Repertoire of human breast and milk microbiota: a systematic review

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Victora CG, Bahl R, Barros AJ et al. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 387(10017), 475–490 (2016). •• Breastfeeding is a major determinant of human health.
  MedlineGoogle Scholar
• 2 Gartner LM, Morton J, Lawrence RA et al. Breastfeeding and the use of human milk. Pediatrics 115(2), 496–506 (2005).
  MedlineGoogle Scholar
• 3 Klement E, Cohen RV, Boxman J, Joseph A, Reif S. Breastfeeding and risk of inflammatory bowel disease: a systematic review with meta-analysis. Am. J. Clin. Nutr. 80(5), 1342–1352 (2004).
  Medline CASGoogle Scholar
• 4 Williams CD. A nutritional disease of childhood associated with a maize diet. Arch. Dis. Child. 8(48), 423–433 (1933).
  Medline CASGoogle Scholar
• 5 Newburg DS. Innate immunity and human milk. J. Nutr. 135(5), 1308–1312 (2005).
  Medline CASGoogle Scholar
• 6 Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr. Clin. North Am. 60(1), 49–74 (2013).
  MedlineGoogle Scholar
• 7 Lönnerdal B, Erdmann P, Thakkar SK, Sauser J, Destaillats F. Longitudinal evolution of true protein, amino acids and bioactive proteins in breast milk: a developmental perspective. J. Nutr. Biochem. 41, 1–11 (2017).
  Medline CASGoogle Scholar
• 8 Pannaraj PS, Li F, Cerini C et al. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr. 171(7), 647–654 (2017).
  MedlineGoogle Scholar
• 9 Heikkilä MP, Saris PEJ. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J. Appl. Microbiol. 95(3), 471–478 (2003).
  Medline CASGoogle Scholar
• 10 Urbaniak C, Cummins J, Brackstone M et al. Microbiota of human breast tissue. Appl. Environ. Microbiol. 80(10), 3007–3014 (2014).
  MedlineGoogle Scholar
• 11 Martín R, Langa S, Reviriego C et al. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr. 143(6), 754–758 (2003). • Demonstrates the vertical transmission of Lactobacillus at the strain level.
  Medline CASGoogle Scholar
• 12 Berardi A, Rossi C, Creti R et al. Group B streptococcal colonization in 160 mother-baby pairs: a prospective cohort study. J. Pediatr. 163(4), 1099.e1091–1104.e1091 (2013).
  Google Scholar
• 13 Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ. Microbiol. 16(9), 2891–2904 (2014).
  Medline CASGoogle Scholar
• 14 Asnicar F, Manara S, Zolfo M et al. Studying vertical microbiome transmission from mothers to infants by strain-level metagenomic profiling. mSystems 2(1), pii:e00164–16 (2017).
  Google Scholar
• 15 Perez PF, Doré J, Leclerc M et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics 119(3), e724–e732 (2007).
  MedlineGoogle Scholar
• 16 Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science 352(6285), 539–544 (2016).
  Medline CASGoogle Scholar
• 17 Ho NT, Li F, Lee-Sarwar KA et al. Meta-analysis of effects of exclusive breastfeeding on infant gut microbiota across populations. Nat. Commun. 9(1), 4169 (2018).
  MedlineGoogle Scholar
• 18 Xuan C, Shamonki JM, Chung A et al. Microbial dysbiosis is associated with human breast cancer. PLoS ONE 9(1), e83744 (2014).
  MedlineGoogle Scholar
• 19 Urbaniak C, Gloor GB, Brackstone M, Scott L, Tangney M, Reid G. The microbiota of breast tissue and its association with breast cancer. Appl. Environ. Microbiol. 82(16), 5039–5048 (2016).
  Medline CASGoogle Scholar
• 20 Jiménez E, De Andrés J, Manrique M et al. Metagenomic analysis of milk of healthy and mastitis-suffering women. J. Hum. Lact. 31(3), 406–415 (2015).
  MedlineGoogle Scholar
• 21 Lagier JC, Armougom F, Million M et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin. Microbiol. Infect. 18(12), 1185–1193 (2012).
  Medline CASGoogle Scholar
• 22 Lagier JC, Dubourg G, Million M et al. Culturing the human microbiota and culturomics. Nat. Rev. Microbiol. doi:10.1038/s41579-018-0041-0 540-550 (2018) (Epub ahead of print). •• Microbial culturomics offers an unprecedented opportunity to study and manipulate the human microbiome.
  MedlineGoogle Scholar
• 23 Lagier J-C, Khelaifia S, Alou MT et al. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat. Microbiol. 1, 16203 (2016).
  Medline CASGoogle Scholar
• 24 Seck E-H, Senghor B, Merhej V et al. Salt in stools is associated with obesity, gut halophilic microbiota and Akkermansia muciniphila depletion in humans. Int. J. Obes. doi:10.1038/s41366-018-0201-3 (2018) (Epub ahead of print).
  Google Scholar
• 25 Dickson I. Gut microbiota: Culturomics: illuminating microbial dark matter. Nat. Rev. Gastroenterol. Hepatol. 14(1), 3 (2017).
  Medline CASGoogle Scholar
• 26 Hugon P, Dufour J-C, Colson P, Fournier P-E, Sallah K, Raoult D. A comprehensive repertoire of prokaryotic species identified in human beings. Lancet Infect. Dis. 15(10), 1211–1219 (2015).
  MedlineGoogle Scholar
• 27 Bilen M, Dufour J-C, Lagier J-C et al. The contribution of culturomics to the repertoire of isolated human bacterial and archaeal species. Microbiome 6(1), 94 (2018).
  MedlineGoogle Scholar
• 28 Fonkou M-D, Dufour J-C, Dubourg G, Raoult D. Repertoire of bacterial species cultured from the human oral cavity and respiratory tract. Future Microbiol. 13, 1611–1624 (2018).
  CASGoogle Scholar
• 29 Morand A, Cornu F, Dufour J-C, Tsimaratos M, Lagier JC, Raoult D. Human bacterial repertoire of urinary tract: a paradigm shift. J. Clin. Microbiol. doi:10.1128/JCM.00675-18 (2018) (Epub ahead of print).
  Google Scholar
• 30 Diop K, Dufour J-C, Levasseur A, Fenollar F. Exhaustive repertoire of human vaginal microbiota. Hum. Microbiome J. doi:10.1016/j.humic.2018.11.002 (2018) (Epub ahead of print).
  Google Scholar
• 31 Million M, Angelakis E, Maraninchi M et al. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. (Lond.) 37(11), 1460–1466 (2013).
  CASGoogle Scholar
• 32 Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb. Pathog. 53(2), 100–108 (2012).
  MedlineGoogle Scholar
• 33 Million M, Maraninchi M, Henry M et al. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes. (Lond.) 36(6), 817–825 (2012).
  CASGoogle Scholar
• 34 Million M, Raoult D. Species and strain specificity of Lactobacillus probiotics effect on weight regulation. Microb. Pathog. 55, 52–54 (2013).
  MedlineGoogle Scholar
• 35 Euzéby JP. List of bacterial names with standing in nomenclature: a folder available on the internet. Int. J. Syst. Evol. Microbiol. 47(2), 590–592 (1997).
  CASGoogle Scholar
• 36 Parte AC. LPSN – List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int. J. Syst. Evol. Microbiol. 68(6), 1825–1829 (2018).
  MedlineGoogle Scholar
• 37 Million M, Tidjani Alou M, Khelaifia S et al. Increased gut redox and depletion of anaerobic and methanogenic prokaryotes in severe acute malnutrition. Sci. Rep. 6, 26051 (2016).
  Medline CASGoogle Scholar
• 38 Million M, Raoult D. Linking gut redox to human microbiome. Hum. Microbiome J. 10, 27–32 (2018).
  Google Scholar
• 39 Campbell C, Dikiy S, Bhattarai SK et al. Extrathymically generated regulatory T cells establish a niche for intestinal border-dwelling bacteria and affect physiologic metabolite balance. Immunity 48(6), 1245.e1249–1257.e1249 (2018).
  Google Scholar
• 40 Loy A, Pfann C, Steinberger M et al. Lifestyle and horizontal gene transfer-mediated evolution of mucispirillum schaedleri, a core member of the murine gut microbiota. mSystems 2(1), pii:e00171-16 (2017).
  MedlineGoogle Scholar
• 41 Everard A, Belzer C, Geurts L et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl Acad. Sci. USA 110(22), 9066–9071 (2013).
  Medline CASGoogle Scholar
• 42 Million M, Diallo A, Raoult D. Gut microbiota and malnutrition. Microb. Pathog. 106, 127–138 (2017).
  MedlineGoogle Scholar
• 43 Togo AH, Diop A, Bittar F et al. Description of Mediterraneibacter massiliensis, gen. nov., sp. nov., a new genus isolated from the gut microbiota of an obese patient and reclassification of Ruminococcus faecis, Ruminococcus lactaris, Ruminococcus torques, Ruminococcus gnavus and Clostridium glycyrrhizinilyticum as Mediterraneibacter faecis comb. nov., Mediterraneibacter lactaris comb. nov., Mediterraneibacter torques comb. nov., Mediterraneibacter gnavus comb. nov. and Mediterraneibacter glycyrrhizinilyticus comb. nov. Antonie Van Leeuwenhoek doi:10.1007/s10482-018-1104-y (2018) (Epub ahead of print).
  Google Scholar
• 44 Patel SH, Vaidya YH, Patel RJ, Pandit RJ, Joshi CG, Kunjadiya AP. Culture independent assessment of human milk microbial community in lactational mastitis. Sci. Rep. 7(1), 7804 (2017).
  MedlineGoogle Scholar
• 45 Biagi E, Quercia S, Aceti A et al. The bacterial ecosystem of mother's milk and infant's mouth and gut. Front. Microbiol. 8, 1214 (2017).
  MedlineGoogle Scholar
• 46 Li S-W, Watanabe K, Hsu C-C et al. Bacterial composition and diversity in breast milk samples from mothers living in Taiwan and mainland China. Front. Microbiol. 8, 965 (2017).
  MedlineGoogle Scholar
• 47 Milani C, Mancabelli L, Lugli GA et al. Exploring vertical transmission of bifidobacteria from mother to child. Appl. Environ. Microbiol. 81(20), 7078–7087 (2015).
  Medline CASGoogle Scholar
• 48 Samuel B-S, Gordon J-I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc. Natl Acad. Sci. USA 103(26), 10011–6 (2006).
  Medline CASGoogle Scholar
• 49 Samuel BS, Hansen EE, Manchester JK et al. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc. Natl Acad. Sci. USA 104(25), 10643–8 (2007).
  Medline CASGoogle Scholar
• 50 Ward TL, Hosid S, Ioshikhes I, Altosaar I. Human milk metagenome: a functional capacity analysis. BMC Microbiol. 13, 116 (2013).
  MedlineGoogle Scholar
• 51 Koren O, Goodrich Julia K, Cullender Tyler C et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150(3), 470–480 (2012).
  Medline CASGoogle Scholar
• 52 Arroyo R, Martín V, Maldonado A, Jiménez E, Fernández L, Rodríguez Juan M. Treatment of infectious mastitis during lactation: antibiotics versus oral administration of Lactobacilli isolated from breast milk. Clin. Inf. Dis. 50(12), 1551–1558 (2010). •• Treatment of infectious mastitis by oral administration of Lactobacilli.
  Medline CASGoogle Scholar
• 53 Schafer P, Furrer C, Mermillod B. An association of cigarette smoking with recurrent subareolar breast abscess. Int. J. Epidemiol. 17(4), 810–813 (1988).
  Medline CASGoogle Scholar
• 54 Co M, Cheng VCC, Wei J et al. Idiopathic granulomatous mastitis: a 10-year study from a multicentre clinical database. Pathology doi:10.1016/j.pathol.2018.08.010 (2018) (Epub ahead of print).
  MedlineGoogle Scholar
• 55 Bundred NJ, Dover MS, Coley S, Morrison JM. Breast abscesses and cigarette smoking. Br. J. Sur. 79(1), 58–59 (1992).
  Medline CASGoogle Scholar
• 56 Bharat A, Gao F, Aft RL, Gillanders WE, Eberlein TJ, Margenthaler JA. Predictors of primary breast abscesses and recurrence. World J. Surg. 33(12), 2582–2586 (2009).
  MedlineGoogle Scholar
• 57 Gollapalli V, Liao J, Dudakovic A, Sugg SL, Scott-Conner CE, Weigel RJ. Risk factors for development and recurrence of primary breast abscesses. J. Am. Coll. Surg. 211(1), 41–48 (2010).
  MedlineGoogle Scholar
• 58 Martin V, Manes-Lazaro R, Rodriguez JM, Maldonado-Barragan A. Streptococcus lactarius sp. nov., isolated from breast milk of healthy women. Int. J. Syst. Evol. Microbiol. 61(5), 1048–1052 (2011).
  Medline CASGoogle Scholar
• 59 Yatsunenko T, Rey FE, Manary MJ et al. Human gut microbiome viewed across age and geography. Nature 486(7402), 222–227 (2012). • Bifidobacterium breve, Bifidobacterium longum and Bifidobacterium dentium are the three species particularly associated with breastfeeding and with a higher relative abundance in babies versus adults (see supplementary data of this article).
  Medline CASGoogle Scholar
• 60 Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS ONE 7(8), e44595 (2012).
  Medline CASGoogle Scholar
• 61 Solís G, De Los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 16(3), 307–310 (2010).
  Medline CASGoogle Scholar
• 62 Million M, Tomas J, Wagner C, Lelouard H, Raoult D, Gorvel J-P. New insights in gut microbiota and mucosal immunity of the small intestine. Human Microbiome J. 7–8, 10 (2018).
  Google Scholar
• 63 Thornton JW, Argenta LC, Mcclatchey KD, Marks MW. Studies on the endogenous flora of the human breast. Ann. Plast. Surg. 20(1), 39–42 (1988).
  Medline CASGoogle Scholar
• 64 Ransjo U, Asplund OA, Gylbert L, Jurell G. Bacteria in the female breast. Scand. J. Plast. Reconstr. Surg. 19(1), 87–89 (1985).
  Medline CASGoogle Scholar
• 65 Lelouard H, Fallet M, De Bovis B, Meresse S, Gorvel JP. Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology 142(3), 592.e3–601.e3 (2012).
  Google Scholar
• 66 Hashiguchi M, Kashiwakura Y, Kojima H, Kobayashi A, Kanno Y, Kobata T. Peyer's patch innate lymphoid cells regulate commensal bacteria expansion. Immunol. Lett. 165(1), 1–9 (2015).
  Medline CASGoogle Scholar
• 67 Nielsen ML, Raahave D, Stage JG, Justesen T. Anaerobic and aerobic skin bacteria before and after skin-disinfection with chlorhexidine: an experimental study in volunteers. J. Clin. Pathol. 28(10), 793–797 (1975).
  Medline CASGoogle Scholar
• 68 Delgado S, Arroyo R, Martín R, Rodríguez JM. PCR-DGGE assessment of the bacterial diversity of breast milk in women with lactational infectious mastitis. BMC infect. Dis. 8, 51 (2008).
  MedlineGoogle Scholar
• 69 Donaire A, Guillen J, Rajegowda B. Neonatal breast hypertrophy: Revisited. Pediatr. Thera. 6(3), 2 (2016).
  Google Scholar
• 70 Raveenthiran V. Neonatal mastauxe (breast enlargement of the newborn). J. Neonatal Surg. 2(3), 31 (2013).
  Medline CASGoogle Scholar
• 71 Kunisawa J, Kiyono H. Alcaligenes is commensal bacteria habituating in the gut-associated lymphoid tissue for the regulation of intestinal IgA responses. Front. Immunol. 3, 65 (2012).
  MedlineGoogle Scholar
• 72 Obata T, Goto Y, Kunisawa J et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc. Natl Acad. Sci. USA 107(16), 7419–7424 (2010).
  Medline CASGoogle Scholar
• 73 Riboulet-Bisson E, Sturme MH, Jeffery IB et al. Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. PLoS ONE 7(2), e31113 (2012).
  Medline CASGoogle Scholar
• 74 Murphy EF, Cotter PD, Hogan A et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut 62(2), 220–226 (2013).
  MedlineGoogle Scholar
• 75 Le Doare K, Holder B, Bassett A, Pannaraj PS. Mother's milk: a purposeful contribution to the development of the infant microbiota and immunity. Front. Immunol. 9, 361 (2018).
  MedlineGoogle Scholar
• 76 Devaux CA, Raoult D. The microbiological memory, an epigenetic regulator governing the balance between good health and metabolic disorders. Front. Microbiol. 9, 1379 (2018).
  MedlineGoogle Scholar
• 77 Ferrari A, Brusa T, Rutili A, Canzi E, Biavati B. Isolation and characterization of Methanobrevibacter oralis sp. nov. Curr. Microbiol. 29(1), 6 (1994).
  Google Scholar
• 78 Miller TL, Wolin MJ, Conway De Macario E, Macario AJ. Isolation of Methanobrevibacter smithii from human feces. Appl. Environ. Microbiol. 43(1), 227–232 (1982).
  Medline CASGoogle Scholar
• 79 Grine G, Boualam MA, Drancourt M. Methanobrevibacter smithii, a methanogen consistently colonising the newborn stomach. Eur. J. Clin. Microbiol. Infec. Dis. 36(12), 2449–2455 (2017). • Suggests that Methanobrevibacter smithii, the main human gut methanogenic archaea, is transmitthed through breastfeeding.
  Medline CASGoogle Scholar
• 80 Desnues B, Al Moussawi K, Raoult D. Defining causality in emerging agents of acute bacterial diarrheas: a step beyond the Koch's postulates. Future Microbiol. 5(12), 1787–1797 (2010).
  Google Scholar