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Maternal Psychological Distress and Lactation and Breastfeeding Outcomes: a Narrative Review

      Abstract

      Purpose

      Despite recommendations from the World Health Organization and the American Academy of Pediatrics to exclusively breastfeed infants for their first 6 months of life, 75% of women do not meet exclusive breastfeeding guidelines, and 60% do not meet their own breastfeeding goals. Numerous observational studies have linked maternal psychological distress (eg, perceived stress, anxiety, and depression) with nonoptimal breastfeeding outcomes, such as decreased proportion and duration of exclusive breastfeeding. The physiological mechanisms underlying these associations, however, remain unclear.

      Methods

      For this narrative review, we evaluated the evidence of relationships between maternal psychological distress and lactation and breastfeeding outcomes in pregnancy and post partum and the possible physiological mechanisms that facilitate these relationships. We searched PubMed using the following terms: stress, anxiety, depression, breastfeeding, and lactation. Additional search by hand was conducted to ensure a thorough review of the literature.

      Findings

      Among the studies examined, methods used to assess maternal psychological distress were not uniform, with some studies examining perceived distress via a variety of validated tools and others measuring biological measures of distress, such as cortisol. Evidence supports a role for psychological distress in multiple breastfeeding outcomes, including delayed secretory activation and decreased duration of exclusive breastfeeding. One physiological mechanism proposed to explain these relationships is that psychological distress may impair the release of oxytocin, a hormone that plays a critical role in milk ejection during lactation. Continued impairment of milk ejection may lead to decreased milk production because of incomplete emptying of the breast during each feed. Maternal distress may also yield elevated levels of serum cortisol and decreased insulin sensitivity, which are associated with decreased milk production. The relationship between psychological distress and breastfeeding is likely to be bidirectional, however, in that breastfeeding appears to reduce maternal distress, again possibly via effects on the pleasure or reward pathway and calming effects of oxytocin on the mother. This finding suggests that interventions to support lactation and breastfeeding goals in women who score high on measures of psychological distress would be beneficial for both maternal and infant well-being.

      Implications

      Evidence to date suggests that maternal psychological distress may impair lactation and breastfeeding outcomes, but stronger study designs and rigorous assessment methods are needed. A better understanding of the physiological mechanisms leading to impaired lactation may assist in the development of early interventions for mothers experiencing distress. In addition, stress-reducing programs and policies should be investigated for their potential to improve breastfeeding outcomes.

      Key words

      Introduction

      Both the World Health Organization and American Academy of Pediatrics recommend exclusive breastfeeding until an infant reaches 6 months of age.
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      World Health Organization. Breastfeeding. Accessed June 3, 2021. https://www.who.int/health-topics/breastfeeding#tab=tab_1

      Breastfeeding is associated with many health benefits, including decreased risk of type 1 diabetes,
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      gastrointestinal infections,
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      cardiovascular disease,
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      for the mother. Despite the known benefits of human milk for infants, only 25% of infants are exclusively breastfed at 6 months of age, and 60% of women do not meet their own breastfeeding goals.
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      Centers for Disease Control and Prevention. Breastfeeding Report Card; 2020. Accessed October 21, 2020. https://www.cdc.gov/breastfeeding/data/reportcard.htm

      US breastfeeding data for infants born in 2017 reveal that 85% of mothers initiated breastfeeding, but nearly 20% provided formula before their infants were 2 days of age, and <50% were exclusively breastfeeding when their infants were 3 months of age.

      Centers for Disease Control and Prevention. Breastfeeding Report Card; 2020. Accessed October 21, 2020. https://www.cdc.gov/breastfeeding/data/reportcard.htm

      ,

      Centers for Disease Control and Prevention. Breastfeeding: Why It Matters. Accessed June 3, 2021. https://www.cdc.gov/breastfeeding/about-breastfeeding/why-it-matters.html

      In the United States, it is estimated that low rates of breastfeeding add >$3 billion annually to medical care costs for mothers and infants.

      Centers for Disease Control and Prevention. Breastfeeding: Why It Matters. Accessed June 3, 2021. https://www.cdc.gov/breastfeeding/about-breastfeeding/why-it-matters.html

      Several studies have examined reasons for nonoptimal breastfeeding outcomes (nonexclusive breastfeeding and/or breastfeeding cessation), which include barriers such as unsupportive employment and hospital policies, lactation difficulties, and maternal or health care worker concerns about infant growth and nutrition.
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      In addition, large disparities in breastfeeding rates exist across racial and ethnic groups, with non-Hispanic black mothers and Native American/American Indian mothers less likely to ever breastfeed compared with other groups.

      Centers for Disease Control and Prevention. Breastfeeding: Facts . Accessed June 3, 2021. https://www.cdc.gov/breastfeeding/data/facts.html#stopearly

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      Maternal psychological distress (eg, perceived stress, anxiety, and depression) has also been linked to lactation difficulty and breastfeeding cessation.
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      Maternal and fetal stress are associated with impaired lactogenesis in humans.
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      A moderated mediation model of maternal perinatal stress, anxiety, infant perceptions and breastfeeding.
      Despite being potentially modifiable, the associations between maternal distress and breastfeeding outcomes are unclear. Thus, in this narrative review we focus our attention on these relationships and the potential physiological processes that drive them.

      Lactation and the Mother-Infant Dyad

      Successful lactation begins long before the infant is born. The first stage is controlled primarily via increases in estrogen and progesterone secreted from the placenta
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      and involves rapid differentiation of the mammary epithelium within the highly branched lobular and ductal network of the developing mammary gland. The basal layer of the ductal epithelium becomes the myoepithelium, responsible for milk ejection. The luminal layer of the mammary epithelium is composed of epithelial secretory cells called lactocytes, which synthesize and secrete milk components into the lumen of the alveoli.
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      High progesterone concentrations during pregnancy inhibit milk secretion, leading to accumulation of small amounts of colostrum and no milk production.
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      Mechanism of milk secretion.
      Within 48 to 72 hours after parturition, maternal progesterone levels decrease 10-fold, initiating secretory activation in the mammary gland, with copious production of milk.
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      Studies in human lactation: Milk volumes in lactating women during the onset of lactation and full lactation.
      Prolactin facilitates sustained lactation as progesterone levels decrease and can regulate many aspects of milk synthesis and secretion, although its primacy as a driver of lactation has come under scrutiny of late.
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      During early lactation, glucocorticoids assist in the closure of tight junctions between lactocytes, which prevents the leakage of milk components, whereas insulin is observed to facilitate the expression of genes involved in milk protein synthesis.
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      Many other hormones play a role, including cortisol, thyroid hormone, and possibly serotonin.
      • IA F
      • MC N
      Introduction: hormonal regulation of mammary development and milk protein gene expression at the whole animal and molecular levels.
      Disruption of these hormonally controlled processes may lead to delayed onset of milk production and insufficient milk volume.
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      Sustained adequate milk production depends first on efficient nutrient partitioning and uptake by the mammary gland and second on frequent and complete emptying of milk from the breast and thus rests on the biobehavioral interaction within the mother-infant dyad.
      • Newton ER
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      Infant suckling stimulates neurons in the areola to trigger the release of oxytocin from maternal hypothalamic neurons in the pleasure or reward pathway, leading to calming effects for the nursing mother.
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      • Prime D.
      Oxytocin effects in mothers and infants during breastfeeding.
      Infant suckling also prompts oxytocin release from the posterior pituitary into maternal circulation, which causes contraction of the myoepithelial cells surrounding the alveoli to allow milk to be ejected into the ducts for passage to the infant.
      • Moberg K
      • Prime D.
      Oxytocin effects in mothers and infants during breastfeeding.
      ,
      • Ramsay DT
      • Kent JC
      • Owens RA
      • Hartmann PE.
      Ultrasound Imaging of Milk Ejection in the Breast of Lactating Women.
      If emptying of the breast is partial or infrequent, milk accumulates in the ducts, distending them and exposing the mammary gland to increased concentrations of a small whey protein called feedback inhibition of lactation. Feedback inhibition of lactation provides autocrine feedback control on milk production to match maternal milk supply with infant milk demand.
      • Linzell JL
      • Peaker M.
      Mechanism of milk secretion.
      Successful establishment and continuation of lactation therefore rely on a complex hormonally driven orchestration of glandular development during pregnancy and then secretory activation in the early postpartum period, which must be accompanied by prompt initiation of breastfeeding after delivery, proper infant positioning on the breast and efficient latching to achieve efficient milk removal, positive maternal-infant interaction during feeding, and continued frequent nursing.
      Institute of Medicine (US) Committee on Nutritional Status During Pregnancy and Lactation
      Milk Volume.
      Given the deeply biobehavioral and interactive nature of lactation, it is reasonable to consider both maternal and infant psychological health and well-being as potentially important drivers of breastfeeding success.

      Maternal Psychological Distress

      For this narrative review, we use the term psychological distress to refer to different psychological or physiological responses to stressful challenges, such as cognitive appraisals of stress (ie, perceived stress), symptoms of anxiety or depression, and cortisol levels.

      Gunnar M, Quevedo K. The Neurobiology of Stress and Development. Published online 2006. doi:10.1146/annurev.psych.58.110405.085605.

      ,
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      Depression, anxiety, and perceived stress are commonly grouped together to characterize maternal distress in perinatal research, and these symptoms are highly comorbid in the perinatal period.
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      • Ystrom E.
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      Psychological distress is commonly measured by assessing maternal perception via psychometric instruments
      • Nast I
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      • Hellhammer DH.
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      or using biological markers such as cortisol (serum, saliva, or hair).
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      ,
      • Levine A
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      Measuring cortisol in human psychobiological studies.
      In response to stress, neurobiological systems activate to protect the body and promote adaptation, facilitated by the sympathetic adrenomedullary system and the hypothalamic-pituitary-adrenocortical (HPA) axis.
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      Neuroendocrinology and pathophysiology of the stress system.
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      As part of the sympathetic nervous system, the sympathetic adrenomedullary system releases epinephrine, which signals the fight or flight response,
      • Cannon WB.
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      whereas the HPA axis is a component of the central nervous system and produces cortisol in response to stress.
      • Stratakis CA
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      Neuroendocrinology and pathophysiology of the stress system.
      Repeated or long-term exposure to stress creates a cumulative burden on the body, increasing its allostatic load and increasing the risk for disease.
      • McEwen BS
      • Seeman T.
      Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load.
      Maternal psychological distress during pregnancy has been associated with negative birth outcomes, such as low birth weight, preterm birth, and later risk for neurodevelopmental, psychiatric, cardiovascular, and metabolic disease.
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      • O'Connor TG
      The persisting effect of maternal mood in pregnancy on childhood psychopathology.
      Activation of the HPA axis leading to increased maternal cortisol concentrations is the most commonly studied physiological mechanism for assessing the effects of maternal psychological distress on infant outcomes.
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      • Riksen-Walraven JM
      • de Weerth C.
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      Maternal cortisol can be directly transported across the placenta to enter fetal circulation and has been observed to account for approximately 40% of the variance in fetal cortisol concentrations.
      • Gitau R
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      • Glover V.
      Fetal exposure to maternal cortisol.
      Although most maternal cortisol is metabolized during passage through the placenta, increased maternal cortisol concentrations may still have a significant effect on fetal concentrations.
      • Murphy BE
      • Clark SJ
      • Donald IR
      • Pinsky M
      • Vedady D.
      Conversion of maternal cortisol to cortisone during placental transfer to the human fetus.
      Furthermore, an increasing body of evidence suggests that maternal HPA axis dysregulation is not the only physiological mechanism responsible for adverse infant outcomes, and indirect mechanisms, such as colonization of the infant gut by maternal microbes, may be affected by maternal distress.
      • Zijlmans MAC
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      • Riksen-Walraven JM
      • de Vos WM
      • de Weerth C.
      Maternal prenatal stress is associated with the infant intestinal microbiota.
      The physiological mechanisms explaining the observed relationships between maternal psychological distress and adverse breastfeeding outcomes remain unclear.
      • Dozier AM
      • Nelson A
      • Brownell E.
      The Relationship between Life Stress and Breastfeeding Outcomes among Low-Income Mothers.
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      • Riedstra JP
      • Aubuchon-Endsley NL.
      A moderated mediation model of maternal perinatal stress, anxiety, infant perceptions and breastfeeding.
      Elucidating these mechanisms may assist in better development of early interventions targeted at improving breastfeeding outcomes among mothers at risk for experiencing psychological distress. Thus, for this narrative review, we aimed to evaluate the evidence of relationships between psychological distress and nonoptimal breastfeeding outcomes in humans and to identify potential physiological mechanisms that could underlie these associations.

      Methods

      For this narrative review, we evaluated the evidence of relationships between maternal psychological distress and lactation and breastfeeding outcomes (ie, exclusivity and duration) and the possible physiological mechanisms that facilitate these relationships. We reviewed PubMed using the following search terms: stress, anxiety, depression, breastfeeding, and lactation. An additional search by hand was conducted to ensure a thorough review of the literature. Peer-reviewed publications from the United States, Canada, Europe, and Australia were considered for inclusion and selected for their relevance to the review's objectives.

      Results

      Maternal Psychological Distress and Lactation and Infant Feeding Outcomes

      Multiple studies have examined lactation and infant feeding outcomes in relation to maternal psychological distress with varied results, likely because of differences in stress measurement (type and timing of measures), feeding outcomes, and adjustment for confounding factors. In addition, attributing feeding outcomes specifically to maternal psychological distress may be difficult because of the numerous interrelated factors that are potentially associated with lactogenesis (eg, delivery mode, duration of labor, and maternal distress).
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      ,
      • Dewey KG
      • Nommsen-Rivers LA
      • Heinig MJ
      • Cohen RJ.
      Lactogenesis and infant weight change in the first weeks of life.
      We identified 7 systematic reviews and 1 meta-analysis examining maternal distress and breastfeeding outcomes.
      • MS B
      • SL Y
      • EL T
      Perinatal depressive symptoms and breastfeeding behaviors: A systematic literature review and biosocial research agenda.
      • de Jager E
      • Skouteris H
      • Broadbent J
      • Amir L
      • Mellor K.
      Psychosocial correlates of exclusive breastfeeding: a systematic review.
      • Dias CC
      • Figueiredo B.
      Breastfeeding and depression: a systematic review of the literature.
      • Fallon V
      • Bennett KM
      • Harrold JA.
      Prenatal anxiety and infant feeding outcomes: A systematic review.
      • Fallon V
      • Groves R
      • Halford JCG
      • Bennett KM
      • Harrold JA.
      Postpartum anxiety and infant-feeding outcomes.

      Grigoriadis S, Graves L, Peer M, Mamisashvili L, Tomlinson G, Vigod SN, Dennis C-L, Steiner M, Brown C, Cheung A, et al. A systematic review and meta-analysis of the effects of antenatal anxiety on postpartum outcomes. Arch Women's Ment Health. 2018;22:543–556. doi:10.1007/S00737-018-0930-2

      • Hoff CE
      • Movva N
      • Vollmar AKR
      • Pérez-Escamilla R
      Impact of maternal anxiety on breastfeeding outcomes: A systematic review.
      • Mangrio E
      • Persson K
      • Bramhagen A-C.
      Sociodemographic, physical, mental and social factors in the cessation of breastfeeding before 6 months: a systematic review.
      The associations between maternal anxiety, depression, or perceived stress and breastfeeding outcomes were inconclusive, with several meta-analyses citing low-quality studies (inadequate adjustment for confounding, lack of uniform definition of breastfeeding, lack of prospective measurements, inadequate statistical power, or insufficient analysis to determine relationship between variables) and heterogenous outcomes. The link between maternal depression and breastfeeding outcomes, however, appears to be stronger, with 1 meta-analysis reporting associations between elevated maternal depressive symptoms and nonexclusive breastfeeding or shorter breastfeeding duration for more than half of the 38 studies examined. In our further review of the literature, 15 studies found positive associations between maternal distress (perceived stress, anxiety, and/or depression) and nonoptimal breastfeeding outcomes, whereas 6 studies found no association, and 5 studies found that maternal distress was associated with increased breastfeeding or provided potential evidence for a bidirectional relationship (because most studies assessed multiple types of maternal distress [ie, prenatal and postnatal anxiety and depression]; some overlap exists between the provided numbers).
      There are 2 primary time points when maternal stress may reduce breastfeeding: before breastfeeding begins (eg, by delaying initial milk production [ie, lactogenesis]) or after breastfeeding is initiated. The next sections describe each of these time points.

      Delayed Onset of Lactogenesis

      Delayed onset of lactogenesis is defined as insufficient milk production in the first 2 weeks post partum.
      • Neville MC
      • Keller R
      • Seacat J
      • Lutes V
      • Neifert M
      • Casey C
      • Allen J
      • Archer P.
      Studies in human lactation: Milk volumes in lactating women during the onset of lactation and full lactation.
      This delay may occur for a multitude of reasons, such as poor infant suckling ability and subsequent incomplete emptying of milk from the breast,
      • Daly SEJ
      • Kent JC
      • Owens RA
      • Hartmann PE.
      Frequency and degree of milk removal and the short-term control of human milk synthesis.
      but several studies have noted associations with long duration of labor and urgent caesarean delivery, which are strongly linked with postpartum stress for both mother and infant at birth.
      • Dewey KG
      • Nommsen-Rivers LA
      • Heinig MJ
      • Cohen RJ.
      Lactogenesis and infant weight change in the first weeks of life.
      ,
      • Chapman DJ
      • Pérez-Escamilla R.
      Identification of risk factors for delayed onset of lactation.
      ,
      • Doulougeri K
      • Panagopoulou E
      • Montgomery A.
      The impact of maternal stress on initiation andestablishment of breastfeeding.
      Higher postdelivery stress is also associated with delayed onset of lactation, which may lead to nonexclusive breastfeeding.
      • Doulougeri K
      • Panagopoulou E
      • Montgomery A.
      The impact of maternal stress on initiation andestablishment of breastfeeding.
      • Chapman DJ
      • Pérez-Escamilla R.
      Does delayed perception of the onset of lactation shorten breastfeeding duration?.
      • Dimitraki M
      • Tsikouras P
      • Manav B
      • Gioka T
      • Koutlaki N
      • Zervoudis S
      • Galazios G.
      Evaluation of the effect of natural and emotional stress of labor on lactation and breast-feeding.
      Women who experience delayed onset of lactation may introduce formula to their infants shortly after birth, and supplementation of human milk with infant formula during hospitalization is predictive of breastfeeding cessation in early lactation.
      • DiGirolamo AM
      • Grummer-Strawn LM
      • Fein S.
      Maternity care practices: Implications for breastfeeding.
      ,
      • Bolton TA
      • Chow T
      • Benton PA
      • Olson BH.
      Characteristics associated with longer breastfeeding duration: An analysis of a peer counseling support program.
      However, it is possible that providing a small amount of formula in the hospital setting could decrease acute maternal psychological distress and/or improve the perception of adequate milk supply, benefiting long-term exclusivity of maternal breastmilk feeding. A randomized controlled trial conducted by Flaherman et al
      • Flaherman VJ
      • Aby J
      • Burgos AE
      • Lee KA
      • Cabana MD
      • Newman TB
      Effect of early limited formula on duration and exclusivity of breastfeeding in at-risk infants: an RCT.
      assigned participants to receive small formula volumes (10 mL after each breastfeeding) or exclusive breastfeeding before the onset of mature milk production. They hypothesized that early provision of formula would reduce the discontinuation of exclusive breastfeeding by alleviating maternal concerns about milk supply and found that 79% of the formula group were breastfeeding exclusively at 6 months post partum compared with 42% of the exclusive breastfeeding group (P = 0.02).

      Insufficient Milk Supply and Decreased Duration and Exclusivity of Breastfeeding

      Many women discontinue exclusive breastfeeding when infants are between 3 and 6 months of age, and evidence suggests that maternal psychological distress may also affect breastfeeding even after milk production has been fully established (ie, after 1 month post partum).

      Centers for Disease Control and Prevention. Breastfeeding Report Card; 2020. Accessed October 21, 2020. https://www.cdc.gov/breastfeeding/data/reportcard.htm

      ,

      Kent JC. How Breastfeeding Works. J Midwifery Women's Heal. 2007;52:564–570. doi:10.1016/j.jmwh.2007.04.007

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      • Downs DS
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      • Weisman CS.
      Postpartum anxiety and maternal-infant health outcomes.
      • Mehta UJ
      • Siega-Riz AM
      • Herring AH
      • Adair LS
      • Bentley ME.
      Pregravid body mass index, psychological factors during pregnancy and breastfeeding duration: Is there a link?.
      Maternal anxiety and depressive symptoms during pregnancy are predictive of depressive symptoms in the postpartum period, which are associated with shorter duration of exclusive (and/or any) breastfeeding.
      • Ystrom E.
      Breastfeeding cessation and symptoms of anxiety and depression: A longitudinal cohort study.
      ,
      • Ahlqvist-Björkroth S
      • Vaarno J
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      • Pajulo M
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      • Lagström H.
      Initiation and exclusivity of breastfeeding: Association with mothers’ and fathers’ prenatal and postnatal depression and marital distress.
      • Skouteris H
      • Wertheim EH
      • Rallis S
      • Milgrom J
      • Paxton SJ.
      Depression and anxiety through pregnancy and the early postpartum: An examination of prospective relationships.
      • Figueiredo B
      • Dias CC
      • Brandão S
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      Breastfeeding and postpartum depression: state of the art review.
      • Woolhouse H
      • James J
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      • Brown SJ.
      Maternal depressive symptoms at three months postpartum and breastfeeding rates at six months postpartum: Implications for primary care in a prospective cohort study of primiparous women in Australia.
      In a sample of 255 Canadian women, Adedinsewo et al
      • Adedinsewo DA
      • Fleming AS
      • Steiner M
      • Meaney MJ
      • Girard AW
      • MAVAN team
      Maternal anxiety and breastfeeding: findings from the MAVAN (Maternal Adversity, Vulnerability and Neurodevelopment) Study.
      found that every point increase in the State Trait Anxiety Inventory score at 3 months post partum (when lactation had already been established) was associated with decreased odds of any breastfeeding at 12 months post partum. Exposure to stressful life events may negatively affect breastfeeding exclusivity. Data from the Pregnancy Risk Assessment and Monitoring System reveal that among women ≤24 years of age, the odds of exclusive breastfeeding for 3 months were lower for those who experienced ≥2 stressful life events compared with those who experienced no stressful life events.
      • Dugat VM
      • Chertok IRA
      • Haile ZT.
      Association between stressful life events and exclusive breastfeeding among mothers in the United States.
      Another study documented evidence of bidirectional associations between maternal depressive symptoms and breastfeeding duration in a group of 205 women who were followed up prenatally and at 3, 6, 12, and 24 months after birth.
      • Hahn-Holbrook J
      • Haselton MG
      • Schetter CD
      • Glynn LM.
      Does breastfeeding offer protection against maternal depressive symptomatology? A prospective study from pregnancy to 2 years after birth.
      Women with elevated depressive symptoms during pregnancy weaned their infants approximately 2 months earlier than women who did not experience prenatal depression, and in turn, women who breastfed more frequently at 3 months post partum had greater decreases in depressive symptoms up to 2 years after birth. Similarly, mothers who were exclusively breastfeeding at 3 months post partum had significantly lower perceived stress scores compared with those providing mixed feedings (breast milk and formula).
      • Gila-Díaz A
      • Carrillo GH
      • de Pablo ÁLL
      • Arribas SM
      • Ramiro-Cortijo D
      Association between maternal postpartum depression, stress, optimism, and breastfeeding pattern in the first six months.
      Exclusive breastfeeding through 4 to 6 months post partum is also associated with lower maternal perceived stress compared with formula feeding.
      • Groër MW
      Differences between exclusive breastfeeders, formula-feeders, and controls: a study of stress, mood, and endocrine variables.
      Other studies have failed to find associations between anxiety or depressive symptoms in the later postpartum period,
      • Hatton DC
      • Harrison-Hohner J
      • Coste S
      • Dorato V
      • Curet LB
      • McCarron DA.
      Symptoms of postpartum depression and breastfeeding.
      • Ahn S
      • Corwin EJ.
      The association between breastfeeding, the stress response, inflammation, and postpartum depression during the postpartum period: Prospective cohort study.
      • Galbally M
      • Watson SJ
      • Ball H
      • Lewis AJ.
      Breastfeeding, antidepressants, and depression in the Mercy pregnancy and emotional well-being study.
      and others found differing associations with breastfeeding outcomes for prenatal versus postnatal maternal distress.
      • Riedstra JP
      • Aubuchon-Endsley NL.
      A moderated mediation model of maternal perinatal stress, anxiety, infant perceptions and breastfeeding.
      ,
      • Ahlqvist-Björkroth S
      • Vaarno J
      • Junttila N
      • Pajulo M
      • Räihä H
      • Niinikoski H
      • Lagström H.
      Initiation and exclusivity of breastfeeding: Association with mothers’ and fathers’ prenatal and postnatal depression and marital distress.
      Inadequate milk supply (perceived or actual) is a commonly cited reason for discontinuation of exclusive breastfeeding both early in lactation and after lactation has been established; approximately 35% of women report early perceived insufficient milk supply as the primary reason for cessation of breastfeeding.
      • Gatti L.
      Maternal perceptions of insufficient milk supply in breastfeeding.
      By 8 days post partum, the lactating woman produces a mean of 650 mL of breastmilk per 24 hours; from 1 to 6 months of lactation, a woman who is exclusively breastfeeding produces a mean of 750 to 800 mL per 24 hours.
      • Kent JC
      • Mitoulas LR
      • Cregan MD
      • Ramsay DT
      • Doherty DA
      • Hartmann PE.
      Volume and frequency of breastfeedings and fat content of breast milk throughout the day.
      In a sample of 1323 women, the perception that infants were not satisfied by breastmilk alone was among the top 3 reasons provided by mothers for breastfeeding cessation regardless of weaning age (assessed from 2–12 months post partum).
      • Li R
      • Fein SB
      • Chen J
      • Grummer-Strawn LM.
      Why mothers stop breastfeeding: Mothers’ self-reported reasons for stopping during the first year.
      In this study, inadequate milk supply was reported more often by Hispanic mothers and those with a household income of <350% of the federal poverty level compared with white mothers and those with income >350% of the federal poverty level, suggesting that multiple factors (including nonphysiological factors) may influence breastfeeding duration.

      Potential Mechanisms by Which Psychological Distress Affects Lactation

      Physiological mechanisms by which maternal psychological distress may impair lactation are not fully elucidated, and much of the existing support for the association between these variables arises from animal studies or from observational studies in humans. We discuss the potential impact of distress on hormones implicated in lactation and on HPA axis–related mechanisms (Fig. 1).

      Regulation of Hormones Implicated in Lactation

      Lactation is dependent on the intricate coordination of hormones, such as progesterone, prolactin, and oxytocin. One hypothesized physiologic mechanism for the relationship between maternal distress and lactation is the impaired release of maternal oxytocin, which impedes the contraction of myoepithelial cells involved in milk ejection.
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      In a sample of 22 women at 5 days post partum, Ueda et al
      • Ueda T
      • Yokoyama Y
      • Irahara M
      • Aono T.
      Influence of psychological stress on suckling-induced pulsatile oxytocin release.
      found that maternal exposure to stress impaired oxytocin release in response to infant suckling. Participants were exposed to stressors via noise or mental calculation (arithmetic problems), and the number of pulsatile releases of oxytocin in maternal blood was measured. Women in the stressor groups had decreased and delayed responses to suckling and decreased number of oxytocin pulsatile releases. Prolactin levels before and during infant suckling were also measured in relationship to milk secretion volume, and no differences were observed among the groups. The authors concluded that, unlike oxytocin, the increase in prolactin level in response to infant suckling was not impaired by maternal psychological distress. These results are confirmed by studies that have found that higher anxiety and depression scores are associated with lower maternal oxytocin levels during breastfeeding
      • Stuebe AM
      • Grewen K
      • Meltzer-Brody S.
      Association between maternal mood and oxytocin response to breastfeeding.
      and that significant interactions between early breastfeeding cessation and depression status on maternal oxytocin levels are present at 8 weeks post partum.
      • Lara-Cinisomo S
      • McKenney K
      • Di Florio A
      • Meltzer-Brody S
      Associations between postpartum depression, breastfeeding, and oxytocin levels in Latina mothers.
      Similarly, Doulougeri et al
      • Doulougeri K
      • Panagopoulou E
      • Montgomery A.
      The impact of maternal stress on initiation andestablishment of breastfeeding.
      found that positive maternal emotions were associated with increased infant feeding frequency and greater milk volume. Because positive emotions are correlated with increased maternal oxytocin,
      • Mezzacappa ES
      • Katkin ES.
      Breast-feeding is associated with reduced perceived stress and negative mood in mothers.
      these authors suggested that oxytocin was responsible for the favorable feeding and lactation outcomes.
      • Doulougeri K
      • Panagopoulou E
      • Montgomery A.
      The impact of maternal stress on initiation andestablishment of breastfeeding.
      Thus, mothers who experience positive emotions and less distress may have better lactation outcomes. However, maternal depression and anxiety are not necessarily predictive of maternal oxytocin levels and may be influenced by other factors. At 2 and 6 months post partum, Whitley et al
      • Whitley J.
      • Wouk K.
      • Bauer A.E.
      • Grewen K.
      • Gottfredson N.C.
      • Meltzer-Brody S.
      • Propper C.
      • Mills-Koonce R.
      • Pearson B.
      • Stuebe A
      Oxytocin during breastfeeding and maternal mood symptoms.
      found no significant differences in oxytocin levels across a feed between women with symptoms of depression or anxiety versus asymptomatic women.
      Maternal distress may affect lactation by interfering with insulin sensitivity and secretion. Insulin and its regulation of glucose are important for optimal lactation. Insulin resistance and impaired glucose tolerance, such as that observed in type 2 diabetes mellitus or gestational diabetes, have been associated with delayed onset of lactation, low maternal milk supply, and decreased breastfeeding duration.
      • Riddle SW
      • Nommsen-Rivers LA.
      A case control study of diabetes during pregnancy and low milk supply.
      • Nommsen-Rivers LA
      • Dolan LM
      • Huang B.
      Timing of stage II lactogenesis is predicted by antenatal metabolic health in a cohort of primiparas.
      • Oza-Frank R
      • Chertok I
      • Bartley A.
      Differences in breast-feeding initiation and continuation by maternal diabetes status.
      As reviewed by Nommsen-Rivers,
      • Nommsen-Rivers LA.
      Does insulin explain the relation between maternal obesity and poor lactation outcomes? An overview of the literature.
      insulin promotes the expression of genes involved in milk protein synthesis. Nommsen-Rivers
      • Nommsen-Rivers LA.
      Does insulin explain the relation between maternal obesity and poor lactation outcomes? An overview of the literature.
      hypothesized that the combined effects of insulin resistance and impaired insulin secretion on insulin-sensitive signaling in the lactocyte (rather than circulating levels of insulin or glucose) are responsible for the decreased rate of milk synthesis. This hypothesis is supported by work from Neville et al,
      • Neville MC
      • Webb P
      • Ramanathan P
      • Mannino MP
      • Pecorini C
      • Monks J
      • Anderson SM
      • MacLean P.
      The insulin receptor plays an important role in secretory differentiation in the mammary gland.
      who found that genes involved in mammary differentiation and milk synthesis were significantly down-regulated in an insulin receptor knockout mouse model. Although rarely examined in studies that assess impaired glucose tolerance and lactation, psychological distress is associated with decreased insulin sensitivity. In animal models, early-life stress impairs insulin secretion in response to psychological stress in adulthood.
      • Zardooz H
      • Sadeghimahalli F
      • Khodagholi F.
      Early postnatal stress impairs insulin secretion in response to psychological stress in adult rats.
      Animal (mouse) models also reveal that acute psychological stress can alter glucose metabolism by decreasing hepatic sensitivity to insulin, leading to insulin resistance.
      • Li L
      • Li X
      • Zhou W
      • Messina JL.
      Acute psychological stress results in the rapid development of insulin resistance.
      In humans, maternal perception of discrimination, an established psychological stressor, is associated with increased odds of developing gestational diabetes mellitus.
      • MacGregor C
      • Freedman A
      • Keenan-Devlin L
      • Grobman W
      • Wadhwa P
      • Simhan HN
      • Buss C
      • Borders A.
      Maternal perceived discrimination and association with gestational diabetes.
      Furthermore, patients diagnosed with major depression exhibit insulin resistance after administration of oral glucose tolerance tests compared with healthy patients.
      • Winokur A
      • Maislin G
      • Phillips JL
      • Amsterdam JD.
      Insulin Resistance After Oral Glucose Tolerance Testing in Patients With Major Depression.
      These studies outline a potential physiological mechanism by which stress-induced glucose dysregulation and insulin resistance may lead to lactation difficulty.

      Cortisol and HPA Axis–Related Mechanisms

      The HPA axis is activated in response to stress and involves a cascade of hormonal events that lead to release of the glucocorticoid steroid hormone cortisol into the bloodstream. The effects of stress-induced alterations in circulating cortisol are numerous because glucocorticoid receptors are widely distributed throughout the body. Pregnancy and the postpartum period involve normative changes in HPA axis function, which plays a role in lactation.
      • Brunton PJ
      • Russell JA
      • Douglas AJ.
      Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation.
      Cortisol is a necessary cofactor for milk production and is involved in the differentiation of mammary gland cells into lactocytes, as well as milk secretion and lactogenesis.
      • Pang WW
      • Hartmann PE.
      Initiation of Human Lactation: Secretory Differentiation and Secretory Activation.
      At the same time, lactation results in a reduction in maternal cortisol levels during feeding and an attenuation of maternal HPA axis reactivity to stress,
      • M H
      • G M
      • I N
      • S W
      • C K
      • U E
      • DH H
      Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women.
      • Cox EQ
      • Stuebe A
      • Pearson B
      • Grewen K
      • Rubinow D
      • Meltzer-Brody S.
      Oxytocin and HPA stress axis reactivity in postpartum women.
      • Stuebe AM
      • Grewen K
      • Pedersen CA
      • Propper C
      • Meltzer-Brody S.
      Failed lactation and perinatal depression: common problems with shared neuroendocrine mechanisms?.
      • Tu MT
      • Lupien SJ
      • Walker CD.
      Multiparity reveals the blunting effect of breastfeeding on physiological reactivity to psychological stress.
      • Amico JA
      • Johnston JM
      • Vagnucci AH.
      Suckling-induced attenuation of plasma cortisol concentrations in postpartum lactating women.
      further highlighting the protective effects of lactation as well as the likelihood that psychological distress and lactation associations are bidirectional. Both maternal psychosocial distress and difficulties with lactation are associated with altered HPA axis functioning, suggesting that maternal HPA axis dysregulation is a pathway by which maternal distress compromises lactation.
      • Stuebe AM
      • Grewen K
      • Pedersen CA
      • Propper C
      • Meltzer-Brody S.
      Failed lactation and perinatal depression: common problems with shared neuroendocrine mechanisms?.
      However, the extant literature regarding maternal psychological distress and HPA axis activity associations is equivocal,
      • Seth S
      • Lewis AJ
      • Galbally M.
      Perinatal maternal depression and cortisol function in pregnancy and the postpartum period: a systematic literature review.
      potentially because of measurement differences across studies, failure to consider the interacting effects of multiple hormones (eg, cortisol and oxytocin
      • Cox EQ
      • Stuebe A
      • Pearson B
      • Grewen K
      • Rubinow D
      • Meltzer-Brody S.
      Oxytocin and HPA stress axis reactivity in postpartum women.
      ), and/or involvement of other mechanisms.

      Future Directions

      The lack of uniform study results is likely reflective of varying sample sizes, measures of psychological distress, and breastfeeding outcomes, as well as limited evidence from animal studies and observational studies in humans because of ethicality of assigning participants into nonbreastfeeding groups. Future exploration of maternal distress and lactation and feeding outcomes should use adequate adjustment for potential confounding factors (ie, parity
      • Paul IM
      • Downs DS
      • Schaefer EW
      • Beiler JS
      • Weisman CS.
      Postpartum anxiety and maternal-infant health outcomes.
      ) and explore additional variables that may mediate or moderate relationships, such as those discussed below.
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      Milk composition may be altered by maternal psychological distress and have an impact on lactation and breastfeeding success. The macronutrient content, specifically fatty acid concentration, of human milk is negatively associated with stress reactivity (measured via saliva cortisol in response to cold).
      • Ziomkiewicz A
      • Babiszewska M
      • Apanasewicz A
      • Piosek M
      • Wychowaniec P
      • Cierniak A
      • Barbarska O
      • Szołtysik M
      • Danel D
      • Wichary S.
      Psychosocial stress and cortisol stress reactivity predict breast milk composition.
      Fatty acids comprise most calories in human milk, and decreased concentrations of fatty acids in milk may lead to decreased infant satiation, affecting maternal perception of adequate milk supply.
      • Ziomkiewicz A
      • Babiszewska M
      • Apanasewicz A
      • Piosek M
      • Wychowaniec P
      • Cierniak A
      • Barbarska O
      • Szołtysik M
      • Danel D
      • Wichary S.
      Psychosocial stress and cortisol stress reactivity predict breast milk composition.
      Maternal psychological distress may also affect the immune components present in milk.
      • Thibeau S
      • D'Apolito K
      • Minnick AF
      • Dietrich MS
      • Kane B
      • Cooley S
      • Groer M
      Relationships of maternal stress with milk immune components in African American mothers of healthy term infants.
      Recent evidence supports the finding that milk bioactives may serve as biomarkers for lactation difficulty. We found that bioactives present at 1 month post partum in human milk were associated with breastfeeding cessation by 3 months post partum. Specifically, milk glucose and smaller decreases in glucose from 1 to 3 months post partum were associated with increased odds of exclusive breastfeeding, whereas leptin and increases in insulin and leptin were associated with decreased odds of exclusive breastfeeding

      Nagel EM, Kummer L, Jacobs DR Jr, Foster L, Duncan K, Johnson K, Harnack L, Haapala J, Kharoud H, Gallagher T, Kharbanda EO, Pierce S, Fields DA, Demerath EW. Human Milk Glucose, Leptin, and Insulin Predict Cessation of Full Breastfeeding and Initiation of Formula Use. Breastfeed Med. 2021 Aug 3. doi:10.1089/bfm.2021.0131. Epub ahead of print. PMID: 34348043.

      . Whether changes in these bioactives are associated with maternal psychological distress is unknown and requires further study.
      Lactation and breastfeeding outcomes for non-Hispanic black mothers are less optimal than those of white mothers.

      Centers for Disease Control and Prevention. Breastfeeding: Facts . Accessed June 3, 2021. https://www.cdc.gov/breastfeeding/data/facts.html#stopearly

      Racism has been linked with maternal psychological distress
      • Bécares L
      • Nazroo J
      • Kelly Y.
      A longitudinal examination of maternal, family, and area-level experiences of racism on children's socioemotional development: Patterns and possible explanations.
      ,
      • Murry VM
      • Brown PA
      • Brody GH
      • Cutrona CE
      • Simons RL.
      Racial discrimination as a moderator of the links among stress, maternal psychological functioning, and family relationships.
      but has not been thoroughly studied in conjunction with breastfeeding outcomes. However, work-related racism has been associated with lower odds of longer breastfeeding duration, whereas police-related racism has been associated with higher odds of longer breastfeeding duration.
      • Griswold MK
      • Crawford SL
      • Perry DJ
      • Person SD
      • Rosenberg L
      • Cozier YC
      • Palmer JR.
      Experiences of racism and breastfeeding initiation and duration among first-time mothers of the Black Women's Health Study.
      The intersection between racism and maternal psychological distress should be examined in conjunction with lactation and breastfeeding outcomes to understand policies and interventions that may improve these outcomes.
      Future research should include an exploration of the bidirectional benefits of breastfeeding on maternal psychological distress and overall maternal health.
      • Dewey KG.
      Maternal and fetal stress are associated with impaired lactogenesis in humans.
      ,
      • Henshaw EJ
      • Fried R
      • Siskind E
      • Newhouse L
      • Cooper M.
      Breastfeeding self-efficacy, mood, and breastfeeding outcomes among primiparous women.
      Although maternal psychological distress may decrease breastfeeding duration, breastfeeding itself may decrease maternal distress.
      • Gila-Díaz A
      • Carrillo GH
      • de Pablo ÁLL
      • Arribas SM
      • Ramiro-Cortijo D
      Association between maternal postpartum depression, stress, optimism, and breastfeeding pattern in the first six months.
      ,
      • Groër MW
      Differences between exclusive breastfeeders, formula-feeders, and controls: a study of stress, mood, and endocrine variables.
      ,
      • Mezzacappa ES
      • Katkin ES.
      Breast-feeding is associated with reduced perceived stress and negative mood in mothers.
      In addition, breastfeeding may be used as a coping mechanism for some mothers; higher prenatal maternal marital distress has been associated with longer duration of exclusive breastfeeding.
      • Ahlqvist-Björkroth S
      • Vaarno J
      • Junttila N
      • Pajulo M
      • Räihä H
      • Niinikoski H
      • Lagström H.
      Initiation and exclusivity of breastfeeding: Association with mothers’ and fathers’ prenatal and postnatal depression and marital distress.
      This finding may be because skin-to-skin contact, such as that practiced during breastfeeding, is associated with decreased maternal anxiety.
      • Bigelow AE
      • Power M.
      Mother–infant skin-to-skin contact: Short- and long-term effects for mothers and their children born full-term.
      ,
      • De Alencar AEMA
      • Arraes LC
      • De Albuquerque EC
      • Alves JGB.
      Effect of kangaroo mother care on postpartum depression.
      The intention to breastfeed versus actual practice may also influence the relationship between maternal psychological distress and breastfeeding.
      • Odom EC
      • Li R
      • Scanlon KS
      • Perrine CG
      Grummer-Strawn L. Reasons for earlier than desired cessation of breastfeeding.
      f

      Conclusion

      Current evidence suggests a potential role for acute and chronic maternal psychological distress in lactation success and difficulties, including both establishment of lactation and continued duration of breastfeeding. Both physiological and social or behavioral factors may be involved, but additional studies are needed to understand the mechanisms behind these relationships. Comprehensive strategies to decrease maternal psychological distress, as well as policies that focus on dismantling structural barriers to breastfeeding, may improve breastfeeding outcomes (Figure 1).
      Figure 1
      Figure 1Maternal psychological distress may impair lactation by (1) interfering with oxytocin release, (2) reducing insulin sensitivity and secretion, or (3) causing dysregulation of the hypothalamic-pituitary-adrenocortical (HPA) axis. Figure created with BioRender.com.

      Disclosure

      Emily M. Nagel is supported by an grant T32DK083250 from the National Institute of Diabetes and Digestive and Kidney Diseases. Mariann A. Howland is supported by a National Science Foundation Graduate Research Fellowship (00074041). Cynthia Pando is supported by grant T32HD095134 from the Eunice Kennedy Shriver National Institute of Child Health and Human Development. David A. Fields and Ellen W. Demerath are supported by grant R01HD080444 Eunice Kennedy Shriver National Institute of Child Health and Human Development. The authors have indicated that they have no other conflicts of interest regarding the content of this article.

      Acknowledgments

      Ellen W. Demerath conceptualized the manuscript; Emily M. Nagel, Mariann A. Howland, and Ellen W. Demerath drafted the original manuscript; Cynthia Pando and Emily M. Nagel constructed the figure; Mariann A. Howland, Cynthia Pando, Jamie Stang, Susan M. Mason, David A. Fields, and Ellen W. Demerath critically reviewed the manuscript; Ellen W. Demerath had primary responsibility for final content. All authors read and approved the final manuscript.

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