Breast feeding, bottle feeding, and maternal autonomic responses to stress

Journal of Psychosomatic Res

Breast feeding, bottle feeding, and maternal autonomic responses to stress

Elizabeth Sibolboro Mezzacappaa,b,*, Robert M. Kelseyc, Edward S. Katkinb

aBehavioral Medicine Program, Columbia-Presbyterian Medical Center, Columbia University, Box 427, 622 West 168th Street,

New York, NY 10032-3784, United StatesbDepartment of Psychology, State University of New York at Stony Brook, United States

cDepartment of Pediatrics, The University of Tennessee Health Science Center, United States

Received 16 February 2004; accepted 3 November 2004

Abstract

Objective: The aim of this study was to examine the effects of

breast feeding on autonomic nervous system (ANS) response to

stressors. Methods: Sympathetic and parasympathetic activities

were examined before, during, and after standard laboratory

stressors in women who were either exclusively breast feeding

(n=14) or nonexclusively breast feeding (n=14), and in non-

postpartum controls (n=15). Results: Mothers who breast fed

exclusively showed greater levels of parasympathetic cardiac

modulation and slower heart rate (HR) throughout the session and

less HR increase and preejection period (PEP) shortening to mental

arithmetic (MA) than did nonexclusive breast feeders and controls.

0022-3999/04/$ – see front matter D 2005 Elsevier Inc. All rights reserved.

doi:10.1016/j.jpsychores.2004.11.004

* Corresponding author. Behavioral Medicine Program, Columbia-

Presbyterian Medical Center, Columbia University, Box 427, 622 West

168th Street, New York, NY 10032-3784, United States. Tel.: +1 212 305

4697; fax: +1 208 460 4935.

E-mail address: [email protected] (E.S. Mezzacappa).

Nonexclusive breast-feeders showed greater electrodermal reactiv-

ity to, and greater differences in skin conductance response (SCR)

frequency between baseline and recovery from cold pressor (CP)

than did either exclusive breast-feeders or controls. Sympathetic

activity was negatively related to the number of breast feedings and

positively related to bottle feedings. Conclusion: Breast feeding

shifts maternal ANS balance toward relatively greater parasympa-

thetic and lesser sympathetic activity; the opposite occurs with bottle

feeding. The frequency of feeding also is a critical factor in

determining breast feeding effects on maternal ANS function.

D 2005 Elsevier Inc. All rights reserved.

Keywords: Breast feeding; Electrodermal response; Heart period variability; Heart rate; Preejection period; Stress

Introduction

Maternal effects of breast feeding and weaning

Accumulating evidence indicates that breast feeding has

a significant impact on the mother, as well as the infant

[1–8]. Breast feeding and lactation appear to affect maternal

hypothalamic, autonomic, and cardiovascular functioning

[1–3,5,8]. For instance, a recent investigation [3] reported a

greater vagal modulation of cardiac function in lactating

mothers, but relatively increased sympathetic and decreased

vagal tone in nonlactating mothers. Based on these results, it

appears that breast feeding and non-breast-feeding mothers

have significantly different patterns of autonomic nervous

system (ANS) functioning.

Work with animal models indicates that differences in

ANS functioning also may exist among breast-feeding

mothers, depending on the actual amount of breast feeding

[5]. Rat dams tested either on Day 10 postpartum, which

corresponds to the peak in milk production ([9]; lactating

group), or on Day 25 postpartum, when pups were still

nursing but only rarely (weaning group), were compared

with females that did not become pregnant after exposure

to males during the same breeding cycle (control group).

Heart rates (HRs) in the lactating, weaning, and control

animals were recorded for 10-min periods before, during,

and after immobilization stress. While both the lactating

and weaning animals showed a blunted initial HR

response to the stressor, analyses of these periods revealed

that the HRs of weaning animals failed to habituate to

stress and showed delayed recovery after stress. The

failure of HR reactivity to stress to habituate may be

earch 58 (2005) 351–365

1 Results from a larger data set, from which data are derived, were

presented earlier [7].

E.S. Mezzacappa et al. / Journal of Psychosomatic Research 58 (2005) 351–365352

attributed to either the relative exacerbation of sympathetic

nervous system (SNS) activity or the attenuation of the

vagal modulation of cardiac control [10]. Therefore, ANS

differences appear to exist between breast feeders, and also

among breast-feeding mothers who differ in the amount of

breast feeding.

Further support for the suggestion that the frequency of

breast feeding is an important variable can be found in a

study on the association between breast-feeding behavior

and reports of physician visits [4]. The likelihood of a

physician visit for psychological illness did not differ

between breast-feeders and non-breast-feeders, but a con-

tinuous measure of breast feeding (i.e., frequency of

nursings) was associated with a decreased likelihood of a

physician visit for psychological illness.

It is also possible that the frequency of bottle feeding has

specific effects on breast-feeding mothers. For example,

bottle feeding among breast-feeding mothers is related to a

decrease in positive mood [6] and an increase in perceived

stress [4]. In addition, bottle feeding by breast-feeders

results in increased blood pressure (BP), just as breast

feeding does [7]. Therefore, bottle feeding also may have

ANS effects.

There have been no physiological studies that have gone

beyond the simple classification of breast versus bottle

feeding, although this dichotomy may obscure relationships

between infant feeding practices and maternal measures. It

is therefore important to examine the possible differences in

the effects of different levels of lactation and breast feeding

on autonomic activity.

Moreover, the time since last nursing appears to be

critical in understanding the effects of breast feeding. The

actual act of breast feeding has cardiovascular effects [1,7].

Compared with the same amount of time after bottle

feeding, 10 minutes after breast feeding, systolic BP is

elevated [7]. However, another investigation found that, for

one hour after feeding, breast-feeding mothers had lower

BPs than did bottle-feeding mothers [1]. In addition, an

investigation of neuroendocrine response to stress found

that time since last nursing was a critical factor [11,12]

Breast-feeders who had nursed 100 minutes before stress

showed greater neuroendocrine response to stress than did

breast-feeders who had nursed only 30 minutes before stress

[11]. Based on these findings, time since the last nursing

session may be a critical factor in considering the ANS

effects of infant feeding.

The present study

The specific aim the of the present study was to examine

the underlying sympathetic and parasympathetic nervous

system activity before, during, and after standard laboratory

stressors in two groups of breast-feeding mothers (exclu-

sively or nonexclusively nursing) and non-postpartum

control women. Sympathetic influences were assessed by

the preejection period (PEP), an index of sympathetic effects

on the heart, and skin conductance responses (SCR;

[13–16]). Parasympathetic activity was indexed by the

root-mean-squared successive difference (rMSSD) of the

R–R intervals. The rMSSD is a measure of heart period

variability (HPV) that is positively correlated with the

degree of vagal cardiac control [17–19]. In all analyses, we

controlled for several possible demographic confounds. In

addition, the associations of ANS measures with the

frequency of breast feeding, frequency of bottle feeding,

and time since last nursing were examined.

Method

Participants

Data for this study were drawn from a subset of

participants who were recruited for a study on cognitive

and perceptual changes in motherhood.1 Participants were

mothers (n=28) and non-postpartum women (n=15) who

were between 18 and 45 years old and free of any medical

condition affecting the cardiovascular system. Except for

birth control, or antibiotic and topical treatments, partic-

ipants were not taking any medications. Table 1 presents the

demographic information for each of the groups. The timing

of evaluations was not related to the menstrual cycle.

Mothers received US$25, and nonmothers received US$20

compensation for a 2-hour session.

The participants provided information about age, race,

number of children, and age of the youngest child, and

whether they used pharmacological birth control (yes/no) or

worked out of the house (yes/no). The age of the youngest

child was interpreted as the time since childbirth (weeks

postpartum). Smoking was assessed by the question, bDoyou smoke?Q The answers ranged on a five-point scale from

0 (no) to 4 (yes, more than two packs a day). Participants

also were asked to indicate their breast-feeding status—

whether they were currently breast feeding exclusively or

partially (supplementing with formula or food). If they

answered that they were supplementing, they also were

asked how often they nursed each day. In addition, the

participants indicated how often they bottle fed per day.

Finally, the participants were asked how long it had been

since they last nursed their infants.

All mothers had infants between the ages of 1 and

12 months. Mothers were categorized as exclusively breast

feeding (n=14) if they reported only breast feeding or bottle

feeding with expressed breast milk, and no other liquids (e.g.,

water, formula, and juice) or solid foods were given to the

infant. Mothers were categorized as nonexclusively breast

feeding (n=14) if they reported breast feeding, as well as

supplementing their babies’ diets with formula or solid foods.

Table 1

Demographic information

Nonexclusive

breast-feeders

Exclusive

breast-feeders

Non-postpartum

controls

Age 30.64 (5.24) 29.14 (5.14) 28.53 (5.18)

% Working 21.4 21.4 86.7

% Using birth

control

7.1 0 13.3

% Smokers 7.1 7.1 26.6

% Caucasian 85.7 85.7 53.3

% Latina 0 7.1 0

% African

American

0 0 6.7

% Asian 14.3 7.1 33.4

% Other 0 0 6.7

Time postpartum

(weeks)

23.21 (15.54) 11.61 (5.47) N/A

Number of children 1.36 (.50) 1.79 (1.12) 0

Standard deviations appear in parentheses.

E.S. Mezzacappa et al. / Journal of Psychosomatic Research 58 (2005) 351–365 353

Tasks

Participants completed passive and active coping tasks

[20,21]. The passive coping task was the cold pressor (CP),

which increases sympathetic vasoconstriction and inhibits

the vagal control of HR, resulting in higher HR. The CP task

required the immersion of the dominant hand up to the wrist

in 1 l of a 4 8C ice/water mix for 1 min. The active coping

task was mental arithmetic (MA), which tends to increase

sympathetic and decrease vagal influences on the heart,

resulting in higher HR. The MA task required serial

subtractions by sevens from a four-digit number for 1 min.

The participants were instructed to work as quickly and

accurately as possible.

Procedures

All procedures were approved by the University’s Institu-

tional Review Board. After giving a brief description of the

experiment and obtaining informed consent, a female

experimenter instrumented the participants for electrocardio-

graphic (ECG), impedance cardiographic (ICG), and skin

conductance recordings. Following a 5-min adaptation

period, 5 min of baseline physiological data were recorded.

The participants then completed the MA and CP tasks in

counterbalance to control for carryover effects. A 5-min

baseline period separated the two tasks, and a 1-min recovery

period followed each task. After the recovery period for the

last task, the recording devices were removed, and partic-

ipants completed a questionnaire to assess demographic

information and breast- and bottle-feeding practices. Partic-

ipants were paid and released after debriefing.

Apparatus

Thoracic impedance was assessed with a Minnesota

Impedance Cardiograph (Instrumentation for Medicine

model 304B), using tetrapolar aluminum-Mylar band

electrodes. Voltage recording bands were placed around

the base of the neck and around the thorax, at the level of

the xiphisternal junction. Bands for impressing the AC

current were placed 3 cm above the recording band, at the

base of the neck, and 3 cm below the recording band, at the

xiphisternal junction [15]. The interelectrode distance was

determined from the average of the front and back midline

distances between the two recording electrodes. The ICG

provided ECG signals, detected baseline thoracic impedance

(Z0), and computed the first derivative of the changes in

thoracic impedance (dZ/dt), an index of blood flow through

the aorta [15,22].

Skin conductance was assessed using two Ag–AgCl

electrodes placed on the hypothenar eminence of the

nondominant hand [23], using an electrode gel recommen-

ded by Fowles et al. [24]. These electrodes were connected

to a constant voltage coupler [25] and fed to a Grass

polygraph. The time constant on the Grass amplifier was set

to 0.8 s.

Signal processing

The ECG and dZ/dt signals were digitized at 500 Hz, and

the Z0 signal was digitized at 250 Hz and stored on disk for

postprocessing. The digitized signals were scored on a beat-

to-beat basis and then ensemble averaged with reference to

the peak of the ECG R-wave [15,22,26]. A trained researcher

visually inspected each ensemble-averaged waveform fol-

lowing a procedure reported previously [15,26]. Beat-to-beat

averages for HR and ensemble averages for PEP were

calculated for the last minute of the baseline period

preceding each task, during each 1-min task, and during

the 1 min of recovery following each task. The rMSSD was

calculated for these minutes, using a program that was

specially developed for that purpose.

Skin conductance fluctuations greater than .05 ASiemens

were counted within the last minute of each baseline pe-

riod, within each 1-min task, and in the 1 min following

each task.

Data analyses

MANCOVA analyses

Baseline, task, and recovery measures of PEP, HR,

rMSSD, and SCR were analyzed using repeated measures

MANOVA or MANCOVA. Separate MANOVAs or MAN-

COVAS were conducted for each measure and task, with

group (exclusive/nonexclusive/control) as the between-

subjects factor and period (baseline/task/recovery) as the

within-subjects factor. Wilks lambda (k) criterion was used

for the multivariate significance testing. Significant and

near-significant multivariate effects were followed by

univariate ANCOVAs, with orthogonal contrasts for each

measure. A natural log transform was applied to the rMSSD

data prior to analysis.

Table 2

Correlations between demographic variables and cardiovascular measures

Maternal

age

Work

status Contraceptives Smoking

No. of

children

Infant

age

n =43 n =43 n =43 n =43 n =28 n =28

Baseline measures

Pre mental arithmetic

PEP �0.10 �0.11 0.01 �0.06 0.05 �0.03

HPV �0.24 �0.07 �0.15 �0.16 �0.07 �0.35+

HR 0.10 0.15 0.21 0.25 �0.01 0.30

SCR �0.03 �0.19 �0.18 �0.06 0.13 0.39*

Pre cold pressor

PEP �0.03 �0.07 0.07 �0.05 0.13 0.02

HPV �0.22 �0.14 �0.28 �0.20 0.12 �0.37+

HR 0.12 0.25 0.29+ 0.25 �0.09 0.33+

SCR �0.08 0.08 0.03 0.11 0.13 0.09

Reactivity measures

Mental arithmetic

PEP 0.15 �0.14 �0.14 0.06 0.26 �0.48*

HPV �0.13 �0.16 0.05 0.02 0.06 �0.03

HR �0.18 0.22 0.09 �0.04 �0.41* 0.37+

SCR �0.17 �0.17 0.01 �0.30* �0.02 �0.19

Cold pressor

PEP �0.06 0.07 �0.34* 0.08 �0.08 �0.56**

HPV �0.04 �0.04 0.14 �0.10 0.02 0.17

HR �0.03 �0.08 0.04 �0.01 0.04 �0.10

SCR �0.08 �0.16 �0.16 �0.33* �0.02 0.06

+ P b.1.

* P b.05.

** P b.005.

Fig. 1. Adjusted means and standard errors for PEP during the baseline,

mental arithmetic, and recovery periods for the nonexclusively breast-

feeding, exclusively breast-feeding, and control groups.


Reactivity calculations

For each task, cardiovascular reactivity was calculated

by subtracting the pretask baseline values of PEP,

lnrMSSD, and HR from the task values. Likewise, SCR

reactivity was calculated for each task by subtracting the

number of fluctuations during the baseline from the

number during the task.

Covariates

Associations among physiological, demographic, and

situational variables were analyzed by calculating the

correlations among these variables, using both physiolog-

ical baseline and reactivity measures. The situational and

demographic variables tested were age, work status, birth

control use, smoking frequency, number of children, and

time postpartum/age of youngest child. Correlations were

conducted using data from all the women or, in the case of

number of children and time postpartum, all mothers. The

use of oral contraceptives, work status, and smoking

frequency were analyzed using nonparametric Spearman’s

Rank Correlation. Age, number of children, and time

postpartum were analyzed using Pearson’s correlation.

Because of skewness, number of children and time

postpartum were log transformed before analysis.

Table 2 shows the results of these correlational

analyses. As the table summarizes, there were several

demographic variables that were related to physiological

measures. Of particular note are the associations of oral

contraceptive use with PEP response to CP and smoking

with SCR responses to both tasks. These findings are

consistent with previous work showing an association with

oral contraceptive use and smoking with psychophysio-

logical reactivity in the laboratory [27–29]. If a demo-

graphic variable showed a significant association with a

physiological variable, and the groups appeared to differ

in that demographic variable, then it was used as a

covariate in the MANCOVA analysis. (Analyses control-

ling for time postpartum will be addressed in the

Discussion section.) As indicated in Table 1, the groups

differed with respect to percentage of those using oral

contraceptive and the percentages of smokers. Therefore,

birth control use was used as a covariate in the analyses of

PEP responses to CP, and smoking behavior was used as a

covariate in the analyses of electrodermal responses to

both tasks.

Correlational analyses: number of breast feedings, bottle

feedings, and time since last nursing

Data on the number of nursings per day were available

for all the nonexclusive breast-feeders and for nine of the

exclusive breast-feeders. Data on the number of bottle

feedings per day were available for all mothers, except for

one nonexclusive breast-feeder. To assess the possible dose

response characteristics in the association between fre-

quency of breast feeding and physiological measures,

correlations between the number of breast feedings per

day and physiological baseline and reactivity measures were

calculated. Parallel analyses assessed the associations

between the frequency of bottle feeding and physiological

measures. Because of skewness in the distribution, the

number of bottle feedings per day was square-root trans-

formed before analysis. Time since last nursing was

Table 3

Summary of MANOVA analyses for mental arithmetic

Effect of group Effect of period Effect of interaction Contrast 1 Contrast 2

df F k df F k df F k df F k df F

PEP Overall 2,40 0.39 Multivariate 0.59 2,39 13.45z Multivariate 0.89 4,78 1.15 N vs. C 1 2,39 0.06 N/C vs. E 0.89 2,39 2.3

N vs. C 1,40 0.62 Linear 1,40 22.78z Linear 2,40 0.94 Linear 1,40 0.01 Linear 1,40 1.86

N/C vs. E 1,40 0.15 Quadratic 1,40 22.82z Quadratic 2,40 2.41 Quadratic 1,40 0.11 Quadratic 1,40 4.71*

HPV Omnibus 2,40 5.42** Multivariate 0.46 2,39 23.08z Multivariate 0.9 4,78 1 N vs. C 0.99 2,39 0.21 N/C vs. E 0.91 2,39 1.83


N/C vs. E 1,40 10.74*** Quadratic 1,40 46.43z Quadratic 2,40 1.02 Quadratic 1,40 0.33 Quadratic 1,40 1.73

HR Omnibus 2,40 4.47* Multivariate 0.23 2,39 65.75* Multivariate 0.8 4,78 2.31+ N vs. C 0.94 2,39 1.31 N/C vs. E 0.85 2,39 3.54*

N vs. C 1,40 0.00 Linear 1,40 11.01*** Linear 2,40 0.98 Linear 1,40 1.29 Linear 1,40 0.67

N/C vs. E 1,40 8.95y Quadratic 1,40 131.54z Quadratic 2,40 3.49* Quadratic 1,40 1.04 Quadratic 1,40 5.95*

SC Omnibus 2,39 0.17 Multivariate 0.24 2,39 61.03z Multivariate 0.94 4,78 0.6 N vs. C/E 0.96 2,39 0.84 C vs. E 0.98 2,39 0.37

N vs. C/E 1,39 0.32 Linear 1,40 7.70** Linear 2,40 0.44 Linear 1,40 0.18 Linear 1,40 0.7

C vs. E 1,39 0.04 Quadratic 1,40 121.1z Quadratic 2,40 0.46 Quadratic 1,40 0.9 Quadratic 1,40 0.02

PEP=preejection period; HPV=heart period variability; HR=heart rate; SCR=skin conductance response.

N=nonexclusive breast-feeders; C=controls; E=exclusive breast-feeders.

N/C=combined mean of nonexclusive and control groups; C/E=combined mean of controls and exclusive groups.

z P b.0001.

* P b.05.

** P b.01.

*** P b.005.+ P b.1.

y P b.001.

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Fig. 2. Adjusted means and standard errors for lnrMSSD during the

baseline, mental arithmetic, and recovery periods for the nonexclusively

breast-feeding, exclusively breast-feeding, and control groups.

Fig. 4. Adjusted means and standard errors for SCR frequency the baseline,




converted to hours and tested for correlations with baseline

and reactivity measures.

Results

Mental arithmetic

Cardiac sympathetic activity: PEP

Fig. 1 shows the means and standard errors for PEP

before, during, and after MA. As Table 3 presents, the

MANOVA revealed a significant effect of period (g2=.41),

which was due to significant linear (g2=.36) and quadratic

(g2=.36) effects. PEP was shorter in recovery than in baseline

and shorter during MA than during baseline and recovery.

Multivariate analyses did not reveal a significant group

main effect or group-by-period interaction; however, uni-

variate analyses revealed a marginally significant group-by-

period quadratic effect (g2=.11). PEP shortened less in

Fig. 3. Adjusted means and standard errors for HR during the baseline,



response to MA in the exclusive breast-feeders than in the

combined mean of the nonexclusive breast-feeder and

control groups (g2=.10). The quadratic trends for the latter

two groups were not significantly different from each other.

Cardiac parasympathetic modulation: HPV

Fig. 2 shows the means and standard errors for lnrMSSD

before, during, and after MA. As Table 3 presents, the

MANOVA revealed a significant effect of period (g2=.54),

which was due to a significant quadratic effect (g2=.54).

lnrMSSD was lower during MA than during baseline

and recovery.

The group-by-period interaction was not significant for

lnrMSSD, but there was a significant group main effect

(g2=.21). Mean lnrMSSD was higher in the exclusive

breast-feeders than in the nonexclusive breast-feeding and

control groups; nonexclusive breast-feeders and controls

had similar mean lnrMSSD.

Fig. 5. Adjusted means and standard errors for PEP during the baseline,

cold pressor, and recovery periods for the nonexclusively breast-feeding,

exclusively breast-feeding, and control groups.

Table 4

Summary of MANOVA analyses for cold pressor

Effect of group Effect of period Effect of interaction Contrast 1 Contrast 2

df F k df F k df F k df F k df F

PEP Overall 2,39 0.08 Multivariate 0.37 2,39 33.18z Multivariate 0.94 4,78 0.65 N vs. C 0.99 2,39 0.24 N/C vs. E 0.95 2,39 1.08


N/C vs. E 1,39 0.02 Quadratic 1,40 18.91z Quadratic 2,40 0.93 Quadratic 1,40 0.24 Quadratic 1,40 1.62

HPV Omnibus 2,40 5.49** Multivariate 0.5 2,39 19.28z Multivariate 0.98 4,78 0.93 N vs. C 0.99 2,39 0.27 N/C vs. E 0.99 2,39 0.14



HR Omnibus 2,40 4.50* Multivariate 0.13 2,39 132.91z Multivariate 0.79 4,78 2.41+ N vs. C/E 0.82 2,39 4.31* C vs. E 0.96 2,39 0.7

N vs. C 1,40 0.10+ Linear 1,40 124.54z Linear 2,40 3.97* Linear 1,40 6.94* Linear 1,40 1.01


SCR Omnibus 2,39 1.61 Multivariate 0.54 2,39 16.33z Multivariate 0.77 4,78 2.67* N vs. C/E 0.8 2,39 4.72* C vs. E 0.96 2,39 0.8

N vs. C/E 1,39 3.19+ Linear 1,40 0.02 Linear 2,40 1.19 Linear 1,40 0.89 Linear 1,40 1.49

C vs. E 1,39 0.05 Quadratic 1,40 32.81z Quadratic 2,40 4.76* Quadratic 1,40 9.5*** Quadratic 1,40 0.03

PEP=preejection period, HPV=heart period variability, HR=heart rate, SCR=skin conductance response.

N=nonexclusive breast-feeders, C=controls, E=exclusive breast-feeders.

N/C=combined mean of nonexclusive and control groups, C/E=combined mean of controls and exclusive groups.

y P b.001.

z P b.0001.

** P b.01.

*** P b.005.

* P b.05.+ P b.1.

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Fig. 6. Adjusted means and standard errors for lnrMSSD during the

baseline, cold pressor, and recovery periods for the nonexclusively breast-


Fig. 7. Adjusted means and standard errors for HR during the baseline, cold

pressor, and recovery periods for the nonexclusively breast-feeding,



Heart rate

Fig. 3 shows the means and standard errors for HR

before, during, and after MA. As Table 3 presents,

MANOVA revealed a significant effect of period

(g2=.77), which was due to significant linear (g2=.22)and quadratic (g2=.77) effects. HR was lower in recovery

than at baseline, and HR was higher during MA than during

baseline and recovery.

There was also a marginally significant group-by-period

interaction at the multivariate level (g2=.11), which was dueto a significant quadratic effect (g2=.15). The exclusively

breast-feeding group had a smaller HR increase to MA than

did the nonexclusive breast-feeding and control groups

(g2= .13); the nonexclusive breast-feeding and control

groups had similar HR responses to MA.

There was also a significant group main effect for HR

(g2=.18). The exclusive breast-feeding group had lower

mean HR than did the nonexclusive breast-feeder and

control groups; nonexclusive breast-feeders and controls

had similar mean HR levels.

Sympathetic arousal: SCR

Fig. 4 shows the adjusted means and standard deviations

for SCR frequency before, during, and after MA. As Table 3

presents, MANCOVA revealed a significant effect of period

(g2=.77), which was due to significant linear (g2=.22) and

quadratic (g2=.23) trends. SCRs were more frequent during

MA than during baseline or recovery, and more frequent

during recovery than during baseline. There were no

significant main or interaction effects involving groups.

Cold pressor

Sympathetic activity: PEP

Fig. 5 shows the adjusted means and standard errors for

PEP before, during, and after CP. As Table 4 presents,

MANCOVA revealed a significant effect of period (g2=.63),


(g2=.32) effects. PEP was shorter in recovery than at

baseline, and longer during CP than during baseline and

recovery. There were no significant effects involving groups.

Cardiac parasympathetic modulation: HPV

Fig. 6 shows the means and standard errors for lnrMSSD

before, during, and after CP. As Table 4 presents, MAN-

COVA revealed a significant effect of period (g2=.50),


(g2=.38) effects. lnrMSSD was higher in recovery than

at baseline, and lower during CP than during baseline

and recovery.

The group-by-period interaction was not significant, but

there was a significant group main effect (g2=.22). Contrast

analyses indicated that mean lnrMSSD levels in the exclusive

breast-feeding group were higher than in the combined

nonexclusive breast-feeding and control groups; the latter

two groups did not differ significantly from each other.

Heart rate

Fig. 7 shows the means and standard errors for HR

before, during, and after CP. As Table 4 presents,

MANCOVA revealed a significant effect of period

(g2=.87), which was due to significant linear (g2=.76)

and quadratic (g2=.74) effects. HR was lower in recovery

than at baseline, and higher during CP than during baseline

and recovery.

Multivariate analyses also revealed a marginally signifi-

cant group-by-period interaction (g2=.11), which was due

to a significant group-by-period interaction for the linear

trend (g2= .16). The mean difference in HR between

baseline and recovery was greater in the nonexclusive

breast-feeding group than in the exclusive breast-feeding

and control groups; the exclusive breast-feeding and control

groups did not differ in HR recovery from CP.

Table 5

Correlations between number of feedings and hours since breast-fed with

cardiovascular measures

Number of

breast feedings

Number of

bottle feedings

Hours since

breast fed

n=21 n=26 n=27

PEP resting baseline

pre mental arithmetic

�0.16 0.14 �0.02

PEP resting baseline

pre cold pressor

�0.15 0.14 0.06

lnrMSSD resting baseline


0.42+ �0.34+ �0.11

lnrMSSD resting baseline

pre cold pressor

0.38+ �0.47* �0.15

HR resting baseline


�0.11 0.39* 0.22

HR resting baseline

pre cold pressor

�0.18 0.46* 0.27

SCR resting baseline


0.18 �0.02 �0.15

SCR resting baseline

pre cold pressor

0.44* �0.11 0.05

PEP response to

mental arithmetic

0.58** �0.40* �0.21

PEP response to

cold pressor

0.51* �0.38+ �0.33+

lnrMSSD response to

mental arithmetic

0.26 �0.22 �0.11

lnrMSSD response

to cold pressor

�0.25 0.10 �0.02

HR response to

mental arithmetic

�0.70** 0.37+ 0.16

HR response to

cold pressor

�0.13 0.00 �0.04

SCR response to

mental arithmetic

�0.24 0.20 0.25

SCR response to

cold pressor

�0.44* 0.45* 0.00

+ P b.1.

* P b.05.

** P b.005.


There also was a significant multivariate group main

effect (g2=.18). Contrast analyses revealed that HR was

lower overall in the exclusive breast-feeding group than in

the nonexclusive breast-feeding and control groups

(g2=.18); the nonexclusive breast-feeders and controls had

similar mean HR levels.

Sympathetic arousal: SCR

Fig. 8 shows the adjusted means and standard deviations

for SCR frequency before, during, and after CP. As Table 4

presents, MANCOVA revealed a significant effect of period

(g2=.46), which was due to a significant quadratic trend

(g2=.45). SCRs were more frequent during CP than during

baseline and recovery.

There was a significant multivariate group-by-period

interaction effect (g2=.12), which was due to a significant

group-by-period quadratic interaction effect (g2=.19). Con-trast analyses indicated that the mean increase in SCR

during CP was greater in the nonexclusive breast-feeding

group than in the exclusive breast-feeding and control

groups (g2=.19); SCR responses to CP were similar in the

exclusive breast-feeders and controls.

Breast feeding, bottle feeding, and time since last nursing

Table 5 lists the correlations between the physiological

measures and number of breast feedings, number of bottle

feedings, and time since last nursing. There were several

significant associations between the number of breast

feedings and the physiological measures, including negative

correlations with HR reactivity to MA and SCR reactivity to

CP, as well as positive correlations with PEP reactivity to

both tasks (note that PEP is an inverse index of SNS

activity). The pattern of correlations suggests that the

number of breast feedings was associated with diminished

Fig. 8. Adjusted means and standard errors for SCR frequency the baseline,

cold pressor, and recovery periods for the nonexclusively breast-feeding,


SNS reactivity to stress. The number of breast feedings also

had a moderate association with increased resting vagal

modulation before each task.

Because the number of breast feedings and the number of

bottle feedings were significantly and inversely correlated

(r=�.60), it is not surprising that the number of bottle

feedings was correlated in the opposite direction with the

same variables. Accordingly, the pattern of correlations

suggests that the number of bottle feedings was positively

related to SNS reactivity to stress. With respect to baseline

measures, there were indications that the number of bottle

feedings was associated with decreased resting vagal

modulation. Most notably, however, the number of bottle

feedings was positively related to resting HR preceding both

tasks, suggesting an ANS balance tilted toward increased

SNS and/or decreased PNS activity. There were no

significant correlations between time since last nursing

and the physiological measures.


Discussion

To summarize the main findings of this study, there was

strong evidence of lower HR in exclusively breast-feeding

mothers than in nonexclusively breast-feeding mothers and

non-postpartum controls. The lower HR is apparently due

to higher vagal cardiac modulation in the exclusively

breast-feeding group compared with the other two groups,

as evidenced by lnrMSSD levels. Nonexclusive breast-

feeders and controls did not differ from each other in either

HR or lnrMSSD.

Responses to MA suggest, in addition, that exclusive

breast feeding decreases sympathetic cardiac responses to

stress. Compared with nonexclusively breast-feeding and

non-postpartum controls, exclusively breast-feeding moth-

ers showed smaller increases in HR and less shortening of

PEP during MA. These results suggest that exclusive breast

feeding buffers SNS responses to this psychological stressor.

Responses to CP suggest that nonexclusive breast-

feeding increases autonomic lability. Nonexclusive breast-

feeders had recovery HRs that differed more from baseline

and greater increases in SCR during CP than did exclusive

breast-feeders and non-postpartum controls. These results

suggest tentatively that nonexclusive breast feeding

increases SNS effects during cold stress, which, in turn,

may increase PNS effects during recovery. Moreover,

correlations with frequency of breast feeding and bottle

feeding suggest that breast feeding is negatively associated

with SNS responses to CP, whereas bottle feeding by breast

feeders is associated with increased SNS or decreased PNS

activity. Thus, different amounts of breast feeding (exclu-

sive vs. nonexclusive) elicited different patterns of auto-

nomic alterations.

Overall, the findings support the general notions that,

after statistically controlling for important covariates, such

as oral contraceptive use and smoking, (a) exclusive breast-

feeders have different patterns of ANS function than do

nonexclusive breast-feeders; in fact, nonexclusive breast-

feeders may be more similar to non-postpartum controls

than to exclusive breast-feeders; (b) the effects of breast

feeding on autonomic cardiovascular function suggest dose

response patterning; (c) bottle feeding by breast-feeders

may alter maternal autonomic function. As detailed below,

these results are relevant in developing methodological

guidelines and establishing the direction of causality in

breast-feeding research.

Breast feeding and levels of autonomic

cardiovascular functioning

Mothers who breast fed exclusively showed greater

levels of parasympathetic cardiac modulation and slower

HR throughout the session. These findings replicate those of

Altemus et al. [3]. It is important to note that, in our study,

only exclusive breast feeding was associated with the

parasympathetic effects. Altemus et al. defined breast

feeding as at least 90% of feedings derived from nursing,

which is very close to exclusive breast feeding. Breast-

feeding frequency also had a moderate association with

increased resting PNS modulation before each task. Thus,

one might propose that exclusive breast feeding primarily

alters parasympathetic cardiac modulation.

Breast feeding, bottle feeding, and reactivity to stressors

In addition to increased levels of PNS modulation,

exclusive breast-feeders showed less HR reactivity and

PEP shortening to MA than did nonexclusive breast-feeders

and controls. This is the first human investigation to report

an attenuation of cardiac reactivity to psychological stress

that was associated with breast feeding. Despite a large

animal literature indicating that lactation blunts reactivity to

stress [5,30–34] and one human study that suggests that

breast feeding blunts reactivity to exercise stress, three

previous studies have failed to find solid evidence that

breast feeding blunts reactivity to psychological stress in the

laboratory [1,3,7]. These studies did not restrict their breast-

feeding groups to exclusively nursing mothers; therefore, it

is possible that heterogeneity in breast-feeding frequency

obscured group differences.

In addition, this is one of the first human studies to

address the possible effects of bottle feeding on breast-

feeding mothers. In most of the analyses in this study, the

nonexclusive group responded like the control group did.

Electrodermal response was the only variable that differ-

entiated nonexclusives from the controls. Nonexclusive

breast-feeders showed greater electrodermal reactivity to

CP than did the exclusive breast-feeders and controls. This

finding corroborates earlier findings of increased sympa-

thetic reactivity during weaning (when, by definition, there

is nonexclusive breast feeding; [5]). There were no group

differences in PEP responses to CP that would reflect

differences in cardiac sympathetic arousal. However, CP

elicits peripheral sympathetic vasoconstriction, which might

obscure group differences in PEP responses through

loading effects.

The difference between baseline and recovery HR after

CP was larger in nonexclusive breast-feeders than in

exclusive breast-feeders and controls; nonexclusive breast-

feeders had the largest decrease in HR in recovery. This

finding contradicts earlier findings of decreased parasym-

pathetic activity in recovery during weaning [5]. It is unclear

what the relative difference between baseline and recovery

HR (where recovery HR is lower) means; however, one

interpretation may be that nonexclusive breast feeding is

associated with greater HR instability in stress.

The findings from the group comparisons were com-

plemented by significant correlations between breast-feed-

ing frequency and several physiological measures. For

example, increased frequency of nursing was associated

with diminished HR and PEP reactivity to MA and

diminished PEP and SCR reactivity to CP. This pattern of

Table 6

Correlation between age of infant/time postpartum and cardiovascular

measures for nonexclusive and exclusive breast feeders

Nonexclusive Exclusive

Baseline measures

Pre mental arithmetic

PEP �0.09 �0.09

HPV 0.03 �0.50+

HR 0.06 0.30

SCR 0.48+ 0.46+

Pre cold pressor

PEP �0.29 �0.60*

HPV 0.08 0.12

HR 0.10 0.56*

SCR �0.20 �0.46+

Reactivity measures

Mental arithmetic

PEP �0.06 �0.01

HPV �0.07 �0.40

HR 0.05 0.37

SCR 0.35 0.25

Cold pressor

PEP �0.56* �0.50+

HPV 0.32 0.07

HR �0.10 �0.09

SCR �0.07 �0.36

+ P b.1.

* P b .05.


correlations suggests that breast-feeding frequency was

associated with diminished SNS reactivity to stress. The

pattern of correlations for breast-feeding frequency was

mirrored by an opposite set of associations for bottle-

feeding frequency, which is not surprising, since breast and

bottle feeding are inversely related.

Time since last nursing

The lack of an association between the length of time

since last nursing with any physiological measures conflicts

with a previous investigation reporting stress dampening

effects only immediately after nursing [11]. However, it is

important to note that the previous study measured neuro-

endocrine responses, while the present study measured ANS

responses. Several researchers have noted dissociations

among behavioral, cardiovascular, and hormonal response

to stressors using animal models [5,12,35–37]. For example,

in some investigations, animals showed dampened hormo-

nal responses without the attenuation of behavioral response

[36,37]. Therefore, dependence on the recency of nursing

may be critical for HPA axis alterations and not ANS

alterations. Another proposition may be that, in humans,

lactation has a tonic effect on ANS function, while nursing

has a transient effect on the HPA axis function.

Control of time postpartum

Pregnancy is a time of extensive cardiovascular alter-

ations, and the postpartum period is thought to be a time of

gradual return to prepregnancy levels of functioning [38].

The longer the time postpartum/the older the infant, the

more the recovery from pregnancy has progressed. Thus,

researchers must then separate possible alterations that arise

from breast feeding from those that simply arise from

recovery from childbirth. In the present study, there was a

wide range of time postpartum/age of baby. And, as can be

seen from Table 1, exclusive and nonexclusive mothers

differed in how long ago they gave birth. As expected,

compared with nonexclusive breast-feeding mothers, exclu-

sively breast-feeding mothers were nursing younger babies.

In addition, as can be seen from Table 2, time

postpartum/age of baby also was associated with cardio-

vascular and electrodermal responses. It is possible, then,

that the group differences between exclusive and nonexclu-

sive breast-feeders arose because of differences in time

postpartum, rather than from the different levels of breast

feeding. That is, exclusively breast-feeding mothers with

younger babies may differ from mothers who are weaning

older babies simply because of differences in the progress of

recovery from pregnancy. To address this possibility, post

hoc analyses that controlled for time postpartum were

performed in a second set of MANCOVAs restricted to the

two groups of mothers.

In general, the differences between these two groups of

mothers after controlling for time postpartum were similar

to those in the three group comparisons. Compared with

nonexclusive breast-feeders, exclusive breast-feeders had

higher levels of rMSSD, slower HR, and attenuated SCR

reactivity to CP than did nonexclusive breast-feeders.

However, differences in HR and PEP responses to MA

were reduced to nonsignificance. Thus, for the most part, the

differences in basal ANS levels and responses to CP

between the exclusive and nonexclusive breast-feeders did

not occur because they were nursing babies of different

ages. However, SNS responses to MA appear to be affected

by both time postpartum and breast-feeding frequency.

One complication must be kept in mind—breast feeding

has an impact on processes relating to recovery from

childbirth. It is well known that breast feeding slows the

return of the reproductive function to prepartum levels [39].

That breast feeding interacts with time postpartum is

supported by correlations run separately for exclusive and

nonexclusive mothers. For each category of mothers,

correlations were run, testing the associations between time

postpartum/age of infant and physiological measures.

Table 6 shows the results of these analyses. As the table

shows, time postpartum appears to be related to SNS cardiac

response to MA only in exclusive breast-feeders. In

nonexclusive breast-feeders, age of infant shows no

association with responses to MA. In addition, as the table

shows, in nonexclusive breast-feeders, time postpartum

appears to be associated with PEP response to CP. Thus,

time postpartum has a different association with physio-

logical measures, depending on the breast-feeding status.


This observation suggests that the processes of recovery

from pregnancy and childbirth may differ according to the

amount of lactation. Future studies that control the variable

of time postpartum through the use of prospective,

longitudinal, within-subject designs may tease apart ANS

alterations due to postpartum recovery processes from those

due to breast-feeding behavior.

Mechanisms: oxytocin

The observed ANS cardiovascular changes in breast

feeding may be mediated by both central and peripheral

effects of oxytocin, a hormone necessary for and released by

breast feeding. Several investigations point toward a role of

central oxytocinergic neurons in higher level control of

cardiovascular function through both sympathetic and para-

sympathetic pathways [40–51]. Light et al. [1] reported that

BP was related more reliably to oxytocin responsivity to

stimuli than breast-feeding versus bottle-feeding status.

Moreover, lactation induces alterations in the oxytocinergic

system, including nuclei involved in cardiovascular regu-

lation [52–58]. Finally, there is evidence that oxytocin may

play a role in lactation-induced alterations in behavioral and

physiological responses to stress [35,59–64]. Therefore, it

seems very likely that the observed differences between

breast- and bottle-feeding mothers were mediated, at least in

part, by central changes in the structure and function of the

oxytocinergic system involved in cardiovascular control

[1,7]. Based on the results of the present study, one might

propose that breast feeding induces central oxytocinergic

activity that shifts the ANS balance toward increased PNS

and decreased SNS activity.

Methodological guidelines

Based on these results, improved methods for research on

breast feeding can be suggested. First, to examine the

maternal effects of breast feeding, exclusive breast-feeders

should be the comparison group, as they show the greatest

differences from the controls. Second, nonexclusive breast-

feeders should be considered a separate group because they

appear to exhibit different patterns of autonomic functioning

than do exclusive breast-feeders. Third, breast feeding is a

continuous behavioral pattern and should be considered a

continuous variable in analyses. Fourth, the type (active/

passive or psychological/physical) and phase of the stressor

task (baseline, task, or recovery) determine the pattern of

ANS alterations. Finally, alterations due to recovery

processes (as reflected in age of baby/time postpartum) is

a variable that must be controlled.

Limitations

Because we did not collect data on menses, and there are

menstrual cycle effects on cardiovascular responses

[65–67], our results may be limited. However, the identi-

fication of the cycle phase is very difficult in postpartum, as

spotting and menstrual bleeding may be irregular, and

anovulatory periods may be interspersed among ovulatory

periods. An accurate determination of menstrual status

requires the daily assay of plasma or urinary estrogens,

progesterones, and lutenizing and follicle stimulating

hormones. These assays were beyond the scope of the

present study. In addition, this study employed a cross-

sectional design, with all its inherent flaws. It is possible that

these groups differed on unmeasured individual differences,

especially personality differences, which may account for

the observations. Even possible confounding variables that

were assessed, such as oral contraceptive use or smoking,

were incompletely controlled for in the use of covariates in

statistical analyses.

Task issues

One might argue that a limitation of the work may be in

the relatively short 5-min baseline preceding the tasks.

However, a recent study found equivalent cardiovascular

reactivity to stress following initial baseline periods lasting

from 5 to 16 min [10]. Thus, a longer baseline adaptation

period is not likely to alter findings. Another limitation may

be in the relatively short 1-min recovery following the tasks.

However, the literature on recovery processes clearly

indicates the importance of the initial minute following

the termination of the task. HRs in the initial minute are

predictive of mortality and death [68–71]. Change in HPV

from the minimum during the stress to the first minute of

recovery is associated with risk factors for cardiovascular

disease [72]. Therefore, although the period is short, it is the

critical minute of the recovery process. Future studies are

needed to address how varying lengths of time for

adaptation, task, and recovery measures will modify the

lactation-induced alterations of cardiovascular system

response to stressors.

One of the strengths of the study is the inclusion of two

different types of stressors. Researchers have noted that

lactation-induced alterations of stress response may be

dependent on the type of stressor. Specifically, investigators

have proposed that responses to passive (e.g., CP) rather than

active (e.g., MA) stressors may be affected by lactation [1,5].

In addition, others have proposed that response to physical

stressors (e.g., CP) are chronically dampened by lactation,

while responses to psychosocial stressors (e.g., MA) are

transiently dampened only immediately after breast feeding

[11,12]. The results of this study support the notion that

alterations to the responses to stress are dependent not only on

the type of stressor but also on the amount of breast feeding.

Implications

The clinical implications remain to be seen. Cardiovas-

cular activity is thought to be predictive of future health;

however, it is unclear whether the cardiovascular alterations


in the relatively brief postpartum period have longer lasting

effects. However, if this is the case, then the effects of breast

feeding on increasing PNS and decreasing SNS reactivity

may be cardioprotective [73,74]. If the hypothesis that breast

feeding alters cardiovascular function in a way that is

cardioprotective, then we will have identified a modifiable

behavioral risk factor that can be readily translated into

practice. Rarely does one find a behavior that is cardiopro-

tective, hence, this is valuable information for the area of

women’s health.

If further support is found for a close association between

cardiovascular function and lactational physiology, then it is

possible that we may be able to predict future cardiovascular

disease. That is, infant-feeding method may aid in cardio-

vascular risk stratification for women. Note that it is not

assumed that breast or bottle feeding causes cardiovascular

disease, only that infant feeding method may have

predictive value as a marker. It is possible that the

underlying causes of cardiovascular disease may also be

underlying causes for lactation failure, because of the

reliance of lactation on cardiovascular processes. Thus, the

inability to lactate as a young woman may be associated

with later increased risk for cardiovascular disease.

In addition, the understanding of any possible association

between lactation and cardiovascular function may provide

possible explanations of gender disparities in cardiovascular

health. Research on the association between lactation and

cardiovascular function, furthermore, may yield information

suggesting pharmacological therapies, possibly those based

on oxytocin’s actions, that might be developed for both

females and males.

It is also possible that breast feeding plays a role in the

development of idiopathic peripartum cardiomyopathy

(PPCM; [75]), a rare and poorly characterized form of

cardiomyopathy, which may occur during the last month of

pregnancy to the 5 months after delivery. There is no known

etiology—patients have no demonstrable heart disease

before pregnancy and are without detectable conditions

predicting heart failure. Prognosis is poor, up to 50%

mortality rate. PPCM was initially linked to breast feeding;

however, because a subsequent study did not confirm the

relationship, further investigation is needed to clarify the

association [75]. Information from this study may be

relevant to understanding and managing this disease.

The findings on nonexclusive breast feeding indicate

that there may be cardiovascular alterations that are

deleterious to some populations; this information helps

mothers in their choice of infant feeding. It is possible that

breast feeding, because of enhanced SNS reactivity with

weaning, may be contraindicated in some women with

borderline or frank hypertension.

Given that the choice to breast feed is primarily

determined by culture and logistics (opportunity to breast

feed) and, in particular, the demands of the formal work-

place, this information may not be as relevant to the care of

the individual mother as it is to the legal discussion of

whether to require support for breast-feeding mothers in

public and in the workplace. There are over four million

births in the country, and the sheer number of births makes

the question of possible effects of breast feeding relevant

from a public health perspective.

Conclusions

Exclusive breast feeding appears to increase parasympa-

thetic cardiac modulation and decrease SNS responses to

stress. Nonexclusive breast feeding appears to increase

sympathetic reactivity and autonomic instability in response

to stress. Actual frequency of breast feeding and bottle

feeding is an important variable that shows dose response

associations with cardiovascular ANS measures. Further

research is warranted.

Acknowledgments

This research was supported by a grant from the Applied

Behavioral Medicine Research Institute at the SUNY at

Stony Brook School of Medicine. We would like to thank

Arthur Stone and Joan Broderick for assistance in initiating

this study; Joshua Berg for scoring electrodermal data;

William Guethlein and Glenn Hudson for technical assis-

tance; and Marie Frey, Chris Kocis, Jennifer Lamm, and

Nancy Bowden for assistance in running the procedures.

Special thanks to Lucia and Philip Mezzacappa for their

guidance on the project.

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Breast feeding, bottle feeding, and maternal autonomic responses to stress

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