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© 2001 The American Society for Nutritional Sciences J. Nutr. 131:3012S-3015S, November 2001


Symposium: Human Lactogenesis II: Mechanisms, Determinants and Consequences

Maternal and Fetal Stress Are Associated with Impaired Lactogenesis in Humans1

Kathryn G. Dewey2

Department of Nutrition, University of California, Davis, CA 95616-8669

2To whom correspondence should be addressed. E-mail: kgdewey{at}ucdavis.edu


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 
Studies in animals indicate that various types of stressful stimuli can depress lactation, but there is much less information in humans. Experimental studies in breastfeeding women have shown that acute physical and mental stress can impair the milk ejection reflex by reducing the release of oxytocin during a feed. If this occurs repeatedly, it could reduce milk production by preventing full emptying of the breast at each feed. Prospective observational studies indicate that both maternal and fetal stress during labor and delivery (e.g., urgent Cesarean sections or long duration of labor in vaginal deliveries) are associated with delayed onset of lactation. The effects of chronic emotional stress on lactation are not known. Mothers who experience high levels of stress during and after childbirth should receive additional lactation guidance during the first week or two postpartum.


KEY WORDS: • lactation • breastfeeding • stress • anxiety • oxytocin


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 
There are numerous factors potentially associated with lactogenesis in humans (1Citation ) (Table 1Citation ). On the maternal side, biological factors include parity, mode of delivery, labor experience, body mass index, smoking, breast or nipple abnormalities or surgery, illness, anxiety and stress. Behavioral factors are equally important and include motivation to breastfeed, social support, nursing frequency, the use of supplements such as glucose water or formula, pacifier use and breastfeeding experience. It is important to recognize that the characteristics of the infant also play a role in the establishment of lactation. Biological factors, such as the infant’s birth weight, gestational age and suckling ability, are major determinants of the ability to latch on to the breast effectively and extract milk, thereby stimulating continued milk production. Several factors listed on the maternal side, such as labor medications, may influence lactogenesis via infant suckling ability, in particular, the infant’s alertness and ability to orient (1Citation ). Behavioral characteristics of the infant, such as temperament (e.g., irritability vs. passivity, amount of crying) and suckling style (e.g., gentle vs. firm latch, amplitude and frequency of suckling bouts during a feed) may also play a role, by eliciting different responses from the mother, affecting the efficiency of milk transfer and potentially causing trauma to the nipple.


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Table 1. Maternal and infant factors potentially associated with lactogenesis

 
It is in this context that this article will address the effects of maternal and fetal stress on lactogenesis. Anxiety and stress are listed in Table 1Citation as biological factors because they have physiological components, but they are clearly related to several of the factors listed as behavioral. Because there are complex inter-relationships among the various maternal and infant factors that may affect lactogenesis, it is often not possible to separate the effects of stress from those of other variables. For example, the mode of delivery (vaginal vs. Cesarean section; elective or urgent Cesarean section), duration and difficulty of labor and use of labor medications are strongly associated with one another (Fig. 1Citation ). Maternal and/or fetal stress may trigger or be caused by any of these three variables, which in turn are related to the timing of the first breastfeed and the infant’s suckling ability. When lactogenesis is impaired, leading to delayed onset of milk production and/or insufficient milk volume, it may be due to the combined result of all of these factors. Although the majority of difficulties with lactogenesis can be resolved given sufficient motivation by the mother and appropriate breastfeeding management, many mothers do not have access to adequate lactation guidance and support to help them through this period. For this reason, problems encountered during the initiation of lactation may result in long-term use of supplemental feedings or complete abandonment of breastfeeding. Thus, it is important to understand the role of stress during the period of lactogenesis.



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Figure 1. Example of the inter-relationships among variables that may affect lactogenesis.

 

    Potential mechanisms underlying the association of stress with lactogenesis
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 
A certain amount of stress is normal when considering the events surrounding childbirth and the onset of lactation and is unlikely to have any detrimental effects. However, women and infants whose experience is at the high end of the range for stress may be at greater risk for adverse outcomes. Stress can be categorized as primarily physical or physiological (e.g., pain and exhaustion) or as emotional (e.g., anxiety). It is unknown whether the body’s response to these two types of stress has different effects on lactation.

At least two potential mechanisms can be hypothesized for the relationship between stress and lactogenesis. First, as will be discussed in the next section, maternal stress seems to interfere with the release of oxytocin, the hormone that is responsible for the milk ejection reflex. If the milk ejection reflex is impaired often, the resulting incomplete removal of milk from the breast eventually will lead to down-regulation of milk synthesis. Although milk removal is not necessary to trigger lactogenesis stage II, it may be related to the timing of onset of full milk production or the volume of milk produced (2Citation , 3Citation ). It is likely that maternal stress affects levels of other hormones involved in lactation, such as prolactin (4Citation ), but there is little evidence on this issue in humans (3Citation ).

Second, a newborn who experienced stress during labor and delivery may be too weak or too sleepy to latch on and suckle effectively at the breast. Even if the lactational capacity of the mother is not compromised, this could lead to impaired lactogenesis if milk removal is not adequate.

It should also be recognized that the causal pathway between maternal stress and lactogenesis could be reversed, i.e., mothers who experience delayed onset of milk production are likely to become stressed as a result. In observational studies it is often difficult to determine the temporal relationship between cause and effect.


    Maternal stress and the milk ejection reflex
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 
Animal studies have demonstrated suppression of lactation after exposure to certain types of stressful stimuli (4Citation ). Most of these studies were performed during established lactation, not during lactogenesis. In humans, several studies have examined whether maternal stress affects the milk ejection reflex or the amount of milk transferred during a feed. The first was a unique experiment by Newton and Newton (5Citation ) in 1948, which involved three different types of distractions imposed during the first morning feed on a mother at 7 mo postpartum: immersion of her feet in ice water for 10 s of every 30 s; verbal math problems, accompanied by mild electric shocks if the mother got the wrong answer or took too long in answering, and intermittent pulling of the mother’s big toes, causing sharp pain. On days with one of these distractions, the mother was injected with either saline solution or pitocin (oxytocin) 2 min before the infant began to nurse. Despite the fact that the study included only one woman, the novel design of the experiment provided useful information. Milk intake by the infant at the first morning feed was measured on 8 control days and 12 distraction days (4 d for each of the three treatments). Intake on control days was quite consistent, ranging from 142 to 209 g (mean, 168 g). When saline preceded the distraction, milk intake decreased noticeably (to an average of 99 g), particularly with the ice water treatment (Fig. 2Citation ). However, when pitocin was injected before the distraction, milk intake (average, 153 g) was similar to that of the control days. The authors concluded that the distractions had interfered with the milk ejection reflex, because milk transfer was restored when pitocin was administered.



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Figure 2. Effects of distraction on milk volume transferred during the morning feed in a single mother-infant pair. For the three distractions (ice water, math and electric shock, toe pull), feeds were preceded by injecting the mother with either saline (S) or oxytocin (O); no injection preceded the control feeds. Source: Newton and Newton (5Citation ).

 
The second study (6Citation ) involved mothers of preterm infants (average gestational age, 31 wk) in the neonatal intensive care unit who were regularly expressing their milk using an electric breast pump. Such mothers are typically under a great deal of stress because of the anxiety and fatigue associated with such situations. The investigators randomly assigned 55 women at 3–5 d postpartum to a control or an intervention group. The intervention group received a 20-min audiotape that included a progressive relaxation exercise followed by a guided imagery section. They were encouraged to listen to the tape daily, especially before milk expression. After 1 wk, the volume of milk expressed during a pumping session in the hospital was compared between groups. The average volume was significantly greater in the intervention group than in the control group (99 ± 60 mL vs. 55 ± 48 mL, respectively; P = 0.05). Because milk volume was measured at only a single pumping session, it is not known whether a significant difference would have been seen over a 24-h period. Nonetheless, the results are consistent with the hypothesis that reduced stress enhances milk production.

The third study was a randomized trial with 22 exclusively breastfeeding women studied during a single feed at 5 d postpartum (7Citation ). The women were assigned to one of three groups: control, mental stress (verbal math problems), or noise stress (the sound of building construction, at a mean of 70 dB). Blood samples were collected every 2 min before and after nursing, and milk intake was measured by weighing the infants before and after the feed. Milk yield (average, 36 g) and change in plasma prolactin concentration did not differ significantly among groups. However, the frequency of oxytocin pulses during the 20-min feed was significantly lower in the mothers exposed to stress, by 43% in the mental stress group and 52% in the noise stress group. These results provide additional support for the conclusion reached by Newton and Newton 46 y earlier: that the milk ejection reflex is impaired by maternal stress.


    Effects of stress during labor and delivery on lactogenesis
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 
Data reported in recent years indicate that events during labor and delivery can have a marked impact on lactogenesis. Chen et al. (8Citation ) conducted a prospective study of 40 women in which the lead author observed the labor and delivery of all subjects and took blood samples during pregnancy, parturition (cord and maternal blood) and lactation for analysis of stress hormones. Each day during the first 2 wk postpartum, the mothers collected a milk sample and recorded breastfeeding frequency. On d 5 and 14 postpartum, 24-h milk volume was measured by test weighing. Four markers of lactogenesis were examined: the time postpartum when the subject first felt increased fullness in the breasts, milk volume on d 5, milk lactose concentration on d 5, and the day postpartum when casein first appeared in milk (a marker of the biochemical maturation of the milk). Three of the four markers of lactogenesis were highly correlated with each other (breast fullness, milk volume and milk casein appearance), whereas milk lactose concentration on d 5 was not significantly correlated with any of the other markers. Multiple regression analysis (excluding women with Cesarean deliveries) indicated that several markers of both fetal and maternal stress during labor and delivery (cord glucose concentration, duration of labor and maternal exhaustion score) were associated with delayed breast fullness, lower milk volume on d 5 and/or delayed casein appearance.

Subsequently, Chapman and Perez-Escamilla (9Citation ) conducted a prospective study of 192 women in which maternal perception of the onset of lactation was the primary outcome variable. In this sample, 24% of the mothers chose not to breastfeed. Risk factors for delayed onset of breast fullness (>72 h postpartum) included exclusive formula feeding on d 2, birth weight < 8 lb, unscheduled Cesarean section, prolonged stage II labor (among those with vaginal deliveries), maternal heavy or obese body build and white/Hispanic ethnicity (compared with African-American).

Most recently, our team has investigated the incidence of delayed lactogenesis and insufficient milk intake by the infant in a community-based sample of 280 mother-infant pairs in Davis, CA (1Citation ). Mothers were recruited shortly after delivery in five area hospitals and given lactation guidance by trained professionals in the hospital and in the home on d 3, 7 and 14 and additionally as needed. All infants were healthy, single and born at term (>37 wk) and all mothers planned to breastfeed exclusively for at least 1 mo. Motivation and social support for breastfeeding in this university community are very high. For the data reported here, the major outcome variables were infant suckling ability on d 1 and 3 (assessed using the Infant Breastfeeding Assessment Tool (10Citation ), infant weight change by d 3 and the timing of onset of milk production (defined by when the mother first reported that her breasts were noticeably fuller: 3 on a scale of 5). Delayed onset of milk production (>72 h postpartum) occurred in 24% of the women, and 12% of infants were considered to have excessive weight loss (>=10% of birth weight) by d 3. The percentage of infants identified as having poor suckling ability (<=10 of 12 points on the Infant Breastfeeding Assessment Tool) was 49% on d 1 and 22% on d 3. Several variables reflecting stress were examined as potential predictors of these outcomes, including mode of delivery, duration of labor, pain during labor, exhaustion after delivery, time without sleep before delivery, infant Apgar scores at 1 and 5 min, infant given oxygen, meconium staining of the amniotic fluid and maternal pain, fatigue and stress on d 3 postpartum. Of these variables, duration of labor (both total and stage II), time without sleep and maternal pain and stress on d 3 were significantly associated with a longer interval before onset of breast fullness, and duration of labor and maternal stress on d 3 were also associated with greater infant weight loss by d 3. However, maternal stress on d 3 could be the result of delayed lactogenesis, rather than the cause, so it is difficult to interpret the associations with that variable. In multivariate models, both mode of delivery (particularly an urgent Cesarean section) and duration of labor were linked to delayed onset of breast fullness.

The degree of consistency in the results of these three studies is remarkable, with two major risk factors standing out for delayed lactogenesis: long duration of labor (in vaginal deliveries) and urgent Cesarean section. Both of these are strongly related to the amount of stress experienced by both the mother and the infant during parturition.

Several conclusions can be drawn from the studies described above. First, acute physical and mental stress can impair the milk ejection reflex by affecting release of oxytocin during a feed. If this occurs repeatedly, it could reduce milk production by preventing full emptying of the breast at each feed. Second, both maternal and fetal stress during labor and delivery are associated with impaired lactogenesis. Third, emotional stress postpartum may impair lactogenesis but reverse causation cannot be ruled out. Mothers who experience high levels of stress should receive additional lactation guidance during the first week or two postpartum. With such guidance, nearly all such mother-infant pairs (e.g., those who experience long labor or have an urgent Cesarean section) can be successful at establishing exclusive breastfeeding.


    FOOTNOTES
 
1 Presented as part of the symposium "Human Lactogenesis II: Mechanisms, Determinants and Consequences" given at the Experimental Biology 2001 meeting, Orlando, FL on April 2, 2001. This symposium was sponsored by the American Society for Nutritional Sciences and was supported by educational grants from Medela, Ross Labs and Wyeth Nutrition International. Guest editors for this symposium publication were Nancy F. Butte, Baylor College of Medicine, Houston, TX and Rafael Perez-Escamilla, University of Connecticut, Storrs, CT. Back


    LITERATURE CITED
 TOP
 ABSTRACT
 INTRODUCTION
 Potential mechanisms underlying...
 Maternal stress and the...
 Effects of stress during...
 LITERATURE CITED
 

1. Dewey, K. G., Nommsen-Rivers, L. A., Heinig, M. J. & Cohen, R. J. (2001) Lactogenesis and infant weight change in the first weeks of life. Davis, M. K. Wright, A. L. Isaacs, C. E. Hanson, L. eds. Integrating Population Outcomes, Biological Mechanisms, and Research Methods in the Study of Human Milk and Lactation 2001 Kluwer Academic/Plenum Publishers New York, NY. (in press). .

2. Neville, M. & Morton, J. (2001) Lactogenesis: the transition from pregnancy to lactation. Pediatr. Clin. North Am. 48:35-52.[Medline]

3. Chapman, D.J. & Perez-Escamilla, R. (2000) Lactogenesis stage II: hormonal regulation, determinants and public health consequences. Recent Res. Dev. Nutr. 3:43-63.

4. Lau, C. (2001) Effects of stress on lactation. Pediatr. Clin. North Am. 48:221-234.[Medline]

5. Newton, M. & Newton, N. R. (1948) The let-down reflex in human lactation. J. Pediatr. 33:698-704.[Medline]

6. Feher, S.D.K., Berger, L. R., Johnson, J. D. & Wilde, J. B. (1989) Increasing breast milk production for premature infants with a relaxation/imagery audiotape. Pediatrics 83:57-60.[Abstract/Free Full Text]

7. Ueda, T., Yokoyama, Y., Irahara, M. & Aono, T. (1994) Influence of psychological stress on suckling-induced pulsatile oxytocin release. Obstet. Gynecol. 84:259-262.[Medline]

8. Chen, D. C., Nommsen-Rivers, L., Dewey, K. G. & Lonnerdal, B. (1998) Stress during labor and delivery and early lactation performance. Am. J. Clin. Nutr. 68:335-344.[Abstract]

9. Chapman, D. J. & Perez-Escamilla, R. (1999) Identification of risk factors for delayed onset of lactation. J. Am. Diet. Assoc. 99:450-454.[Medline]

10. Matthews, M. K. (1988) Developing an instrument to assess infant breastfeeding behavior in the early neonatal period. Midwifery 4:154-165.[Medline]




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