc). The experimenter who recruited and screened the mothers and infants for eligibility rolled the newborns in their bassinets to a small hospital room where two other experimenters, blind to the infant’s group assignment, received the infant and conducted the testing. One of the two test experimenters (Experimenter “A”) presented the cold and warm nipples and the other experimenter who was blind to the order of

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the temperature presentation (Experimenter “B”) recorded infant sucking. Prior to testing, the bassinet mattress was positioned at a 45◦ angle so the infant was in a semi-upright supine position. If the neonate was sleeping, an attempt was made to awaken the infant by giving the habituation items of the Neonatal Behavior Assessment Scale (NBAS) (Brazelton & Nugent, 1995) (shaking a rattle, ringing a bell). Most sleeping infants were successfully awakened with these NBAS items. A few infants who could not be awakened were returned to the nursery. Second attempts to awaken the sleepy infants 30–45 min after the first attempts were successful except for the two infants who did not suck and were omitted from the study. With the infant supine and drowsy (state 3) or quiet alert (state 4), Experimenter “A” wearing a latex glove pushed her middle or index finger through the back of the nipple, securing it to her finger, and then inserted the nipple into the infant’s mouth. (No infant was tested in sleep (states 1 and 2) or active/agitated alert (state 5) or crying (state 6) states.) One nipple was presented at a time, alternating for eight trials between the cold and warm nipple so that each infant experienced four trials of a cold nipple and four trials of a warm nipple. Neonates received new nipples on each trial to preserve their distinct cold and warm temperatures throughout the procedure. Half of each group (depressed and non-depressed) was assigned to receive the cold nipple on trial one and the other half to receive the warm nipple first. Each trial lasted 20 s and was timed with a stopwatch. Experimenter “B” initiated the trial with the infant’s first suck. Experimenter “B” then silently counted and recorded the number of infant sucks for the duration of each 20-s trial. A suck was operationally defined as one discrete up and down jaw movement. To test reproducibility, initially several practice trials occurred with Experimenter “B” counting the number of sucks out loud while Experimenter “A” monitored the number of times the neonate sucked. For 26% of the participants tested, a second trained observer silently recorded number of sucks to obtain interobserver reliability, which was very high (Pearson’s correlation = .997). 1.5. Dependent measure From Experimenter B’s recordings, total sucks were calculated for each infant for the following measures: (1) the four cold trials; (2) the four warm trials; (3) the first two trials; (4) trials 3 and 4; (5) trials 5 and 6; (6) the last two trials; and (7) all eight trials of the procedure (1–8). The scores were then averaged to obtain mean total sucks for measures 1 through 7 for each group (see Table 2). Measures 1 and 2 were used to examine the neonates’ preference and/or discrimination for cold versus warm rubber nipples. Measures 3–6 provided descriptive data over time. Measure 7 examined whether the groups differed on total sucks across the procedure.

2. Results 2.1. Demographic variables Chi-square and t-tests revealed no differences between the depressed and non-depressed mothers and their infants on the demographic variables (see Table 1). The mean CES-D score for the depressed mothers was 21.5 (S.D. = 5.2) and 8.3 (S.D. = 2.7) for the non-depressed mothers, t(40) = 10.19, p < .01 (Table 1).

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Table 1 Demographic data (standard deviations in parentheses) Variables

Depressed

Non-depressed

p-values t

Mothers Age (years)

25 (6)

24 (4)

10 12

11 8 1

SES (Hollingshead) Middle Lower-middle

3 19

3 17

Obstetric complicationsa

103 (22)

101 (18)

.82

41 (23)

36 (15)

.35

Gender Males Females

9 13

12 8

Postnatal complicationsa

150 (21)

148 (23)

Ethnicity Hispanic Black Caucasian

Infants Age (hours old)

a

χ2

.41 .34

.50

.22

.81

Higher score is optimal.

2.2. Temperature and group effects A 2 (temperature order: cold versus warm first) by 2 (group: depressed versus non-depressed) repeated measures ANOVA with trials (trials 1–8) as the repeated measure, temperature order as the within-group factor and group as the between-subject factor revealed a significant temperature order effect, F(1, 36) = 9.85, p < .01 and a depressed/non-depressed group effect, F(1, 36) = 5.43, p < .05, but no interaction or trial effects. The temperature order effect suggested that when presented with the cold nipple first, newborns sucked more on all but the first two trials (see Fig. 1). The group effect suggested greater sucking by newborns of depressed mothers (see Fig. 2). Means are presented in Table 2 for temperature and group effects.

2.3. Perception of cold versus warm To address the question of whether neonates discriminated the cold from the warm nipples, paired sample t-tests were conducted for the depressed and for the non-depressed groups separately comparing total sucks on the four trials with the cold pacifier to total sucks on the four trials with the warm pacifier. The analyses revealed no temperature preference by either group (see Fig. 3).

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Table 2 Sucking measures (and standard deviations in parentheses) for infants who received the cold vs. the warm nipple to suck on the first trial (temperature effects), irrespective of mothers’ depression and for infants of depressed vs. non-depressed mothers (group effects) Measures

Cold 1st

Warm 1st

F-value

p-value

Temperature effects Total sucks on the four cold trials Total sucks on the four warm trials Total sucks on trials 1 and 2 Total sucks on trials 3 and 4 Total sucks on trials 5 and 6 Total sucks on trials 7 and 8 Total sucks on trials 1–8

67.5 (29.6) 59.4 (30.0) 27.4 (16.4) 31.4 (16.7) 31.0 (16.7) 34.4 (16.3) 123.3 (55.5)

36.3 (23.3) 36.5 (26.3) 19.8 (13.7) 16.7 (8.3) 17.9 (14.5) 18.9 (15.6) 72.4 (45.3)

14.42 6.78 2.60 12.55 7.36 9.88 10.09

.01 .01 .115 .001 .01 .01 .01

Depressed

Non-depressed

62.0 (31.4) 57.0 (31.2) 30.6 (16.4) 29.5 (16.4) 29.3 (18.6) 30.5 (17.2) 117.8 (61.8)

42.4 (27.0) 39.1 (26.9) 16.2 (10.2) 18.7 (11.8) 19.9 (13.4) 23.1 (17.7) 77.9 (42.9)

4.71 3.95 11.43 5.91 3.47 1.89 5.62

.05 .05 .01 .02 .07 .18 .02

Group effects Total sucks on the four cold trials Total sucks on the four warm trials Total sucks on trials 1 and 2 Total sucks on trials 3 and 4 Total sucks on trials 5 and 6 Total sucks on trials 7 and 8 Total sucks on trials 1–8

Fig. 1. Temperature order effect (cold vs. warm 1st) on neonatal sucking.

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Fig. 2. Group effect (depressed vs. non-depressed) on neonatal sucking.

2.4. Depression severity effects Finally, a correlation analysis was performed on the sucking measures and severity of depression. The analysis revealed a significant correlation between maternal depression scores and neonatal sucking, r(42)

Fig. 3. Sucking to cold vs. warm nipples by newborns of depressed vs. non-depressed mothers.

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Fig. 4. Total sucking to cold vs. warm pacifiers by neonates based on their mothers’ depression severity (CES-D score).

= .40, p = .005. Fig. 4 depicts the relation between neonatal sucking and maternal depression, based on maternal depression severity.

3. Discussion In this study we expected that newborns would show differential sucking for a cold versus a warm nipple based on findings that neonates discriminated cold from warm objects with their hands (HernandezReif et al., 2003) and because an object’s temperature might be discernible from oral contact because the oral cavity is particularly densely innervated. However, contrary to our hypothesis, neonates showed comparable sucking on cold and warm bottle nipples suggesting that (1) they did not distinguish cold from warm, or (2) they did detect the temperature difference, but did not have a preference for sucking one over the other nipple. The second explanation is perhaps more plausible given that neonates perceive other aspects of objects by mouth (Hernandez-Reif et al., 2000; Lipsitt & Kaye, 1965; Meltzoff & Borton, 1979; Rochat, 1987). Alternating between the cold and warm nipple might have confused infants and removing the nipple every 20 s might have also impaired their temperature perception. Additionally, any soft rubber nipple might elicit sucking thus interfering with the temperature perception task. A future study might use hard substances or elongated shapes, such as rubber tubes that are less likely to elicit continuous sucking. Also, to be more accurate, future studies should include video recordings or electrical assessments of the mouth movements.

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Differential sucking for neonates of depressed versus those born to non-depressed mothers was also examined in the current study. We hypothesized that neonates of depressed mothers would show less sucking because they have been documented to be more inhibited and less active and exploratory (Field, Diego, Hernandez-Reif, Schanberg, & Kuhn, 2002; Hart, Jones, Field, & Lundy, 1999) and sucked less in a previous texture-detection-by-mouth study (Hernandez-Reif et al., 2000). Contrary to our hypothesis, the neonates of depressed mothers in the current study sucked more than the neonates of non-depressed mothers. The reason for the greater sucking in this study is unknown. The testing was conducted in between feedings so it is unlikely that infant hunger played a role in sucking. However, the infant’s behavioral state might have played a role. A future study might examine non-nutritive sucking (NNS) or sucking and swallowing differences by neonates of depressed versus non-depressed mothers during a longer period (e.g., 1.5 h) to capture the neonates’ sucking responses across varying behavioral states. Perhaps the lesser sucking by the neonates of depressed mothers in the earlier texture study (HernandezReif et al., 2000) and the greater sucking by neonates of depressed mothers in the current study relates to the properties of the objects. That is, the soft nipples in the current study might have elicited more sucking, and the nubby fingertips in the previous study might have elicited less sucking. Alternatively, the neonates’ sucking responses might relate to the degree of attractiveness, “hedonics,” or pleasure that the stimulus offers (Crook & Lipsitt, 1976). Perhaps the neonates of depressed mothers found greater pleasure than the neonates of non-depressed mothers in sucking the warm and cold rubber nipples. However, it is unclear why the sucking pattern in the earlier and current studies by the neonates of depressed mothers differed from the sucking pattern displayed by neonates of non-depressed mothers. Another explanation is that perhaps neonates of depressed mothers are more reactive or tend to show extreme behaviors (more or less sucking). In any case, object properties that regulate neonatal sucking behaviors should be explored, especially with infants who have sucking difficulties or aberrant sucking. The size and shape of stimuli have been reported to affect sucking responses (Gunther, 1961). Perhaps the temperature of the stimuli also affects sucking. For example, introducing a cold nipple prior to feeding might facilitate greater suckling by neonates with difficulty feeding and should be examined. Another interesting and unexplained finding from the current study was that greater neonatal sucking was related to greater maternal depression. Greater non-nutritive sucking (NNS) by newborns of depressed mothers might suggest a greater need for pacifying or comforting or perhaps is a sign of arousal dysregulation, overactivity or elevated sensory threshold (such as needing to suck more for greater stimulation). Previous studies have reported that neonates of depressed mothers have dysregulated biochemistry levels (higher cortisol and norepinephrine levels and lower dopamine) (Field et al., 2002; Lundy et al., 1999). Although in this study we did not measure neonatal biochemisty, it is possible that these might also affect neonatal sucking behaviors. These questions need further exploration. Finally, the unexpected temperature order effect (irrespective of maternal depression) is compelling but difficult to untangle in that neonates who received the cold nipple on the first trial sucked more than newborns who received the warm nipple first, although the cold nipple did not lead to greater sucking on the first trials or on average trials. Perhaps the cold nipple aroused the infants who received it first, resulting in greater sucking for this group over trials. Alternatively, this could be a chance finding that cannot be explained. A future study might compare whether providing infants with only cold nipples (versus only warm nipples) results in differential sucking. If the temperature of a nipple affects sucking behaviors, this would be important to document especially for infants with sucking difficulties, such as preterm infants. The findings and questions raised in this paper will hopefully continue to draw attention to research on neonatal sucking behaviors.

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Acknowledgements We thank the mothers and newborns who participated in this study and the nursing staff at Jackson Memorial Children’s Hospital in Miami, Florida. We also thank Julia Beutler and Shay Largie for their assistance with recruitment and data collection. This research was supported by an NIMH Senior Research Scientist Award (#MH00331) and an NIMH Research Grant (#MH46586) to Tiffany Field.

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