Got bacteria? The astounding, yet not-so-surprising, microbiome of human milk

Current Opinion in Biotechnology

Volumn 44, Issue , 2017, Pages 63-68

  McGuire, Michelle K ^a   McGuire, Mark A ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEALTH; MICROORGANISMS;

DELIVERY MODES; GASTROINTESTINAL TRACT; MAMMARY GLAND; MATERNAL HEALTHS; MICROBIAL COMMUNITY STRUCTURES; MICROBIOME; PSEUDOMONAS GENUS; SHORT TERM;

BACTERIA;

ANTIBIOTIC AGENT; BACTERIAL DNA;

BACTERIAL VIABILITY; BRADYRHIZOBIACEAE; BREAST MILK; CORYNEBACTERIUM; DNA SEQUENCE; DRUG USE; ENERGY BALANCE; FOOD INTAKE; LACTATION; LACTOCOCCUS; LEUCONOSTOC; MATERNAL WELFARE; MICROBIOME; NEXT GENERATION SEQUENCING; NONHUMAN; PATHOGEN LOAD; PRIORITY JOURNAL; PROPIONIBACTERIUM; PSEUDOMONAS; PYROSEQUENCING; RALSTONIA; REVIEW; SERRATIA; SPECIES DOMINANCE; SPHINGOMONAS; STAPHYLOCOCCUS; STREPTOCOCCUS; BACTERIUM; CLASSIFICATION; HUMAN; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MICROFLORA; PUERPERIUM;

BACTERIA; HUMANS; MATERNAL HEALTH; MICROBIAL VIABILITY; MICROBIOTA; MILK, HUMAN; POSTPARTUM PERIOD;

EID: 85002787803     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2016.11.013     Document Type: Review

References (40)

1. 1 Turnbaugh, P.J., Ley, R.E., Hamady, M., Fraser-Liggett, C.M., Knight, R., Gordon, J.I., The human microbiome project. Nature 449 (2007), 804–810.
2. 2 Sender, R., Fuchs, S., Milo, R., Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164 (2016), 337–340.
3. 3 Relman, D.A., Falkow, S., The meaning and impact of the human genome sequence for microbiology. Trends Microbiol 9 (2001), 206–208.
4. 4 McGuire, M.K., McGuire, M.A., Human milk: mother nature's prototypical probiotic food?. Adv Nutr 6 (2015), 112–123.
5. 5 Carroll, L., Osman, M., Davies, D.P., McNeish, A.S., Bacteriology of raw breast milk. Lancet, 2, 1979, 1186.
6. 6 Eidelman, A.I., Szilagyi, G., Patterns of bacterial colonization of human milk. Obstet Gynecol 53 (1979), 550–552.
7. 7 el-Mohandes, A.E., Schatz, V., Keiser, J.F., Jackson, B.J., Bacterial contaminants of collected and frozen human milk used in an intensive care nursery. Am J Infect Control 21 (1993), 226–230.
8. 8 Wyatt, R.G., Mata, L.J., Bacteria in colostrum and milk of Guatemalan Indian women. J Trop Pediatr 15 (1969), 159–162.
9. 9 Thomsen, A.C., Hansen, K.B., Møller, B.R., Leukocyte counts and microbiologic cultivation in the diagnosis of puerperal mastitis. Am J Obstet Gynecol 146 (1983), 938–941.
10. 10 Martín, R., Langa, S., Reviriego, C., Jimínez, E., Marín, M.L., Xaus, J., Fernández, L., Rodríguez, J.M., Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 143 (2003), 754–758.
11. 11 Heikkilä, M.P., Saris, P.E., Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 95 (2003), 471–478.
12. 12 Hunt, K.M., Preuss, J., Nissan, C., Davlin, C.A., Williams, J.E., Shafii, B., Richardson, A.D., McGuire, M.K., Bode, L., McGuire, M.A., Human milk oligosaccharides promote the growth of staphylococci. Appl Environ Microbiol 78 (2012), 4763–4770.
13. 13 Hunt, K.M., Foster, J.A., Forney, L.J., Schutte, U.M.E., Beck, D.L., Abdo, Z., Fox, L.K., Williams, J.E., McGuire, M.K., McGuire, M.A., Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE, 6, 2011, e21313.
14. 14 Cabrera-Rubio, R., Collado, M.C., Laitinen, K., Salminen, S., Isolauri, E., Mira, A., The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96 (2012), 544–551.
15. 15• Urbaniak, C., Cummins, J., Brackstone, M., Macklaim, J.M., Gloor, G.B., Baban, C.K., Scott, L., O'Hanlon, D.M., Burton, J.P., Francis, K.P., Tangney, M., Reid, G., Microbiota of human breast tissue. Appl Environ Microbiol 80 (2014), 3007–3014 In this epidemiologic study, the research team compared microbial communities in mammary tissue collected from women with and without cancer in Canada and Ireland. All samples were found to contain complex bacterial communities, even though some of the women had never breastfed and none of the subjects had signs nor symptoms of infection. There were differences in mammary microbiomes based on geographic site and cancer history. Culture-dependent analyses confirmed viability of some bacteria.
16. 16•• Urbaniak, C., Angelini, M., Gloor, G.B., Reid, G., Human milk microbiota profiles in relation to birthing method, gestation and infant gender. Microbiome, 4, 2016, 1 In this study, milk was collected from 39 Canadian women and analyzed using 16S rRNA technology. There was no evidence of differences based on delivery mode, gender of infant, and gestation length. Dominant genera in the milk samples were Staphylococcus, Pseudomonas, Streptococcus, and Lactobacillus. The authors postulate that ‘there may be a fail-safe mechanism whereby the mother is ‘ready’ to pass along her bacterial imprint irrespective of when and how the baby is born.’.
17. 17 Davé, V., Street, K., Francis, S., Bradman, A., Riley, L., Eskenazi, B., Holland, N., Bacterial microbiome of breast milk and child saliva from low-income Mexican-American women and children. Pediatr Res 79 (2016), 846–854.
18. 18 Boix-Amorós, A., Collado, M.C., Mira, A., Relationship between milk microbiota, bacterial load, macronutrients, and human cells during lactation. Front Microbiol, 7, 2016, 492.
19. 19•• Khodayar-Pardo, P., Mira-Pascual, L., Collado, M.C., Martínez-Costa, C., Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J Perinatol 34 (2014), 599–605 In this longitudinal, observational study, milk was collected repeatedly from 32 healthy women and analyzed using quantitative PCR. Lactobacillus, Streptococcus, and Enterococcus were the predominant bacterial genera. Bifidobacteria were more abundant in milk samples collected from women delivering term infants, compared to those produced by women delivering prematurely. Higher bacterial counts were found in colostrum and transitional milk produced by women undergoing Cesarean section deliveries.
20. 20 Soto, A., Martín, V., Jiménez, E., Mader, I., Rodríguez, J.M., Fernández, L., Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr 59 (2014), 78–88.
21. 21 Cabrera-Rubio, R., Mira-Pascual, L., Mira, A., Collado, M.C., Impact of mode of delivery on the milk microbiota composition of healthy women. J Dev Orig Health Dis 7 (2016), 54–60.
22. 22 Arroyo, R., Martín, V., Maldonado, A., Jiménez, E., Fernández, L., Rodríguez, J., Treatment of infectious mastitis during lactation: antibiotics versus oral administration of Lactobacilli isolated from breast milk. Clin Infect Dis 50 (2010), 1551–1558.
23. 23 Carrothers, J.M., York, M.A., Brooker, S.L., Lackey, K.A., Williams, J.E., Shafii, B., Price, W.J., Settles, M.L., McGuire, M.A., McGuire, M.K., Fecal microbial community structure is stable over time and related to variation in macronutrient and micronutrient intakes in lactating women. J Nutr 145 (2015), 379–388.
24. 24 Urbaniak, C., McMillan, A., Angelini, M., Gloor, G.B., Sumarah, M., Burton, J.P., Reid, G., Effect of chemotherapy on the microbiota and metabolome of human milk, a case report. Microbiome, 2, 2014, 24.
25. 25 González, R., Maldonado, A., Martín, V., Mandomando, I., Fumadó, V., Metzner, K.J., Sacoor, C., Fernández, L., Macete, E., Alonso, P.L., Rodríguez, J.M., Menendez, C., Breast milk and gut microbiota in African mothers and infants from an area of high HIV prevalence. PLoS ONE, 8, 2013, e80299.
26. 26 Martín, R., Jiménez, E., Olivares, M., Marín, M.L., Fernández, L., Xaus, J., Rodríguez, J.M., Lactobacillus salivarius CECT 5713, a potential probiotic strain isolated from infant feces and breast milk of a mother–child pair. Int J Food Microbiol 112 (2006), 35–43.
27. 27 Fernández, L., Langa, S., Martín, V., Maldonado, A., Jiménez, E., Martín, R., Rodríguez, J.M., The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 69 (2013), 1–10.
28. 28• Rodríguez, J.M., The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation?. Adv Nutr 5 (2014), 779–784 This comprehensive review outlines what is currently known (and posited) about the origin of bacteria found in the mammary gland and milk. These origins include the infant's mouth and migration to the mammary glands via an endogenous cellular route.
29. 29 Xuan, C., Shamonki, J.M., Chung, A., Dinome, M.L., Chung, M., Sieling, P.A., Lee, D.J., Microbial dysbiosis is associated with human breast cancer. PLoS ONE, 9, 2014, e83744.
30. 30 Chan, A.A., Bashir, M., Rivas, M.N., Duvall, K., Sieling, P.A., Pieber, T.R., Vaishampayan, P.A., Love, S.M., Lee, D.J., Characterization of the microbiome of nipple aspirate fluid of breast cancer survivors. Sci Rep, 6, 2016, 28061.
31. 31 Latuga, M.S., Stuebe, A., Seed, P.C., A review of the source and function of microbiota in breast milk. Semin Reprod Med 32 (2014), 68–73.
32. 32 Ramsay, D.T., Kent, J.C., Owens, R.A., Hartmann, P.E., Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics 113 (2004), 361–367.
33. 33 Nasidze, I., Li, J., Quinque, D., Tang, K., Stoneking, M., Global diversity in the human salivary microbiome. Genome Res 19 (2009), 636–643.
34. 34 Gao, Z., Perez-Perez, G.I., Chen, Y., Blaser, M.J., Quantitation of major human cutaneous bacterial and fungal populations. J Clin Microbiol 48 (2010), 3575–3581.
35. 35 Perez, P.F., Doré, J., Leclerc, M., Levenez, F., Benyacoub, J., Serrant, P., Segura-Roggero, I., Schiffrin, E.J., Donnet-Hughes, A., Bacterial imprinting of the neonatal immune system: lessons from maternal cells?. Pediatrics 119 (2007), e724–e732.
36. 36 Heida, F.H., van Zoonen, A.G., Hulscher, J.B., Te Kiefte, B.J., Wessels, R., Kooi, E.M., Bos, A.F., Harmsen, H.J., de Goffau, M.C., A necrotizing enterocolitis-associated gut microbiota is present in the meconium: results of a prospective study. Clin Infect Dis 62 (2016), 863–870.
37. 37 Zhuang, X., Xiong, L., Li, L., Li, M., Chen, M.H., Alterations of gut microbiota in patients with irritable bowel syndrome: a systematic review and meta-analysis. J Gastroenterol Hepatol, 2016, June, 10.1111/jgh.13471.
38. 38 D'Argenio, V., Casaburi, G., Precone, V., Pagliuca, C., Colicchio, R., Sarnataro, D., Discepolo, V., Kim, S.M., Russo, I., Del Vecchio Blanco, G., Horner, D.S., Chiara, M., Pesole, G., Salvatore, P., Monteleone, G., Ciacci, C., Caporaso, G.J., Jabrì, B., Salvatore, F., Sacchetti, L., Metagenomics reveals dysbiosis and a potentially pathogenic N. flavescens strain in duodenum of adult celiac patients. Am J Gastroenterol 111 (2016), 879–890.
39. 39 Smith, M.I., Yatsunenko, T., Manary, M.J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A.L., Rich, S.S., Concannon, P., Mychaleckyj, J.C., Liu, J., Houpt, E., Li, J.V., Holmes, E., Nicholson, J., Knights, D., Ursell, L.K., Knight, R., Gordon, J.I., Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339 (2013), 548–554.
40. 40• McGuire, M.K., Meehan, C.L., Brooker, S., Williams, J.E., Foster, J.A., McGuire, M.A., An evolutionary, biosocial perspective on variation in human milk microbes and oligosaccharides: an example of eco-homeorhesis?. McGuire, M.K., McGuire, M.A., Bode, L., (eds.) Prebiotics and Probiotics in Human Milk, 2016, Elsevier This monograph, based on scientific fundamentals and anthropologic paradigm, uses a biosocial lens to relate how evolution and behavior may have, together, shaped variation in global human milk microbiomes and oligosaccharide profiles to optimize health in a particular location and culture. The term ‘eco-homeorhesis’ is introduced and defined as a shift in what would be considered a ‘normal’ homeostatic range or profile to support health in a particular ecological/behavioral niche.