SARS-CoV-2 and Mother-Baby Separation

SARS-CoV-2 and Mother-Baby Separation

Categories: Keeping Up to Date, Leader Today: Public

DENA DURAN, LLL LEADER, NEW YORK CITY AND IDAHO, USA

Risks of Separation (Part 1)

Skip to:Case Review of Infants Born to COVID-19 Positive Mothers (Part 2)

The World Health Organisation (WHO), UNICEF, the United Nations (UN), La Leche League International (LLLI), and the Academy of Breastfeeding Medicine (ABM) all recommend continuing to breastfeed during COVID-19 illness if possible, while following hygiene precautions (WHO, 2019; UNICEF, n.d.; UNFPA, 2020; LLLI, 2020; ABM, 2020).

Despite this, certain hospitals across the world are sometimes creating protocols that call for mother-baby separation at birth when the mother is presumed or positive for SARS-CoV-2 infection or a “person under investigation” (PUI) for SARS-CoV-2 infection. There are stories like these from ChinaFranceItalySpain, and the United States (USA). Country policies vary greatly with Great Britain’s Royal College of Obstetricians and Gynecologists opposing separation, China setting a policy for separation, and the Centers for Disease Control and Prevention (CDC) in the USA recommending separation on a case-by case basis (RCOG, 2020; Wang et al. 2020; CDC, 2020).

So far, I have seen no clear, compelling data that contraindicates keeping mother and baby together but much that supports it.

SARS-CoV-2, which causes the illness known as COVID-19, is a lipid-enveloped virus: it has a “shell” of fat around a strand of RNA (a type of genetic material). Prior research by Pfaender et al (2013) has shown HCV (Hepatitis C), H1N1 (Swine flu) and some other lipid-enveloped RNA-stranded viruses are destroyed in vitro by human milk via slicing of the lipid envelope by free fatty acids generated from triglycerides (a type of fat) by lipases (fat digesting enzymes) in the milk (Pfaender et al., 2013).

The research concludes that “nursing by HCV-positive mothers is unlikely to play a major role in vertical transmission [transmission from mother to baby]” (Pfaender et al., 2013). To my knowledge it has not been scientifically proven that a mother with a lipid-enveloped virus, like SARS-CoV-2, will transmit the active, infective virus to the nursling via her milk. Instead, research suggests that breast milk inactivates the virus, reduces infectivity, and is effective in helping the infant fight the virus (Pfaender et al., 2013). Indeed the first 26 samples of mothers’ milk tested for SARS-CoV-2 were negative (Chen et al., 2020; Egloff et al., 2020). One report has found the virus in human milk (Groß et al., 2020) but its presence in milk does not mean that the virus is infectious to the infant and must be considered alongside the critical immune factors and antibodies also present in human milk.  Recent research shows that many women positive for COVID-19 illness passed along antibodies to the virus in their milk (Fox et al, 2020).

The CDC specifically states in their advice that “Although it is well recognized that the ideal setting for care of a healthy term newborn while in the hospital is within the mother’s room, temporary separation of the newborn from a mother with confirmed or suspected COVID-19 should be strongly considered to reduce the risk of transmission to the neonate …  recommendations will be updated as new information informing the risk-benefit of maternal-infant separation is available (CDC, 2020a).”

Though we don’t have a full picture of SARS-CoV-2, we do know a lot about the necessity of mother-infant closeness. My hope is that the information in this article will help Leaders and the parents they help to have scientifically-backed information all in one place; to help parents and their health care providers make an informed decision that takes into account the known risks of separation.

The risks and benefits of separation should be weighed very carefully and take into account the severity of the mother’s illness, the ability to take precautions (wearing a mask, careful hand washing) and still care for and breastfeed her baby, and the effect separation has on the physiological systems of both mother and baby. The risks of separation are very great.

Risks of separation of mother and baby immediately postpartum

  1. Dysregulation of the physiological systems of mother and baby
  • A mother’s body helps to regulate a baby’s temperature, breathing, heart rate, energy use, acid-base balance, and overall homeostasis (maintenance of body systems) (Winberg, 2005). Removing the baby from the mother introduces the risk of dysregulation of these vital processes.
  1. Introduction of loneliness and an allostatic load (the cumulative negative effects of chronic stress on the body)
  • Several studies have shown that loneliness (i.e., separation) can induce grave consequences in humans. These range from a dull sense of something wrong in light cases to overall negative systemic effects in extreme cases. Removing a newborn from his/her mother is an extreme case (Lupien et al., 2009) (Footnote A) and should be very carefully considered. The following excerpt tells us that the following systems are affected by stress: “the sympathetic-adrenal-medullary (SAM) system, the hypothalamic-pituitary-adrenal (HPA) axis, as well as cardiovascular, metabolic, neural, endocrine and immune systems …and continued stress can cause dysregulation of many of these systems.” (Okamura et al., 2009)
  • The key worry here is the stress hormone cortisol. Sapolsky (1996), in his classic paper in Science, demonstrated that cortisol specifically damaged a part of the brain called the hippocampus, a structure critical in learning and memory. As a number of recent studies on sleep training have found, separation increases cortisol (Buss et al., 2012; Middlemiss et al., 2011; Navarez, 2013).
  • The separation stresses the mother as well, as is discussed in Stuebe’s recent statement published in Breastfeeding Medicine on the same subject (Stuebe, 2020).  Stuebe notes that the “associated physiologic stress could worsen the mother’s disease course.” (Stuebe, 2020)
  1. Altered brain development

Brain development can be negatively affected by stress; changing behavioural and physiological responses (McEwen, 2006; Harvard University, 2014). Some of the possible effects of an altered HPA axis or SAM system include:

  • Stress-related disorders that can affect mental health (e.g., depression, anxiety disorders, alcoholism, drug abuse) and physical health (e.g., cardiovascular disease, diabetes, stroke) (Harvard University, 2014).
  • Chronic stress can lead to suppression of immune function, contribute to metabolic syndrome, bone mineral loss, and muscle atrophy (Harvard University, 2014).
  • Long-term increases in cortisol levels can alter the function of a number of neural systems, and even change the structure of parts of the brain essential for learning and memory (Harvard University, 2014). See also Sapolsky (1996).
  1. Reduction in cellular immunity
  • Effectivity of natural killer (NK) cells (a type of lymphocyte that is crucial to the immune system) is reduced in persons under stress (Kiecolt-Glaser et al., 1984). NK cells are important in fighting viral infection (Brandtstadter & Yang, 2019).) Though we don’t know much about the specific mechanisms of SARS-CoV-2 or how our body fights it (i.e., how involved NK cells are), it seems a large risk to knowingly reduce a known member of the fighting team. This is a risk for both the mother and the baby, as separation puts both of them in stress mode.
  • Reduced effectiveness of T-lymphocytes (specialized white blood cells) has also been shown in persons under stress (Kiecolt-Glaser et al., 1984). Again, to reduce the effectiveness of the immune system of mother and baby through the stress of separation carries a risk.
  1. Increased Inflammation

Another system that is activated during prolonged stress is the inflammatory response system (Kendall-Tackett, 2013). Not only does increased inflammation have serious implications for long-term health (Kendall-Tackett, 2010), but it is specifically a problem in the case of COVID-19 in children. According to the Centers for Disease Control and Prevention, COVID-19 activates a multi-system inflammatory response (CDC, 2020). When COVID-19 seriously affects, or even kills children, it is because of inflammation.

  • Research on early life adversity is instructive here. Separation, inconsistent care, and abuse are all childhood stressors that have a lifetime impact on the inflammatory response (e.g., Gouin et al., 2020; Oshir et al., 2020). Slopen et al. (2015) found that prenatal and early childhood exposure to adversity increased systemic inflammation in the adult offspring by three times.
  • Because of these previous findings, it can be reasonably argued that separation activates the inflammatory response system in both mother and baby, which arguably makes babies more vulnerable to the serious harms caused by COVID-19. Rather than protecting them, separation puts them directly in harm’s way.
  1. Increased difficulty bonding for mother and baby
  • Skin-to-skin contact increases oxytocin which, among other physiological effects, enhances bonding for mother and baby (Handlin, et al., 2009). To deny the pair this important positive hormonal boost at this crucial time can affect bonding and social relationships long past the current pandemic (Crenshaw, 2014). The stress system specifically suppresses oxytocin (Handlin et al., 2009) Conversely, both breastfeeding and skin to skin increases oxytocin which suppresses the stress system, making babies less vulnerable to possible infection (Handlin et al., 2009; Heinrich et al., 2001).
  • Babies cry less and interact with their mothers more when they are put skin-to-skin early (WHO, 2019). To remove this means the baby may cry more, mother and baby may interact less and they may bond to each other less, resulting in negative maternal behavior (Crenshaw, 2014). (Footnote B)
  1. Increased risk of breastfeeding “failing” or being more difficult.
    The risk of undermining the breastfeeding relationship through early separation should not be discounted.
  • Separation of mother and baby has been shown to reduce milk production and the likelihood of exclusive breastfeeding (WHO, 2019; Bystrova et al., 2007; Elander & Lindberg, 1984). In one study, an average of 3.3 days separation (range 1-6 days) in the first week of life resulted in 37% exclusively breastfed infants at three months of age versus 72% in the non-separated group (Elander & Lindberg, 1984).
  • The benefits of the normal nutrition of human milk are huge. Human milk contains many immune factors and unique nutritional components that can help a baby fight off infection—factors that are given to baby with every single breastfeed. (Footnote C) Because the risk of infection from SARS-CoV-2 is so high (both immediately postpartum from hospital sources, perhaps from mother, and after discharge in the home/everyday life environment), the risks of removing these immune factors should be very carefully considered.
  • If breastfeeding fails as a result of the separation, a formula-fed child has increased risk of several diseases, including upper and lower respiratory ailments, colds, viruses and bacterial infections, intestinal disorders, type 2 diabetes, ear infections, obesity, and some childhood cancers, increased likelihood of a smaller thymus, and an increased risk of sudden infant death syndrome (SIDS) (LLLI, n.d.; Jackson & Nazar, 2019; Alm, 2002; Thompson et al., 2017).
  • The mother who does not breastfeed has an increased risk of breast and ovarian cancer, earlier menopause age, decreased bone strength and size, non-fatty liver disease, and coronary artery disease (Wiklund et al., 2011; Enger et al., 1997; Langton et al., 2020; Ajmera et al., 2019; Rajaei et al., 2002).

Treatment of each COVID-19 positive mother and her baby should be considered on a case-by-case basis. Separation is not suggested by the WHO, the UN, UNICEF, the ABM or LLLI. All of these risks should be carefully considered and shared with the mother to help her make an informed decision whenever separation is being proposed. 

Footnotes

‌(A) The stress hyporesponsive period (SHRP)—a period during which the body is much less reactive to stessors—has been modeled in rats and may also be present in humans.  One thing that overarches this lowered response to stress is separation of the pup from the dam—the pup is extremely stressed by separation from its mother and the ill effects of separation are even greater from earlier separations than later (Lupien et al., 2009). Furthermore, primate studies also show that mother-baby separations affect the HPA axis months or years later (Lupien et al., 2009).  The primate studies also show “heightened fear behavior, exaggerated startle responses, hippocampal changes …, and atypical development of prefrontal regions involved in emotion and behavior control” (Lupien et al., 2009). Lupien et al further notes that human studies suggest that the HPA axis is buffered by parents and social contact in the first year of life.  With all of this in mind, separating the newborn from the mother might be one of the most stressful things in a hospital protocol that can be done to the child.

‌(B) Crenshaw explains,

“Disrupting or delaying skin-to-skin care may suppress a newborn’s innate protective behaviors, lead to behavioral disorganization, and make self-attachment and breastfeeding more difficult. Lack of skin-to-skin care and early separation also may disturb maternal–infant bonding, reduce the mother’s affective response to her baby, and have a negative effect on maternal behavior.” (Crenshaw, 2014 )

(C) These immune factors include leukocytes (granulocytes, monocytes/macrophages, and lymphocytes [T-cells, NK cells, and antibody-producing B cells]), stem cells of hematopoietic and mammary gland origin (shown to differentiate), sigA, casein, serum albumin, growth factors (EGF, BDNF, GDNF, CNTF, IGF-I, IGF-II, VEGF), Epo, lysozyme, lactoferrin, nucleotides, alpha lactalbumin, tryptophan, calcitonin, miRNA, pre-and probiotics including oligosaccharides, lipase, amino acids, lactose, fatty acids, vitamins, cytokines, chemokines, cytokine inhibitors, metabolic hormones, mucins, and others (Ballard & Ardythe, 2013; Field, 2005; Jantscher-Krenn & Bode, 2012; Ray et al., 2019; Butler, 1979).

Case Review of Infants Born to COVID-19 Positive Mothers (Part 2)

What do the case reports of mother-infant pairs with SARS-CoV-2 involvement tell us?

  • Dong et al. (2020) published a single case report of possible vertical transmission from mother to infant. Yet what they found to denote infection was antibodies in the baby’s blood: elevated IgG and IgM antibodies. All 5 reverse transcription-polymerase chain reaction (RT-PCR) nasal swabs for SARS-CoV-2 came back negative (from 2 hours to 16 days). Baby was born via cesarean section and was not allowed contact with the mother so I believe the likelihood of antepartum transmission via close contact with the mother is low.
  • Zeng et al. looked at six babies born to mothers with COVID-19 who were born via cesarean (mothers wore masks). They found elevated IgM antibodies in two infants, elevated IgG in five, RT-PCR was negative in all, and none of the infants had any symptoms (H. Zeng et al., 2020).
  • Chen et al. looked at nine dyads whose mothers tested positive for COVID-19 (via RT-PCR) and had cesarean sections. Of the six babies with data, amniotic fluid, cord blood, neonatal throat swab, and human milk samples were tested for SARS-CoV-2, and results were negative for the virus pointing to NO vertical transmission of the virus (Chen et al., 2020).
  • The latest report by L. Zeng et al., is of 33 infants born to COVID-19 positive mothers (L. Zeng et al., 2020). Three infants became ill or were born ill and tested positive. The sickest patient (who also recovered) was 31 weeks gestation so at least part of the issues and severity were likely due to gestational age. All three were born via cesarean. Vertical transmission cannot be ruled out (L. Zeng et al., 2020). No patients were tested on day one. Data on IgG, amniotic fluid, etc. is not reported.
    • Patient One: on day two lethargy and fever. Swabs positive on days two and four, negative on day six (L. Zeng et al., 2020).
    • Patient Two, presented ill, also had meconium staining: swabs positive days two and four, negative on day six (L. Zeng et al., 2020).
    • Patient Three: born at 31 weeks, resuscitation required, suspected sepsis, positive on days two and four, negative on day seven.
  • Egloff et al found that because babies were not tested at birth (earliest positive is 16 hours) vertical transmission cannot be proved or ruled out (Egloff et al., 2020).

Whether infection is in utero or postpartum, a baby will receive his mother’s antibodies, and perhaps start to produce his/her own in some cases (possibly indicated by the presence of IgM in a few of the babies). Being close to mother with all the many benefits that affords as well as the antiviral powerhouse of breast milk seems much better for reducing viral load and infectivity and increasing overall health (or maintaining a baseline of health) than separation. Also, since loneliness is proven to negatively affect health (by Kiecolt-Glaser et al., 1984), reducing the effective action of cellular immunity via separation (for mother and baby) seems a strong negative (immunocompromising) choice to make in the face of a pandemic.

Let’s not separate babies and mothers unless the great risks outlined in Part 1 are truly outweighed by the benefit of separating them. What is the perceived benefit?  What is the actual benefit? As Leaders, we need to share comprehensive information with parents and give mothers the opportunity to make a fully informed decision.

NOTES ON VERTICAL TRANSMISSION, IGM, AND IGG LEVELS:

IgM is normally not passed from the placenta to the baby so the presence of positive IgM (but negative RT-PCR) in newborns is a paradox. Positive IgG is not surprising since the mothers were COVID-19 positive and these immunoglobulins are passed from the placenta to the baby.  Since SARS-CoV-2 incubation is thought to be 2–14 days, and no swabs were done on day one of life for those who tested positive, while vertical transmission cannot be ruled out, it also cannot be proved since it is possible infants were exposed and developed COVID-19 in the hospital after birth (CDC 2020b).

In response to H. Zeng et al.’s six babies report (H. Zeng et al., 2020), Professor Richard Tedder, Visiting Professor in Medical Virology, Imperial College London, said, “To confirm the existence of intrauterine infection, undetectable by PCR, continued follow-up of the children should show that the IgG levels persist. If this is done and the infants antibody levels wane with time after delivery then infection would be deemed not to have occurred (Science Media Centre, 2020).” 

The same reasoning may stand in the single reported case study by Dong et al.  The single case report was dismissed on day 16 with IgG levels that had dropped by half from birth (from 140.32 to 69.94 (ref <10). (Unfortunately, we don’t have IgG levels at dismissal for the H. Zeng cases.) Thus, it sounds as if vertical transmission may not have occurred, although this is a case report sometimes being used as evidence of vertical transmission. Dong et al. are careful to state that because the amniotic fluid and placenta wasn’t tested by PCR it is a preliminary observation.  Chen et al. states clearly in their last paragraph “We found no evidence for vertical transmission in late pregnancy (2020).”

Two of the babies in the earlier H. Zeng et al. six dyads report also had IgM antibodies (2020). Reasoning was as varied as perhaps the mother’s placenta was damaged and allowed the larger immune cells through from placenta to baby, or the baby produced his/her own antibodies to the infection (though infection was not proved) (Science Media Centre, 2020). All six babies in the earlier report (H. Zeng et al) and the one in the single report (Dong et al) were separated from their mothers at birth (2020, 2020). All babies who had positive swab tests and those who had IgG antibodies to COVID-19 were born via cesarean section. The three babies in the L. Zeng et al report show signs of either infection from mother in utero or infection after birth from unknown source (positive tests on day 2 of life) (2020).

 

NOTE

The content of this article was last edited 3rd of June, 2020. Please keep in mind that research and recommendations around SARS-CoV-2 are constantly evolving.

Dena Duran has a long interest in the health and science fields and is honored to be a part of La Leche League (since 2013), helping mothers and babies in New York City and in Idaho, USA.  She is an Associate Professional Liaison for LLL New York and is the newest representative to the US Breastfeeding Committee for LLL Alliance for Breastfeeding Education.  Dena is thankful for her loving, supportive husband, Jason and their two wonderful girls, Sophia and Sabrina. Contact Dena at lll.denaduran@gmail.com

 

REFERENCES

ABM. (2020, March 10). ABM STATEMENT CORONAVIRUS. Retrieved from www.bfmed.org website: https://www.bfmed.org/abm-statement-coronavirus

Ajmera, V. H., Terrault, N. A., VanWagner, L. B., Sarkar, M., Lewis, C. E., Carr, J. J., & Gunderson, E. P. (2019). Longer lactation duration is associated with decreased prevalence of non-alcoholic fatty liver disease in women. Journal of Hepatology, 70(1), 126–132. https://doi.org/10.1016/j.jhep.2018.09.013

Alm, B. (2002). Breast feeding and the sudden infant death syndrome in Scandinavia, 1992-95. Archives of Disease in Childhood, 86(6), 400–402. https://doi.org/10.1136/adc.86.6.400

Ballard, O., & Morrow, A. L. (2013). Human Milk Composition. Pediatric Clinics of North America, 60(1), 49–74. https://doi.org/10.1016/j.pcl.2012.10.002

Brandstadter, J. D., & Yang, Y. (2011). Natural Killer Cell Responses to Viral Infection. Journal of Innate Immunity, 3(3), 274–279. https://doi.org/10.1159/000324176

Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affecive problems. Proceedings of the National Academy of Sciences USA, 109(20), E1312-E1319.

Butler, J. E. (1979). Immunologic aspects of breast feeding, antiinfectious activity of breast milk. Seminars in Perinatology, 3(3), 255–270. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/392768.

Bystrova, K., Widström, A.-M., Matthiesen, A.-S., Ransjö-Arvidson, A.-B., Welles-Nyström, B., Vorontsov, I., & Uvnäs-Moberg, K. (2007). Early lactation performance in primiparous and multiparous women in relation to different maternity home practices. A randomised trial in St. Petersburg. International Breastfeeding Journal, 2(1), 9. https://doi.org/10.1186/1746-4358-2-9

CDC. (2020a, February 11). Coronavirus Disease 2019 (COVID-19). Retrieved April 24, 2020, from Centers for Disease Control and Prevention website: http://www.cdc.gov/coronavirus/2019-ncov/hcp/inpatient-obstetric-healthcare-guidance.html

CDC. (2020b, March 14). Coronavirus Disease 2019 (COVID-19) – Symptoms. Retrieved from Centers for Disease Control and Prevention website: https://www.cdc.gov/coronavirus/2019-ncov/symptoms-testing/symptoms.html?CDC_AA_refVal=https%3A%2F%2Fwww.cdc.gov%2Fcoronavirus%2F2019-ncov%2Fabout%2Fsymptoms.html

Centers for Disease Control and Prevention. (,2020). For parents: Multisystem Inflammatory Syndrome in Children (MIS-C) associated with COVID-19.   Retrieved from https://www.cdc.gov/coronavirus/2019-ncov/daily-life-coping/children/mis-c.html

Chen, H., Guo, J., Wang, C., Luo, F., Yu, X., Zhang, W., … Zhang, Y. (2020). Clinical characteristics and intrauterine vertical transmission potential of COVID-19 infection in nine pregnant women: a retrospective review of medical records. The Lancet, 395(10226), 809–815. https://doi.org/10.1016/S0140-6736(20)30360-3

Crenshaw, J. T. (2014). Healthy Birth Practice #6: Keep Mother and Baby Together— It’s Best for Mother, Baby, and Breastfeeding. The Journal of Perinatal Education, 23(4), 211–217. https://doi.org/10.1891/1058-1243.23.4.211

Dong, L., Tian, J., He, S., Zhu, C., Wang, J., Liu, C., & Yang, J. (2020). Possible Vertical Transmission of SARS-CoV-2 From an Infected Mother to Her Newborn. JAMA. https://doi.org/10.1001/jama.2020.4621

Egloff, C., Vauloup-Fellous, C., Picone, O., Mandelbrot, L., & Roques, P. (2020). Evidence and possible mechanisms of rare maternal-fetal transmission of SARS-CoV-2. Journal of Clinical Virology. https://doi.org/10.1016/j.jcv.2020.104447

ELANDER, G., & LINDBERG, T. (1984). Short Mother-Infant Separation during First Week of Life Influences the Duration of Breastfeeding. Acta Paediatrica, 73(2), 237–240. https://doi.org/10.1111/j.1651-2227.1984.tb09935.x

Enger, S., Ross, R., Henderson, B., & Bernstein, L. (1997). Breastfeeding history, pregnancy experience and risk of breast cancer. British Journal of Cancer, 76(1), 118–123. https://doi.org/10.1038/bjc.1997.346

Field, C. J. (2005). The Immunological Components of Human Milk and Their Effect on Immune Development in Infants. The Journal of Nutrition, 135(1), 1–4. https://doi.org/10.1093/jn/135.1.1

Gouin, J.-P., Paquin, C., Wrosch, C., McGrath, J., Arbour, N., & Booij, L. (2020). Marital quality and inflammation: The moderating role of early life adversity. Health Psychology, 39(1), 58-67. doi:https://doi.org/10.1037/hea0000790

Groß, R., Conzelmann, C., Müller, J. A., Stenger, S., Steinhart, K., Kirchhoff, F., & Münch, J. (2020). Detection of SARS-CoV-2 in human breastmilk. The Lancet. https://doi.org/10.1016/s0140-6736(20)31181-8

Handlin, L., Jonas, W., Pettersson, M., Ejdeback, M., Ransjo-Arvidson, A.-B., Nissen, A., & Uvnas-Moberg, K. (2009). Effects of sucking and skin-to-skin contact on maternal ACTH and cortisol levels during the second day postpartum–Influences of epidural analgesia and oxytocin in the perinatal period. Breastfeeding Medicine, 4(4), 207-220.

Harvard University, N. S. C. on the D. C. (2014). Excessive Stress Disrupts the Architecture of the Developing Brain. Retrieved from https://developingchild.harvard.edu/wp-content/uploads/2005/05/Stress_Disrupts_Architecture_Developing_Brain-1.pdf

Heinrichs, M., Meinlschmidt, G., Neumann, I., Wagner, S., Kirschbaum, C., Ehlert, U., & Hellhammer, D. H. (2001). Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. Journal of Clinical Endocrinology & Metabolism, 86, 4798-4804.

Jackson, K. M., & Nazar, A. M. (2019). Breastfeeding, the Immune Response, and Long-term Health. The Journal of the American Osteopathic Association, 106(4), 203–207. Retrieved from https://jaoa.org/article.aspx?articleid=2093315

Jantscher-Krenn, E., & Bode, L. (2012). Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatrica, 64(1), 83–99. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/22350049

Kendall-Tackett, K. A. (2013). Treating the lifetime health effects of childhood victimization, 2nd Edition. Kingston, NJ: Civic Research Institute.

Kiecolt-Glaser, J. K., Ricker, D., George, J., Messick, G., Speicher, C. E., Garner, W., & Glaser, R. (1984). Urinary Cortisol Levels, Cellular Immunocompetency, and Loneliness in Psychiatric Inpatients. Psychosomatic Medicine, 46(1), 15–23. https://doi.org/10.1097/00006842-198401000-00004

Langton, C. R., Whitcomb, B. W., Purdue-Smithe, A. C., Sievert, L. L., Hankinson, S. E., Manson, J. E., … Bertone-Johnson, E. R. (2020). Association of Parity and Breastfeeding With Risk of Early Natural Menopause. JAMA Network Open, 3(1), e1919615–e1919615. https://doi.org/10.1001/jamanetworkopen.2019.19615

LLLI. (2020, February 19). Continuing to Nurse Your Baby Through Coronavirus (2019-nCoV; COVID-19) and Other Respiratory Infections. Retrieved March 30, 2020, from La Leche League International website: http://llli.org/coronavirus/

LLLI. (n.d.). Importance of Breastfeeding. Retrieved March 24, 2020, from La Leche League International website: http://www.llli.org/breastfeeding-info/benefits/.

Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10(6), 434–445. https://doi.org/10.1038/nrn2639

McEwen, B. S. (2006). Protective and damaging effects of stress mediators: central role of the brain. Dialogues in Clinical Neuroscience, 8(4), 367–381. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3181832/

Middlemiss, W., & Kendall-Tackett, K. A. (Eds.). (2014). The science of mother-infant sleep: Current findings on bedsharing, breastfeeding, sleep training, and normal infant sleep. Amarillo, TX: Praeclarus Press.

OKAMURA, H., TSUDA, A., & MATSUISHI, T. (2011). The relationship between perceived loneliness and cortisol awakening responses on work days and weekends1. Japanese Psychological Research, 53(2), 113–120. https://doi.org/10.1111/j.1468-5884.2011.00459.x

Oshri, A., Duprey, E. B., Liu, S., & Ehrlich, K. B. (2020). Harsh parenting and youth systemic inflammation: Modulation by the autonomic nervous system. Health Psychology, 39(6), 482-496. doi:https://doi.org/10.1037/hea0000852

Pfaender, S., Heyden, J., Friesland, M., Ciesek, S., Ejaz, A., Steinmann, J., … Steinmann, E. (2013). Inactivation of Hepatitis C Virus Infectivity by Human Breast Milk. The Journal of Infectious Diseases, 208(12), 1943–1952. https://doi.org/10.1093/infdis/jit519

Rajaei, S., Rigdon, J., Crowe, S., Tremmel, J., Tsai, S., & Assimes, T. L. (2019). Breastfeeding Duration and the Risk of Coronary Artery Disease. Journal of Women’s Health (2002), 28(1), 30–36. https://doi.org/10.1089/jwh.2018.6970

Ray, C., Kerketta, J. A., Rao, S., Patel, S., Dutt, S., Arora, K., … Bhushan, P. (2019). Human Milk Oligosaccharides: The Journey Ahead. International Journal of Pediatrics, 2019, 1–8. https://doi.org/10.1155/2019/2390240

RCOG. (2020). Information for healthcare professionals Coronavirus (COVID-19) Infection in Pregnancy. Retrieved from Royal College of Obstetricians and Gynaecologists website: https://www.rcog.org.uk/globalassets/documents/guidelines/2020-03-28-covid19-pregnancy-guidance.pdf

Sapolsky, R. M. (1996). Why stress is bad for your brain. Science, 273, 749-750.

Slopen, N., Loucks, E. B., Appleton, A. A., Kawachi, I., Kubzansky, L. D., Non, A. L., . . . Gilman, S. E. (2015). Early origins of inflammation: An examination of prenatal and childhood social adversity in a prospective cohort study. Psychoneuroendocrinology, 51, 403-413.

Science Media Centre. (2020). Expert reaction to antibodies found in babies born to COVID-19 mothers | Science Media Centre. Retrieved March 30, 2020, from Science Media Centre: Where science meets the headlines website: http://www.sciencemediacentre.org/expert-reaction-to-antibodies-found-in-babies-born-to-covid-19-mothers/.

Stuebe, A. (2020). Should Infants Be Separated from Mothers with COVID-19? First, Do No Harm. Breastfeeding Medicine, 15(5). https://doi.org/10.1089/bfm.2020.29153.ams

Thompson, J. M. D., Tanabe, K., Moon, R. Y., Mitchell, E. A., McGarvey, C., Tappin, D., … Hauck, F. R. (2017). Duration of Breastfeeding and Risk of SIDS: An Individual Participant Data Meta-analysis. Pediatrics, 140(5), e20171324. https://doi.org/10.1542/peds.2017-1324

UNFPA. (n.d.). UNFPA statement on novel coronavirus (COVID-19) and pregnancy. Retrieved April 1, 2020, from www.unfpa.org website: http://www.unfpa.org/press/unfpa-statement-novel-coronavirus-covid-19-and-pregnancy

UNICEF. (n.d.). Coronavirus disease (COVID-19): What parents should know. Retrieved March 30, 2020, from www.unicef.org website: http://www.unicef.org/stories/novel-coronavirus-outbreak-what-parents-should-know#advice-breastfeeding

Wang, L., Shi, Y., Xiao, T., Fu, J., Feng, X., Mu, D., … Zhou, W. (2020). Chinese expert consensus on the perinatal and neonatal management for the prevention and control of the 2019 novel coronavirus infection (First edition). Annals of Translational Medicine, 8(3). https://doi.org/10.21037/atm.2020.02.20

WHO. (2019). Early initiation of breastfeeding to promote exclusive breastfeeding. World Health Organization. https://doi.org//entity/elena/titles/early_breastfeeding/en/index.html

WHO. (2020, March 18). Q&A on COVID-19, pregnancy, childbirth and breastfeeding. Retrieved March 30, 2020, from Who.int website: http://www.who.int/news-room/q-a-detail/q-a-on-covid-19-pregnancy-childbirth-and-breastfeeding

WHO. (2020b, April 28). FREQUENTLY ASKED QUESTIONS: Breastfeeding and COVID-19 For health care workers. Retrieved May 15, 2020, from www.who.int website: https://www.who.int/docs/default-source/maternal-health/faqs-breastfeeding-and-covid-19.pdf?sfvrsn=d839e6c0_1

Wiklund, P. K., Xu, L., Wang, Q., Mikkola, T., Lyytikäinen, A., Völgyi, E., … Cheng, S. (2011). Lactation is associated with greater maternal bone size and bone strength later in life. Osteoporosis International, 23(7), 1939–1945. https://doi.org/10.1007/s00198-011-1790-z

Winberg, J. (2005). Mother and newborn baby: mutual regulation of physiology and behavior–a selective review. Developmental Psychobiology, 47(3), 217–229. https://doi.org/10.1002/dev.20094

Zeng, H., Xu, C., Fan, J., Tang, Y., Deng, Q., Zhang, W., & Long, X. (2020). Antibodies in Infants Born to Mothers With COVID-19 Pneumonia. JAMA. https://doi.org/10.1001/jama.2020.4861

Zeng, L., Xia, S., Yuan, W., Yan, K., Xiao, F., Shao, J., & Zhou, W. (2020). Neonatal Early-Onset Infection With SARS-CoV-2 in 33 Neonates Born to Mothers With COVID-19 in Wuhan, China. JAMA Pediatrics. https://doi.org/10.1001/jamapediatrics.2020.08781

You can print to paper or to a PDF file.

For best printing results, open the llli.org site in Google Chrome or Microsoft Edge. Although you can view the site well in any browser, printing from other browsers might not operate correctly.

1. Browse to the web document that you want to print.

2. Click the Print button that is displayed on the web page (not the Print command on the browser menu or toolbar).
This opens the browser print window. The window displays a preview of the document that will be printed. The preview might take a minute to display, depending on the document size.

3. In the Printer box, select the desired printer.
For example, if you are working on a Windows computer, and you want to print to a PDF file, select Save as PDF.

4. As required, configure the other options such as the pages to print.

5. Click the Print button.
If you are generating a PDF, click Save. You are prompted for the name and folder location to save the file.