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Department of Nutritional Sciences, University of Connecticut, Storrs, CT 06269
5To whom correspondence should be addressed. E-mail: rperez{at}canr.uconn.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • breast-feeding • cortisol • lactogenesis stage II • onset of lactation • stress
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Pérez-Escamilla et al. (2
) found in a longitudinal study in Hermosillo, Mexico, that the OL occurred later among those who were feeding formula to their babies by 1 wk pp compared with their fully breast-fed counterparts (3.3 vs. 2.9 d pp, respectively; P 
0.05). As in Honduras, the early use of formula was associated with an earlier termination of breast-feeding. In Hartford, CT, among women who were planning to breast-feed their children for at least 6 mo at the time of delivery, a delayed OL was significantly associated with a shorter duration of breast-feeding (3.4 mo vs. 11.7 mo, respectively; P < 0.001) (3
).
The negative influence of a delayed OL on breast-feeding outcomes is perhaps explained by a higher likelihood of women becoming anxious about the adequacy of their milk supply followed by the introduction of infant formulas which in turn may lead to a further delay in OL (1
–3
). Different factors such as parity, birth weight, mode of delivery (4
,5
), infant feeding practices (2
,4
), insulin-dependent diabetes mellitus (6
,7
), maternal obesity (8
,9
) and maternal and/or infant stress (4
,10
) have been associated with a delayed OL.
The negative association between stress and milk production has been recognized for many years (11
), but few studies have been performed in humans to attempt to understand the influence of stress during labor and delivery on OL. Chapman and Pérez-Escamilla (4
) conducted a prospective study to identify the risk factors for delayed OL among U.S. women. Multivariate logistic regression analyses indicated that unscheduled cesarean section delivery and vaginal delivery with prolonged second stage of labor (i.e., "pushing" stage) were risk factors for delayed OL. Chen et al. (10
) found an association among longer labor duration, maternal exhaustion, increased stress hormones, reduced breast-feeding frequency and delayed OL. To our knowledge, these relationships have not been tested in a developing country setting.
The objective of this project was to conduct a longitudinal study to examine the influence of stress during labor and delivery on OL among urban Guatemalan women.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This study was approved by the Institutional Review Boards from the University of Connecticut, the Institute of Nutrition of Central America and Panama and the Instituto Guatemalteco de Seguridad Social. The study followed a longitudinal design and was conducted in Guatemala City between June and August 2000 in the labor and pp units of an Instituto Guatemalteco de Seguridad Social tertiary teaching hospital where 
12,000 babies are born per year. The hospital maternity ward serves mainly low-income employed women and housewives who live in periurban areas surrounding Guatemala City.
Subjects who participated in the study met the following criteria: 1) telephone at home; 2) experiencing first stage of labor at time of recruitment; 3) term pregnancy (37–42 wk of gestation age by last menstrual period); 4) no medical or obstetric complications precluding breast-feeding, including being positive for the human immunodeficiency virus; 5) healthy newborn (born at term, birth weight >2500 g, 1-min Apgar score 
7).
A total of 364 low-income pregnant women were contacted upon arrival to the low-risk labor unit. A screening questionnaire was administered to identify women who met the study selection criteria. Of the women who were contacted, 170 met these criteria and of these 16 did not complete the hospital follow-up because the baby was born after midnight or during the weekend. Eighteen women completed the hospital follow-up, but when personnel from the project tried to contact them, the telephone number was wrong or out of service or the mother decided to stay with other relatives. Thus, 136 women completed the hospital phase and the home telephone follow-up phase of the study (Fig. 1
).
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Saliva samples were obtained using a Salivette, which consists of a plastic stopper, a tube insert, a centrifuge tube and a cotton cylinder. Women received instruction to hold the cotton cylinder under the tongue for 2–3 min and were encouraged to wet the cotton cylinder with saliva. The cotton cylinder was then placed in the tube insert and kept in a cooler with an ice pack for 4–6 h before being transported to the laboratory. Once in the laboratory, the tubes were refrigerated at -4°C for 10–12 h and centrifuged at room temperature for 15 min at 3000 rpm. Three salivary aliquots were separated in plastic vials and frozen at -20°C. Two sets of salivary samples were shipped from Guatemala to Storrs, CT, in a frozen state and then sent for cortisol determinations to Pennsylvania State University, University Park, PA, in a cooler with dry ice.
Maternal psychosocial stress was measured during labor and early and late pp with a 17-item questionnaire adapted from Hodnett and Simmons-Tropea (12
) and Rini et al. (13
) and pretested in this population. A modified shorter version was used during telephone follow-ups.
Medical charts were used to obtain information about type, date and time of delivery, type of anesthesia if any, vaginal tears or episiotomy, newborn’s health status, gestational age at birth based on newborn’s physical examination and date of last menstrual period, birth weight and Apgar scores 1 and 5 min after birth. A questionnaire was applied during the postnatal hospital stay to gather data on demographics, socioeconomic status, breast-feeding knowledge and infant feeding plans and intentions.
Questions about OL symptoms were asked during the hospital stay and daily via telephone after hospital discharge until the mother reported OL following the methodology developed and validated by Chapman and Pérez-Escamilla (14
,15
). With this method, after the birth of the child subjects are interviewed at least once daily regarding breast symptoms (i.e., breast fullness, swelling, leakage) to evaluate clinical signs of lactogenesis. This symptom checklist is followed by the following question: "Has your milk come in yet?" If the response is positive, the subject is asked to explain how she knows that her milk has "come in" and the timing of OL is recorded in hours. Pérez-Escamilla and Chapman (15
) have recently documented that the vast majority of women can identify when OL occurs and that they report similar symptoms of OL across cultures that are fully consistent with the physiology of lactogenesis stage II. Furthermore, conclusions reached from studies examining risk factors for delayed OL are remarkably similar when comparing maternal perception with more invasive procedures for measuring OL (i.e., infant test weighing, changes in milk composition).
Five community nutrition experts, of whom two are experts in breast-feeding research in Latin America, tested instruments for content validity. A pilot study was conducted before formal data collection with a convenience sample of 20 women contacted at different stages of labor and delivery to assess the clarity of the questionnaires and the need for further revision of them (i.e., face validity), data collection procedures and/or salivary sample collection techniques. The field coordinator and one of the study’s research assistants were standardized in the administration of the screening and stress and anxiety forms. A second research assistant was trained on the application of the hospital and home phone follow-up forms. The standardization procedure involved applying the survey by either the field coordinator or an interviewer while both recorded simultaneously the responses provided by each woman. Results were compared between interviewers and field coordinator. A minimum level of 95% agreement in responses was used before proceeding with formal data collection. Data collected during the pilot phase was not included in the final analyses.
Laboratory procedures
Salimetrics’ HS-Cortisol Kits (Salimetrics, State College, PA) were used to measure salivary cortisol. This enzyme immunoassay uses 25 µL of saliva per test. The principle of this method is that cortisol standards and salivary cortisol compete with cortisol linked to horseradish peroxidase for rabbit antibody binding sites to cortisol. Bound cortisol peroxidase is measured through optical density read on a standard plate reader at 450 nm. The amount of cortisol peroxidase detected is inversely proportional to the amount of cortisol present (16
). The assay has a range of sensitivity from 0.194 to 200 nmol/L. Method accuracy, determined by spike recovery, and linearity, determined by serial dilution, are 105 and 95%, respectively. Values from matched serum and saliva samples show the expected strong linear relationship (r = 0.94; P < 0.0001). All samples were tested in duplicate, and duplicate test values that varied by >7% were subject to repeat testing. The average intra- and interassay coefficients of variation were 7.99 and 8.89%, respectively. The mean of the duplicate tests was used in the statistical analyses.
Statistical analyses
The study field director (R. Grajeda) entered and cleaned the data using Epi-Info for Windows version 1.0 (17
). All analyses were conducted with SPSS for Windows version 10.0.7 (18
).
Analyses were based on the 136 women who completed both the hospital and phone follow-up phases of the study. Salivary cortisol levels were plotted by parity and against time before or after delivery. Mean cortisol concentrations were compared by parity at each time point using the Student t test. Sample size for first time of collection (i.e., 3 h antepartum) was 112 because 11% of women could not wet the cotton cylinder due to dehydration and an additional 6.6% had unphysiologically high cortisol levels indicative of blood contamination, most likely as a result of biting the mouth walls during contractions. For the sample taken 2 h pp (i.e., soon after the "pushing" effort) the corresponding figures were 12.5 and 16.9%, respectively, yielding a sample size of 96. As expected, dehydration or blood contamination was not a problem with the sample taken 17 h pp. At this point only three women had to be excluded from the analytical sample (n = 133).
Bivariate analyses were conducted to examine the association between the independent variables and OL expressed both as a categorical (OL 3 d vs. >3 d pp) and as a continuous variable. In agreement with previous studies (15
) the OL cut-off of 3 d pp was selected because it is likely that the level of concern of the mother and support individuals about the adequacy of the maternal milk supply for the infant will start increasing dramatically if the milk has not come in by this time (4
). Chi-square analyses were conducted when OL was expressed categorically and Student’s t test or analysis of variance when OL was continuous. Key independent variables examined were parity (primiparous vs. multiparous women), salivary cortisol levels at different time points (40th percentile vs. >40th percentile), type of delivery (vaginal, scheduled cesarean section, emergency cesarean section), second stage of labor duration (i.e., "pushing time"), infant gender, medications administered during labor and delivery, socioeconomic status, mother’s age, cervical dilation upon recruitment and every item of the stress questionnaire. The 40th percentile of salivary cortisol was based on the distribution of this variable in the whole analytical sample and was selected based on a) exploratory analyses with this data set and b) the fact that using a lower cortisol cut-off would have left practically all primiparous women out of the analyses (because the overwhelming majority of primiparae were above the 35th percentile) (19
).
Based on these exploratory bivariate analyses, two multivariate models were tested. The general linear model (GLM) was used to examine OL as a continuous variable by parity and delivery mode after adjusting for maternal age and cervical dilation upon recruitment (i.e., when the first salivary sample was taken). Multivariate logistic regression was used to test the same hypothesis using OL as a dichotomous variable (3 vs. >3 d pp). Likewise, multivariate logistic regression was used to test the association between salivary cortisol levels upon recruitment and OL after adjusting for maternal age and cervical dilation at the time when the first salivary sample was obtained. These two variables were controlled for in the multivariate analyses because they were the only two covariates significantly associated with OL in the bivariate analyses. Similar conclusions were reached with both GLM and logistic regression analyses; thus, only the former results are presented. Differences were considered to be significant when the two-sided probability value was 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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On average, women were in their middle 20s and had 9 y of formal education, two pregnancies and 4 cm of cervical dilation upon recruitment. There were no differences in these variables between women who met the study criteria and those who left the study. However, women who dropped tended to have less education (P = 0.10) (Table 1
).
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).
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Cortisol levels during labor and delivery and pp
Salivary cortisol concentration increased from 27.8 ± 2.2 nmol/L in the first stage of labor to 64.1 ± 4.2 nmol/L soon after the delivery of the placenta, followed by a decline to 12.6 ± 1.3 nmol/L in the following 17 h. Primiparous women had higher antepartum and early postnatal cortisol levels that were almost twice as high as those among multiparous women (P < 0.05). The parity difference in salivary cortisol concentrations vanished with time (Fig. 2
).
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OL occurred at 2.7 ± 1.1 d pp (range 0.9–8.1 d pp); 27% of the women had a delayed OL (i.e., >3 d pp). Among primiparae, OL tended to occur (P = 0.23) 5.4 h later than among multiparae (2.8 ± 1.1 vs. 2.6 ± 1 d pp) (Table 2)
.
The symptoms most commonly associated with OL were breast fullness (99%), breast heaviness (97%), infant being full (92.6%), breast pain (91.9%), increase in breast temperature (89%), milk leakage (88.2%), milk in baby’s mouth (86%), breast tingling (56.6%) and increase in body temperature (41.9%).
Stress and OL
Multivariate GLM analysis results found a significant association (P = 0.04) between parity/delivery mode and OL (Table 3
). Multiparous women (irrespective of mode of delivery) had an earlier OL than primiparae who underwent emergency cesarean section deliveries. Likewise, primiparous women with vaginal deliveries tended to have (P = 0.163) an earlier OL than their counterparts who underwent an emergency cesarean section delivery (Fig. 3
).
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[adjusted OL timing (mean ± SEM): 3 ± 0.2 d pp (n = 28) vs. 2.4 ± 0.2 d pp (n = 38), respectively; P = 0.02]. Among primiparae, cortisol levels were not associated with the timing of OL [2.8 ± 0.2 d pp (n = 38) vs. 3 ± 0.4 d pp (n = 7), respectively; P = 0.73].
In the multivariate analyses, maternal age was positively associated with OL but cervical dilation upon recruitment was no longer associated with OL (Table 3)
.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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,10
), results strongly suggest that stress during labor and delivery is a significant risk factor for a delayed OL. First, primiparous women who underwent emergency cesarean section deliveries were more likely than the rest of the sample to have a significantly delayed OL. A recent analytical overview indicates that previous studies (15
) have identified mode of delivery (i.e., emergency cesarean section delivery, vaginal deliveries with prolonged second stage of labor) and primiparity as independent risk factors of delayed OL. In this study, it was the interaction between primiparity and a stressful delivery (i.e., emergency cesarean section delivery) that was associated with an increased risk of delayed OL.
In this study there were no subjects who had a vaginal delivery that pushed for >30 min. The active management of labor and delivery in the study hospital, which included widespread use of oxytocin and other labor inducers, perhaps explains this finding (19
). Thus, the hypothesis that a prolonged second stage of labor is a risk factor for delayed OL among women undergoing vaginal deliveries (4
) could not be tested with these data.
Second, among multiparous women cortisol levels were positively associated with the timing of OL. Through this study it is not possible to establish whether high cortisol levels are causally linked with a delayed lactogenesis stage II among multiparae. Cortisol is required for lactogenesis to occur (20
); thus, it is not known whether cortisol is simply a marker of other stress hormones or cortisol concentration beyond a threshold level impairs lactogenesis stage II. Indeed, it is possible that the relatively high cortisol levels among primiparous women, which were twice as high in the antepartum and early postnatal period compared with multiparae, explains why the association between this stress hormone and OL was not found in this subgroup. Further mechanistic research is clearly needed in this area.
OL in this population of low-income Guatemalan women occurred 2.7 ± 1.1 d pp and the incidence of delayed OL was 27%, both of which fall well within the range previously reported (15
). OL symptoms reported by Guatemalan women, such as breast fullness, are in agreement with those reported in industrialized countries, confirming that women perceive OL using similar cues across cultures (15
).
Salivary cortisol levels increased dramatically from the time of recruitment during the first stage of labor until the delivery of the placenta and then returned to baseline levels between 17 and 30 h pp. Cortisol levels were significantly and positively associated with cervical dilation upon recruitment and with several items of the psychosocial and anxiety scales (19
). These observations indicate that salivary cortisol is a valid stress indicator during labor and delivery.
Study limitations
Subjects’ access to a telephone was a key selection criterion in this study. Thus, the findings may have been biased toward a relatively more "privileged" group among the low-income population served by the social security system in Guatemala City. Thus, although no major differences in socioeconomic and demographic characteristics were observed between subjects who participated and did not participate in the study, the results of this study can not be generalized to the whole low-income population served by public hospitals or neighborhood maternity clinics in Guatemala City.
The salivary cortisol technique is a useful approach to study stress and reproductive outcomes (including human lactation) prospectively. There were two limitations of the method used in this study: 1) the inability of a small percentage of women to provide a saliva sample due to dehydration during labor and delivery and 2) the likelihood of blood contamination of saliva samples, perhaps as a result of biting the internal surfaces of the mouth during labor and "pushing" contractions. By contrast, 17 h after delivery the overwhelming majority of women were able to provide adequate saliva samples. Thus, special precautions need to be taken when applying this technique during labor and delivery. Measures could include ensuring that women understand that they need to wet the cotton cylinder, providing subjects with neutral gum or other substances that facilitate saliva production but do not interfere with the assay and asking women to try to prevent biting their mouths’ inner surfaces.
In conclusion, this study has important public health implications because women who experience psychosocial and/or birth-related biological stress during labor and delivery are likely to experience a delayed OL. Mechanistic research is needed to gain a better understanding of the neuroendocrinological mechanisms that may be responsible for the association between stress and impaired lactogenesis stage II. Results from this line of inquiry are likely to have profound infant feeding implications because preventing a delayed OL is likely to have a positive impact on breast-feeding outcomes (1
–3
).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by financial and in-kind support from the Institute of Nutrition of Central America and Panama (Guatemala City, Guatemala) for the implementation of this study.
3 Contribution #2098 from the Storrs Agricultural Experiment Station.
4 Current address: Institute of Nutrition of Central America and Panama, Guatemala City, Guatemala.
6 Abbreviations used: GLM, general linear model; OL, onset of lactation; pp, postpartum.
Manuscript received 15 May 2002. Initial review completed 17 June 2002. Revision accepted 26 June 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Pérez-Escamilla, R., Segura-Millán, S., Canahuati, J. & Allen, H. (1996) Prelacteal feeds are negatively associated with breastfeeding outcomes in Honduras. J. Nutr. 126:2765-2773.
2. Pérez-Escamilla, R., Segura-Millán, S., Pollitt, E. & Dewey, K. G. (1993) Determinant of lactation performance across time in an urban population from Mexico. Soc. Sci. Med. 37:1069-1078.
3. Chapman, D. J. & Pérez-Escamilla, R. (1999) Does delayed perception of the onset of lactation shorten breastfeeding duration?. J. Hum. Lact. 15:107-111.
4. Chapman, D. J. & Pérez-Escamilla, R. (1999) Identification of risk factors for delayed onset of lactation. J. Am. Diet. Assoc. 99:450-454.[Medline]
5. Hildebrandt, H. M. (1999) Maternal perception of lactogenesis time: a clinical report. J. Hum. Lact. 15:317-323.
6. Arthur, P. G., Smith, M. & Hartmann, P. E. (1989) Milk lactose, citrate and glucose as markers of lactogenesis in normal and diabetic women. J. Pediatr. Gastroenterol. Nutr. 9:488-496.[Medline]
7. Ferris, A. M., Neubauer, S. H., Bendel, R. B., Green, K. W., Ingardia, C. J. & Reece, E. A. (1993) Perinatal lactation protocol and outcome in mothers with and without insulin-dependent diabetes mellitus. Am. J. Clin. Nutr. 58:43-48.
8. Ferris, A. M., McCabe, L. T., Allen, L. H. & Pelto, G. H. (1987) Biological and sociocultural determinants of successful lactation among women in eastern Connecticut. J. Am. Diet. Assoc. 87:316-321.[Medline]
9. Rasmussen, K. M., Hilson, J. A. & Kjolhede, C. L. (2001) Obesity may impair lactogenesis II. J. Nutr. 131:3009S-3011S.
10. Chen, D. C., Nommsen-Rivers, L., Dewey, K. G. & Lönnerdal, B. (1998) Stress during labor and delivery and early lactation performance. Am. J. Clin. Nutr. 68:335-344.[Abstract]
11. Dewey, K. G. (2001) Maternal and fetal stress are associated with impaired lactogenesis in humans. J. Nutr. 131:3012S-3015S.
12. Hodnett, E. D. & Simmons-Tropea, D. A. (1987) The Labour Agentry Scale: psychometric properties of an instrument measuring control during childbirth. Res. Nurs. Health 10:301-310.[Medline]
13. Rini, C. K., Dunkel-Schetter, C., Wadhwa, P. D. & Sandman, C. A. (1999) Psychological adaptation and birth outcomes: the role of personal resources, stress, and sociocultural context in pregnancy. Health Psychol 18:333-345.[Medline]
14. Chapman, D. J. & Pérez-Escamilla, R. (2000) Maternal perception of the onset of lactation is a valid, public health indicator of lactogenesis stage II. J. Nutr. 130:2972-2980.
15. Pérez-Escamilla, R. & Chapman, D. J. (2001) Validity and public health implications of maternal perception of the onset of lactation: an international analytical overview. J. Nutr. 131:3021S-3024S.
16. Granger, D. A., Schwartz, E. B., Booth, A., Curran, M. & Zakaria, D. (1999) Assessing dehydroepiandrosterone in saliva: a simple radioimmunoassay for use in studies of children, adolescents, and adults. Psychoneuroendocrinology 24:567-579.[Medline]
17. Epi-Info for Windows 95/98/NT/2000 2001 World Health Organization Geneva, Switzerland. .
18. SPSS Inc.. SPSS for Windows: version 10.0 1999 SPSS Chicago, IL. .
19. Grajeda, R. (2001) The Influence of Stress During Labor and Delivery on the Onset of Lactation. Master’s thesis 2001 University of Connecticut Storrs, CT. .
20. Neville, M. C. & Berga, S. E. (1983) Cellular and molecular aspects of hormonal control of mammary function. Neville, M. C. Neifert, M. R. eds. Lactation: Physiology, Nutrition and Breast-Feeding 1983:103-140 Plenum Press New York, NY. .
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