Health Psychology 2000, Vol. 19, No. 6, 560-567
Copyright 2000 by the American Psychological Association, Inc. 0278-6133/00/$5.1)0 1301:10.1037//I)278-6133.19.6.560
Oxytocin Responsivity in Mothers of Infants: A Preliminary Study of Relationships With Blood Pressure During Laboratory Stress and Normal Ambulatory Activity J a n e t A, A m i c o University of Pittsburgh School of Medicine
K a t h l e e n C. Light, T a r a E. S m i t h , J o s e p h i n e M . J o h n s , K i m b e r l y A. B r o w n l e y , a n d Julie A. H o f h e i m e r University of North Carolina at Chapel Hill
The neuropeptide oxytocin (OT) enhances maternal behavior and decreases blood pressure (BP) and stress responses in animals. Thus, the relationship of OT responsivity to BP in 14 breast- and 11 bottle-feeding mothers of infants was examined. Laboratory BP was assessed during baseline, speech preparation, active speech, and recovery on 2 days, 1 in which baselineand speech were separated by 10 min of baby holding and the other by no baby contact. SystolicBP reactivityto speech was lower after baby contact. PlasmaOT changefrom baselineto speech after baby contactdefinedOT increase,minimal OT change, and OT decrease groups. OT increasemothers were primarilybreast-feeders, and they had lower BP throughoutboth stress sessions and after baby feedingat home than OT decrease mothers, who also had greater BP reactivity to preparation and recovery. These results suggest that oxytocin has antistress and BP-loweringeffects in humans. Key words: oxytocin,breast-feeding,blood pressure, stress
pressure (BP) and stress responses are well documented in animal models but less well established in humans (Carter, 1998; Carter, Devries, & Getz, 1995; Insel, 1997; Keverne & Kendrick, 1997; Pedersen, Ascher, Monroe, & Prange, 1982; Uvnas-Moberg, 1998a, 1998b). In rats, administration of oxytocin or natural oxytocin released by stroking leads to decreases in both BP and cortisol levels and to diminished distress behavior (Agren, Lundeberg, Uvnas-Moberg, & Sato, 1995; Uvnas-Moberg, Atdenius, Hillegaart, & Alster, 1994). After 5 days of dally oxytocin injections to rats, BP reductions of 10 to 20 mm Hg persist for 1 to several weeks, even though the plasma half-life of oxytocin is minutes (Uvnas-Moberg, 1998a, 1998b; Petersson, Alster, Lundeberg, & Uvnas-Moberg, 1996a, 1996b). Although the short-term effects on BP may be primarily due to direct effects of circulating oxytocin on the vasculature, these long-term physiological and behavioral effects have been related to increased central a 2adrenergic activity (Petersson, Uvnas-Moberg, Erhardt, & Engberg, 1998). In humans, the evidence linking oxytocin to lower BP or reduced stress responses is limited, and most studies have used the indirect proxy of breast-feeding rather than examining oxytocin measures directly. Breast-feeding mothers tested at 1 month postpartum showed less anxiety than botfle-feeders (Virden, 1988). In women who use both feeding methods, selfreported anxiety, depression, stress, and guilt were lower when assessed after breast-feeding (a potent elicitor of oxytocin release) than after bottle-feeding (Modahl & Newton, 1979; Heck & deCastro, 1993). The act of breast-feeding has also been shown to suppress cortisol responses in women (Amico, Johnston, & Vagnucci, 1994). Suppression of stress-responsive
The early months after an infant's birth are widely accepted as a stressful period for the mother, associated with increased demands on her time and energy to meet the infant's needs, unsetfling changes in daily routines, and sleep deprivation (Brazelton & Crarner, 1990). Some mothers, however, show better physiological and psychological responses than others during this stressful period. Although many factors contribute to these response differences, one promising biological factor that may relate to improved functioning is oxytocin. Oxytocin is a mammalian hypothalamic neuropeptide that is released into the circulation to influence many organs and tissues, including multiple areas of the brain itself. Although produced in both genders, its best known functions relate to milk ejection during breast-feeding and enhancing uterine contractions during childbirth. Other roles, such as facilitating maternal behavior and pair bonding and, most relevantly, reducing blood
Kathleen C. Light, Tara E. Smith, Josephine M. Johns, Kimberly A. Brownley, and Julie A. Hofheimer, Stress and Health Research Program, Department of Psychiatry, University of North Carolina at Chapel Hill; Janet A. Amico, Department of Pharmaceutical Sciences, University of Pittsburgh School of Medicine. This research was supported in part by National Institutes of Health Grants HL31533, HL64927, DA08456, RR00046, and MH33127. This research could not have been completed without the technical skills and assistance of Sunny H. Chung and Monica Adamian and the secretarial support of Dot Faulkner. Correspondenceconcerningthis article shouldbe addressed to Kathleen C. Light, CB# 7175, Medical Research Building A, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7175. Electronic mail may be sent to
[email protected]. 560
SPECIAL SECTION: OXYTOCIN, STRESS, AND BLOOD PRESSURE h o r m o n e s during exercise stress has also been reported in breast-feeding mothers (Altemus, Deuster, Galliven, Carter, & Gold, 1995), Reduction of stress responses m a y improve maternal care o f the young by conserving the m o t h e r ' s energy, preventing stress-related decreases in milk production and release, and diminishing fear responses that could interfere with maternal protective behaviors. Oxytocin is cited as a probable mediator o f these effects (Uvnas-Moberg, 1998a, 1998b), although the relationship of oxytocin response to reduced stress responses in mothers of infants has not previously been directly confirmed. In part, this lack of studies directly relating oxytocin to stress responses in human mothers is due to the difficulty of assessing oxytocin activity. Central nervous system levels of oxytocin assessed by spinal taps cannot be obtained during normal motherinfant interactions and also impose potential risks. Plasma levels of oxytocin are readily accessible; however, because oxytocin centrally has a pulsatile release pattern in response to specific stimuli like breast-feeding or sexual activity, basal plasma oxytocin levels may not reflect the individual's oxytocin respousivity. Turner, Altemus, Enos, Cooper, and McGuinness (1999) proposed that oxytocin changes from baseline levels in response to specific sfimufi may more directly test oxytocin responsivity. They found that basal plasma level of oxytocin in nonlactating women had a paradoxical relationship to distress; higher levels, not lower levels, were seen in women reporting greater interpersonal distress. In contrast, changes in oxytocin from baseline levels during massage and imagery tasks demonstrated the expected relationships with lower distress and more positive mood. W o m e n with greater oxytocin increases while imaging a positive attachment experience and lesser oxytocin decreases while imaging a negative separation experience reported less anxiety and interpersonal problems than other women. Thus, the present study examined BP responses in 25 mothers of infants during laboratory stress sessions and during normal daily activities. W e tested the hypothesis that mothers who were higher oxytocin responders demonstrate lower overall B P levels and reduced B P reactivity while actively giving a speech about a recent interpersonal conflict or during the periods before or after the speech. Oxytocin responsivity was defined as the change in plasma levels from noncontact baseline to levels during the speech immediately after 10 rain of baby holding. It was expected that the recent baby contact would enhance oxytocin increases evoked by the speech stressor. This expected outcome was tested by comparing oxytocin responses of the same mothers to the same speech stressor on a second day when the speech task followed a neutral rest with no baby contact, with the order of baby contact and no baby contact testing days counterbalanced. BP responses on the baby contact and no baby contact days were also compared. This was to assess whether any beneficial BP reductions would be limited to periods soon after recent contact or whether they were more long lasting, similar to the BP reductions observed in rats after daily oxytocin injections (Uvnas-Moberg, 1998a, 1998b). The hypothesized relationship of higher oxytocin responsivity to lower B P during real-life activities of the mothers was also examined through 24-hr ambulatory BP monitoring in their home environments. During ambulatory monitoring, special attention was paid to the time period immediately after baby feeding, when many
561
mothers (especially breast-feeders) would normally have increased oxytocin release. Method Participants This study recruited and tested 26 mothers (14 breast-feeding, 12 bottlefeeding), ages 20 to 42 years. One bottle-feeder was excluded from analysis because of technical problems. Of the final 25 participants, 18 were White and 7 were Black. All were recruited to participate in a study investigating hormone and BP responses to lab and home events in mothers of infants through written advertisements in the university and surrounding communities. Each volunteer read a description of the protocol, which was approved by the local review board, and provided written informed consent. Women who currently used a combination of breast- and bottlefeeding were excluded as were those who switched feeding methods in the past month. Medical history information provided by each individual was used to exclude any person having an average resting systolic BP (SBP) or diastolic BP (DBP) greater than 160 and 95 mm Hg, respectively, serious cardiovascular, renal, or pulmonary problems, or chronic physical or psychological disorders or using antihypertensive or other prescription medications at screening. Participants were paid for their participation. Protocol Each participant attended an initial 45-min screening session (when they were evaluated for study eligibility and provided consent to participate) and two consecutive morning laboratory test sessions, one with and one without the baby (baby contact vs. no baby contact). The order of these sessions was counterbalanced across participants. Between the first and second lab test sessions, the mother underwent 24-hr ambulatory BP monitoring. On the first test session, the protocol began with fitting the mother with the Accui~acker II ambulatory blood pressure monitor (Suntech, Raleigh, NC), which provided all in-lab as well as ambulatory BP readings. Previous studies by our research group have confirmed that BP readings with the Accutracker monitor correlate highly with both direct arterial BP and standard auscultatory BP readings (Light, Obrist, & Cubeddu, 1988) and that the monitor can be used to track BP variations during normal work and home activities in both women and men (Brownley, Light, & Anderson, 1996). In the present study, manually initiated readings at intervals timed by a stopwatch were used for the two lab sessions, and automated readings using the programmable software of the monitor were used for the ambulatory monitoring. The monitor's SBP and DBP determinations obtained in both seated and standing postures were compared against auscultatory levels simultaneously obtained by a trained staff member with a stethoscope on both test days to ensure comparability within 5 nun Hg against standard clinical readings. No baby contact test day. Mothers were instructed not to bring their infant with them for this appointment and to allow a minimum of 1 hr to elapse between their most recent baby feeding and their arrival for testing to minimize carryover effects of recent nursing. After the BP monitor was in place and functioning well, a 12-rain baseline period occurred in which BP determinations were obtained every other minute, with three readings in the seated position and three in the standing posture. These six BP readings were averaged to serve as a baseline. At the end of baseline, a blood sample was drawn for baseline plasma oxytocin determinations. Baby contact test day. Mothers brought their infant with them on this day, but the baby was placed in a carder or stroller and watched by a staff member &wing instrumentation and baseline. After the same baseline BP determinations as were obtained on the no baby contact day, a 10-rain period of physical contact, semistruetured play, and cuddling followed between the mother and her infant. First, the mother sat on a couch holding her baby on her lap, and she was asked to interact with the baby just as she
562
LIGHT El" AL.
normally would, except that no nursing or feeding was permitted until after all study procedures were done. A standardized set of age-appropriate toys was available to the mother for use in play with her baby; some used these toys and others did not. This unstructured interaction period was followed by a semistructured interaction. During this phase of baby contact time, the mother was asked to read a small book, The Little Book of Hugs (Wiesinger, 1990), to her baby. This book was selected because it provided many opportunities for the mother to cuddle and physically interact with her baby. The baby was then taken from the room by a lab assistant to allow the mother to be alone as on the no baby contact day to perform the speech task. Some infants were calm but alert, others drowsy, and still others fussy during the interaction period; however, no relationship between these three baby states and the mother's oxytocin response was seen. Speech stressor. Similar stress testing followed the period of motherinfant interaction on the baby contact day versus the rest alone control condition on the no baby contact day. Participants performed the same type of speech on both lab test days but spoke about a different stressful experience each day. The participant was given 2 rain to prepare a speech about a recent anger-arousing or stressful incident, with BP determined during Minute 2 of the preparation period. She was then told to speak for 3 rain, describing the incident, the people involved, how she dealt with it, her feelings about the outcome, and her level of satisfaction with the outcome. The speech was tape-recorded. The tape was then rewound and played for the participant, who was asked to listen while she recovered and to think about how effective she was in explaining her reasons for feeling angry or stressed. Replay of the tape was used to slow recovery of BP, encouraging maladaptive poststress rumination behaviors. BP readings were taken during Minute 2 of the preparation period, during Minute 1 and Minute 3 of the active speech, and during Minute 1 and 3 of the tape replay/recovery period. A blood sample was drawn in Minute 2 of active speech to assess plasma oxytocin levels to this stressor on both the baby contact and no baby contact days. This involved a separate venipuncture from the baseline sample, because an indwelling arm catheter might interfere with normal mother-infant interactions on the baby contact day. On the baby contact day, the infant was brought back to the mother after completion of the speech task. On the first test day, the mother then was instructed about the 24-hr ambulatory BP monitoring, particularly about the importance of completion of the diary page for each BP reading. The mother then left the lab wearing the ambulatory BP monitor and returned the next morning still wearing the monitor, when the second lab session occurred. Ambulatory monitoring. The participants continued to wear the Accutracker II monitor for the 24-hr ambulatory BP monitoring period spent at home and at the workplace for mothers who worked outside the home. The monitor was programmed to obtain a BP determination four times per hour while the participant was awake and two times per hour during sleep. Each waking reading was accompanied by an entry in a diary on current posture, location, consumption, physical exertion, current activity, mood state (nervousness, depression, happiness, and irritation levels), whether baby feeding or holding had occurred since the last reading, and whether the baby was crying. The ambulatory BP data were divided into three categories and mean levels calculated for these categories for subsequent analysis: (a) readings during sleep, (b) readings during and for 1 hr after baby feeding (nursing or bottle-feeding), and (c) all other waking readings.
Hormone Assays To assess plasma oxytocin levels, blood was drawn continuously into chilled tubes containing sodium beparin, kept on ice, and centrifuged to separate plasma within a few minutes after collection. Plasma was pipetted into tubes, rapidly frozen, and maintained at - 8 0 °C until assayed. The oxytocin assays were performed in the laboratory of Dr. Janet Amico of the University of Pittsburgh, following published methods (Amico et al., 1985; Amico, Seif, & Robinson, 1981). For assay of oxytocin in plasma, a starting volume of I ml was extracted using the acetone-ether method and
assay methods previously described from this laboratory. Plasma, 1 ml, was mixed with two volumes of acetone, and the supernatant was saved and washed with two volumes of anhydrous ether. After the ether phase was removed, the remaining extract was air dried and reconstituted in 500 p,i of 0.01 mol potassium phosphate with added sodium chloride (NaCl), bovine serum albumin (1 mg/ml), and sodium azide (1 mg/ml). Duplicate 200-/,1 aliquots were assayed for oxytocin. The antiserum to oxytocin (Pittsburgh antibody 2) is specific for oxytocin and was generated in rabbits. Its characteristics have been previously published (Amico et al., 1985). The final dilution of the oxytocin antiserum in the assay was 1:125,000. The antiserum has less than 1% cross-reactivity with arginine vasopressin or arginine vasotocin. Synthetic oxytocin (Bachem, Torrance, CA) was used in the standard curve. The standard curve was linear between 0.5 and 10 pg/tube, and the minimal detectable oxytocin concentration in extracted plasma was 0.5 pg/mi. For the assay, samples were incubated for 24 hr at 4 *C with 50 p,l of the diluted antiserum and 2,500 cpm (50 p~l) of iodine 125 oxytocin (New England Nuclear) followed by additional incubation for 5 days. Antibody-bound oxytoein was separated using gamma globulin and 25% polyethylene glycol. The sediments in each tube were counted in a gamma counter. Samples from participants in an experimental condition were assayed simultaneously. The intraassay coefficient of variation was 6.5%, and the interassay coefficient of variation was 8%, both of which were determined by assaying multiple replicates of charcoal-stripped plasma enriched with synthetic oxytocin at relevant concentrations in the standard curve. Recovery of oxytocin from exogenously enriched charcoal-treated plasma is 75% +__ 3%. Oxytocin levels are reported corrected for recovery.
Classification of Participants for Analysis Oxytocin response (the change in oxytocin from baseline to the speech) was determined on both the baby contact and no baby contact days. Approximately equal numbers of participants showed increases versus decreases versus minimal changes from baseline on both days. Although the participants' oxytocin responses across days were significantly correlated (Pearson r --- +0.56, p < .005), indicating moderate stability of stress-evoked responses despite the protocol differences, oxytocin increases were larger on the baby contact day. Thus, we defined oxytocin responsivity based on changes from baseline to speech on the baby contact day, when baseline was followed by baby holding and then the speech, merging effects of baby holding with effects of the stressor. Changes from baseline in plasma oxytocin on the baby contact day ranged from - 2 to +4 pg/mi. Cutpoints separating participants into the low, moderate, and high tertiles for oxytocin responsivity were then determined (n - 9, 8, and 8, respectively). Because the tertile of high responders all showed increases from baseline greater than 0.40 pg/ml, whereas the tertile of low responders all showed decreases from baseline greater than 0.25 pg/ml and the middle tertile showed very small increases or decreases falling between these cutpoints, these high- to lowresponsivity groups in effect separated participants into oxytocin increase, minimal oxytocin change, and oxytocin decrease groups. Mean baseline oxytocin levels differed among the oxytocin responsivity groups but were not consistently associated with increasing oxytocin responsivity (1.7 vs. 1.3 vs. 2.6 pg/ml for the oxytocin increase, minimal change, and decrease groups, respectively; there were no reliable differences between the first two groups, although both differed from the third, p < .01). Preliminary analyses indicated that mean baseline oxytocin was not significantly related to BP measures. Demographic information on the mothers in the three subgroups is given in Table 1. Oxytocin responsivity groups did not differ in terms of mother's or baby's age, mother's education, racial group proportions, those living with versus without a spouse/partner, first-time mother versus not, mothers working versus not working outside the home, and smokers versus nonsmokers. Oxytocin responsivity groups did differ significantly in the num-
SPECIAL SECTION: OXYTOCIN, STRESS, AND BLOOD PRESSURE Table 1
Results
Demographic Information on Oxytocin Decrease, Minimal Oxytocin Change, and Oxytocin Increase Groups Variable Mother age (years) Education (years) Baby age (months) Black:White Partner:no partner Work:no work First baby:not first Smoke:do not smoke Breast-feeding: bonle-feedinga
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Oxytocin Responsivity and Laboratory BP Levels
Oxytocin decrease
Minimal oxytocin change
Oxytocin increase
29.3 14.9
30.8 16.3
26.1 14.0
6.7 4:5 6:3 5:4 5:4
5.3 1:7 8:0 4:4 2:6
5.0 2:6 6:2 3:5 4:4
2:7
1:7
1:7
2:7
5:3
7:1
a Proportion of breast- versus bottle-feeders differs by group (p < .017). All other differences are nonsignificant.
ber of breast-feeders versus bottle-feeders. The oxytocin increase group included more breast-feeders than bottle-feeders (7:1), whereas the oxytocin decrease group included fewer breast-feeders than bottle-feeders (2:7), and the minimal change group showed a more even ratio (5:3), likelihood Xz(2) = 8.15, p < .017. Oxytocin responses of the three groups on baby contact and no baby contact days are depicted in Figure 1. Analysis of variance confLrmed that the oxytocin responsivity groups (defined based on baby contact day responses) differed significantly in their oxytocin responses on the no baby contact day as well, F(2, 22) = 7.97, p < .0025; all group differences p < .01. The effect of baby contact differed by group, Group X Days F(2, 22) = 9.53, p < .001. Oxytocin responses to the speech were unchanged from the no baby contact to the baby contact day in the minimal change and oxytocin decrease groups (p > .50), whereas they were markedly higher on the baby contact versus the no baby contact day in the oxytocin increase group (p < .001; see Figure 1).
The initial omnibus analyses comparing overall lab stress session SBP and D B P levels of the oxytocin responsivity groups across both days and all time periods (areas under the curve throughout baseline, preparation, speech, and recovery) yielded significant main effects of group, F(2, 22) = 4.26 and 3.49, ps < .05 and .03, respectively. Overall SBP and DBP levels across all activities of the two test days were higher in the oxytocin decrease group than the oxytocin increase group (ps < .03 and .05, respectively); the minimal oxytocin change group showed intermediate SBP and DBP levels. Thus, higher oxytocin response was associated with lower overall BP on both test days (Figures 2 and 3). SBP and DBP levels for the no baby contact and the baby contact days were highly correlated (Table 2). For lab DBP, the second set of omnibus analyses indicated a Group × Time Periods interaction as well, F(6, 152) = 3.38, p < .004. For lab SBP, this interaction was not significant ( p > .20), and the main effect of oxytocin responsivity groups across all events was significant, F(2, 22) = 4.13, p < .03. Thus, group differences in D B P were greater during some time periods (specifically speech preparation and recovery) than others, whereas group differences in SBP levels were similar during all lab events. Univariate linear regression analyses (see Table 3 for correlations) indicated significant inverse relationships between oxytocin responsivity and D B P levels during speech preparation and recovery Minute 1 on both the no baby contact and baby contact days, preparation Fs(1, 23) = 6.68 and 9.14, ps < .017 and .007, recovery Minute 1 Fs(1, 23) = 4.48 and 4.93, p s < .046 and .038, respectively. There was a significant relationship to D B P level during recovery Minute 3 on the no baby contact day and a marginally significant one on the baby contact day, Fs(1, 23) = 6.23 and 2.94, ps < .021 and .010, respectively. In contrast, oxytocin responsivity effects were nonsignificant for D B P during baseline, speech Minute 1 and Minute 3 on both days, Fs(1, 23) = 0.43 and 2,64, ps > .65
Data Analysis Initial omnibus analyses of laboratory SBP and DBP levels were performed using PROC MIXED (SAS Institutes, Cary NC). First, oxytocin responsivity group differences across all days and time periods (comparing the full area under the curve for the two lab test sessions) were examined. Second, Oxytocin Responsivity Group (3) × Baby Contact/No Baby Contact Day (2) × Time Period (4: baseline, speech preparation, mean speech, and mean recovery) effects were examined using a repeated measures design. Interactions involving time periods were subsequently clarified by simple effects analysis at each time period, using simple univariate linear regression analyses to examine group differences in SBP and DBP levels during baseline, speech preparation, active speech Minute 1 and Minute 3, and recovery Minute 1 and Minute 3. Changes from baseline (SBP and DBP reactivity) during speech preparation and the mean active speech and mean speech recovery periods were also examined separately. For ambulatory SBP and DBP, repeated measures analyses used a Group (3) × Activity (3) design, where activities were sleep, posffeed (all readings during and for the 60 min after breast- or bottle-feeding), and wake (all other waking activities). To permit rough comparisons between the utility of oxytocin responsivity versus breast-/bottle-feeding as grouping factors, analyses substituting the latter for the former are also described briefly. All results were examined using two-tailed tests with a level set at .05, unless specified.
Figure 1. Percentage of change from baseline during speech in plasma oxytocin (OT) level for the OT decrease, minimal OT change, and OT increase groups on the no baby contact day and the baby contact day. The OT increase group showed significant increases and the OT decrease group showed significant decreases on both days (p < .05), whereas the minimal OT change group showed no reliable changes from baseline. For the OT increase group only, oxytocin increases after baby contact were greater than after no baby contact (p < .001).
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vs. +1.3 and +4.0 mm Hg, ps < .04 and .18). During the active speech itself, the group effect was nonsignificant for both SBP and DBP reactivity, Fs(2, 22) = 0.32 and 0.83, p > .45. However, there was a significant effect of baby contact versus no baby contact day for SBP, F(1, 22) = 4.12,p = .05, and for DBP there was a weak trend in the same direction, F(I, 22) = 1.67, p = .20 (Figure 4). Across all participants, SBP increases to the active speech on the baby contact day were less than increases on the no baby contact day ( + 12.5 vs. + 18.0, p = .05). Thus, mothers in the oxytocin decrease group had greater or marginally greater DBP reactivity during preparation and recovery than other mothers, whereas in the sample as a whole recent baby contact led to blunted SBP reactivity to the active speech.
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(Prep), active speech minute (Min) 1 and Min 3, and recovery Min 1 and Min 3 on the no baby contact day and the baby contact day for the three oxytocin (OT) responsivity groups. Overall SBP levels (area under the curve across days) were higher in the OT decrease group versus OT increase group (p < .03).
and .10 for both baselines, and F s ( l , 23) < 0.45, p > .65 for all speech periods. For SBP, the significant main effect of group and the lack of interaction with time periods meant that higher oxytocin responsivity was related to lower SBP across time periods, as Table 3 confirms. These SBP and DBP effects were similar on both the baby contact and the no baby contact days; for day differences, all F s ( l , 23) < 1.67, p > .21.
Reactivity to Preparation, Active Speech, and Recovery Analyses based on changes from baseline showed a significant effect of group collapsed across both days during speech preparation and speech recovery for DBP, Fs(2, 22) = 5.67 and 4.09, ps < .011 and .033, and the same effects for SBP approached significance, Fs(2, 22) = 2.64 and 2.48,ps < .094 and .13. The oxytocin decrease group showed greater DBP increases than the minimal oxytocin change group and marginally greater increases than the oxytocin increase group during preparation (+8.3 vs. +0.1 and +2.3 mm Hg, ps < .02 and .09, respectively) and recovery (+7.5
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Figure 3. Diastolic blood pressure (DBP) during baseline, speech preparation (Prep), active speech minute (Min) 1 and 3, and recovery Min 1 and Min 3 on the no baby contact day and the baby contact day for the three oxytocin (OT) responsivity groups as defined in Figure 1. Overall DBP levels (area under the curve across both days) were higher in the OT decrease group versus the OT increase group (p < .05). Changes from baseline (DBP reactivity) are greater or tended to be greater in the OT decrease group versus the minimal OT change and OT increase groups during speech preparation (ps < .02 and .09, respectively) and recovery (ps < .04 and .18, respectively).
SPECIAL SECTION: OXYTOCIN, STRESS, AND BLOOD PRESSURE
565
Table 2
Correlations of Systolic Blood Pressure (SBP) and Diastolic Blood Pressure (DBP) Levels During Events of Lab Stress Sessions Between No Baby Contact and Baby Contact Test Days Event
SBP
DBP
Baseline Speech preparation
.40" .77***
.49** .76***
Active speech Recovery
.68*** .83***
.76*** .83***
*p < .05. **p < .02. ***p < .0002.
Ambulatory BP Levels in the Home Environment For ambulatory BP, although trends in the same direction were observed under all conditions (Figure 5), significant group differences were obtained only for posffeeding DBP levels, F(1, 22) = 6.99, p < .016. Post'feeding DBP was lower in the oxytocin increase group and marginally lower in the minimal oxytocin change group than in the oxytocin decrease group (65.1 and 67.0 vs. 72.4, ps < .017 and .08, respectively). Posffeeding and sleep SBP were marginally lower in the oxytocin increase versus decrease groups (107.6 vs. 113.1 and 91.9 vs. 97.6, respectively, Fs(1, 22) = 3.22 and 3.44, ps < .087 and .077.
Comparative Analyses Among Breast-Feeder Versus Bottle-Feeders Although our primary focus was on comparing groups defined by oxytoein responsivity, initial analyses were performed to assess BP differences between the 14 breast-feeding and 11 bottlefeeding mothers. No significant differences were seen for laboratory BP levels between breast-feeders and bottle-feeders at any time period except for SBP levels during speech preparation. Collapsed across both days, preparation SBP levels were lower in breast-feeders than in bottle-feeders (106 vs. 116 mm Hg), F(1, 23) = 7.22, p < .015. No differences in laboratory DBP levels between feeding method were significant. Baseline (103/68 vs. 107/69, p > .20) and active speech BP levels (119/80 vs. 121/80, p > .40) were very similar between breast- and bottle-feeders. For ambulatory BP, no group differences were seen during other
Table 3
Correlations Between Oxytocin Responsivity and Blood Pressure During Both Stress Sessions Systolic blood pressure Time period Baseline
Preparation Speech Minute 1 Speech Minute 3 Recovery Minute 1 Recovery Minute 3 tp- 3.49, p < .05. For the breast-feeders only, this reflected a significant drop in DBP level from other waking to feeding hours (p < .05). Discussion This preliminary study encourages further research on possible BP reduction and antistress effects of oxytocin responsivity in humans. It provided evidence of lower overall BP during laboratory stress testing in mothers who showed oxytocin increases versus decreases in response to a speech stressor that immediately followed baby holding. In women with oxytocin increases, BP reductions were seen both after baby contact acutely enhanced oxytocin activity and when there was no recent baby contact. These results are similar to the BP reductions persisting in rats for
566
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Figure 5. Systolicblood pressure (SBP) and diastolic blood pressure (DBP) averaged across all ambulatoryreadings during sleep, nonfeeding waking hours, and for I hr after baby feeding (Post-feed) in the three oxytoein (OT) responsivitygroups. PosffeeclDBP levels are lower in the OT increase group and marginallylower in the minimalOT change group versus the OT decrease group (ps < .017 and .08, respectively).Sleep and posffeed SBP levels are marginallylower in the OT increasegroup versus the OT decrease group (ps < .087 and .077, respectively).
many days after oxytocin treatment (Uvnas-Moberg, 1998a, 1998b). They support the explanation that mothers with oxytocin increases to the lab protocol may have more frequent oxytocin pulses than other mothers, resulting in chronic BP-lowering and antistress effects. Mothers who showed decreases rather than increases in oxytocin from baseline to stress had higher DBP levels and greater DBP reactivity to speech preparation and recovery compared with other mothers. They did not, however, show greater BP reactivity to the active speech itself. This suggests that oxytocin may help limit the duration of stress responses but that it permits the adaptive capacity to mount a brief but intense stress response when appropriate. Two different but not mutually exclusive explanations for these findings are plausible. First, high oxytocin responsivity may be associated with a rise in the threshold for stressor intensity required to elicit a substantial pressor response. Second, oxytocin may blunt BP elevation more effectively during more passive conditions (when no overt response is involved, as in preparation and recovery) than during active coping stress (such as giving the speech). BP increases during passive versus active coping conditions typically involve more vasoconstriction versus greater cardiac output (Sherwood, Dolan, & Light, 1990). Oxytocin in plasma
can act rapidly and directly on vessels to decrease vasoconstriction (Sawchenko, 1991). Still, chronic oxytocin treatment was related to increases in central a2-adrenergic activity (Petersson et al., 1998), which lowers BP by decreasing sympathetic drive on both the heart and vessels. Breast-feeding mothers were more likely than bottle-feeding mothers to show oxytocin increases. However, relationships to BP levels were stronger when oxytocin responsivity rather than the related proxy of breast-feeding was used as the predictor variable. This is consistent with the interpretation that oxytocin's actions on the central nervous system and its peripheral effects on the cardiovascutar system are direct neurobiological pathways through which BP-lowering and antistress effects previously associated with breast-feeding may be mediated. Both breast-feeding and oxytocin increases to stress were associated with lower BP after infant feeding at home. This effect is also likely to be due to oxytocin, because oxytocin release during baby feeding is greater in breast- versus bottle-feeding mothers (Jenkins & Nussey, 1991; Modahl & Newton, 1979). All participants, regardless of their oxytocin response, showed reduced SBP reactivity to the active speech after baby contact versus the no baby contact control condition. The difference across days for the oxytocin increase group could be due to their greater oxytocin response after baby holding, but this is not true for the minimal change or oxytocin decrease groups, who showed similar oxytocin responses on both days. Recent warm contact with the baby may affect activity in other autonomic and neuroendocrine systems, including prolactin,/3-endorphin, estradiol, and parasympathetic activity, all of which have been suggested as possible additional factors influencing antistress responses (McCubbin, Kaufmann, & Nemeroff, 1991; Uchino, Cacioppo, & KiecoltGlaser, 1996). Alternatively, there may have been an undetected oxytocin response in all groups immediately after baby holding, leading to lowered BP responses to the speech. Future studies using more frequent oxytocin sampling and assessment of other potential mediators are needed to examine these possibilities. Several prior studies reported individual differences in human oxytocin responses to specific eliciting stimuli. Amico and Finley (1986) found that in response to breast stimulation, some nonlactaring women showed substantial increases in oxytocin release, whereas others showed no change. Sanders, Freilicher, and Lightman (1991) found that, in women exposed to uncontrollable noise, those high in emotionality showed more consistent oxytocin increases. Turner et al. (1999) found that women in a partner relationship were more likely to show oxytocin increases during mental imagery of positive attachment experiences. Despite the consistency of this study's findings with results from the animal literature on oxytocin's effects, the findings must be interpreted with some caution. First, the sample size was not large, indicating the need for replication in a larger sample of mothers. Second, personality and environmental factors that influence the choice to breast- versus bottle-feed may have contributed to the BP differences observed. Third, no information was obtained on oxytocin responses in the home environment. This would have been helpful to establish that our procedures were indeed identifying the women who have more frequent oxytocin release during daily life. Finally, another important limitation is the need to rely on plasma levels of oxytocin rather than brain tissue
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