The origin of human milk bacteria: Is there a bacterial entero-mammary pathway during late pregnancy and lactation?

Advances in Nutrition

Volumn 5, Issue 6, 2014, Pages 779-784

  Rodríguez, Juan M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BREAST MILK; CLASSIFICATION; FEMALE; GASTROINTESTINAL TRACT; HUMAN; INFANT; ISOLATION AND PURIFICATION; LACTATION; MICROBIOLOGY; MOUTH; PREGNANCY; SKIN;

BACTERIA; FEMALE; GASTROINTESTINAL TRACT; HUMANS; INFANT; LACTATION; MILK, HUMAN; MOUTH; PREGNANCY; SKIN;

EID: 84910677920     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.114.007229     Document Type: Article

References (70)

1. Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 2013;69:1-10.
2. Martín R, Langa S, Reviriego C, Jiménez E,Marín ML, Xaus J, Fernández L, Rodríguez JM. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 2003;143:754-8.
3. Jiménez E, Delgado S, Maldonado A, Arroyo R, Albújar M, García N, Jariod M, Fernández L, Gómez A, Rodríguez JM. Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol 2008;8:143.
4. Martín R, Jiménez E, Heilig HG, Fernández L, Marín ML, Zoetendal EG, Rodríguez JM. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol 2009;75:965-9.
5. Albesharat R, Ehrmann MA, Korakli M, Yazaji S, Vogel RF. Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst Appl Microbiol 2011;34:148-55.
6. Martín V, Maldonado A, Moles L, Rodríguez-Baños M, Del Campo R, Fernández L, Rodríguez JM, Jiménez E. Sharing of bacterial strains between breast milk and infant feces. J Hum Lact 2012;28:36-44.
7. Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical motherneonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol 2014;16:2881-904.
8. West PA, Hewitt JH, Murphy OM. The influence of methods of collection and storage on the bacteriology of human milk. J Appl Bacteriol 1979;46:269-77.
9. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon J, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009;326:1694-7.
10. Ramsay DT, Kent JC, Owens RA, Hartmann PE. Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics 2004;113: 361-7.
11. Martín R, Langa S, Reviriego C, Jiménez E, Marín ML, Olivares M, Boza J, Jiménez J, Fernández L, Xaus J, et al. The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics. Trends Food Sci Technol 2004;15:121-7.
12. Nasidze I, Li J, Quinque D, Tang K, Stoneking M. Global diversity in the human salivary microbiome. Genome Res 2009;19:636-43.
13. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005;43:5721-32.
14. Yang F, Zeng X, Ning K, Liu KL, Lo CC, Wang W, Chen J, Wang D, Huang R, Chang X, et al. Saliva microbiomes distinguish caries-active from healthy human populations. ISME J 2012;6:1-10.
15. Li Y, Teague E, Zhuang Z, Caufield PW. Screening for the spaP gene of Streptococcus mutans in predentate infants. J Dent Res 1997;76:102.
16. Caufield PW, Dasanayake AP, Li Y, Pan Y, Hsu J, Hardin JM. Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 2000;68:4018-23.
17. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. Br J Obstet Gynaecol 2002;109:527-33.
18. Cephas KD, Kim J, Mathai RA, Barry KA, Dowd SE, Meline BS, Swanson KS. Comparative analysis of salivary bacterial microbiome diversity in edentulous infants and their mothers or primary care givers using pyrosequencing. PLoS ONE 2011;6:e23503.
19. Jiménez E, Fernández L, Delgado S, García N, Albújar M, Gómez A, Rodríguez JM. Assessment of the bacterial diversity of human colostrum by cultural-based techniques: analysis of the staphylococcal and enterococcal populations. Res Microbiol 2008;159:595-601.
20. Hunt KM, Foster JA, Forney LJ, Schütte UME, Beck DL, Abdo Z, Fox LK, Williams JE, McGuire MK, McGuire MA. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 2011;6:e21313.
21. Gao Z, Tseng C, Pei Z, Blaser MJ. Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 2007;104:2927-32.
22. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC; NISC Comparative Sequencing Program, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA. Topographical and temporal diversity of the human skin microbiome. Science 2009;324:1190-2.
23. Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodríguez JM. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by caesarean section. Curr Microbiol 2005;51:270-4.
24. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med 2014;6:237ra65.
25. Sakata H, Yoshioka H, Fujita K. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur J Pediatr 1985;144:186-90.
26. Lundequist B, Nord CE, Winberg J. The composition of the faecal microflora in breastfed and bottle-fed infants from birth to eight weeks. Acta Paediatr Scand 1985;74:45-51.
27. Balmer SE, Wharton BA. Diet and faecal flora in the newborn: breast milk and infant formula. Arch Dis Child 1989;64:1672-7.
28. Adlerberth I, Lindberg E, Aberg N, Hesselmar B, Saalman R, Strannegård IL, Wold AE. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle. Pediatr Res 2006;59:96-101.
29. Schleifer KH, Hartinger A, Götz F. Occurrence of D-tagatose-6-phosphate pathway of D-galactose metabolism among staphylococci. FEMS Microbiol Lett 1978;3:9-11.
30. Hunt KM, Preuss J, Nissan C, Davlin CA, Williams JE, Shafii B, Richardson AD, McGuire MK, Bode L, McGuire MA. Human milk oligosaccharides promote the growth of staphylococci. Appl Environ Microbiol 2012;78:4763-70.
31. Otto M, Sussmuth R, Vuong C, Jung G, Gotz F. Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives. FEBS Lett 1999;450:257-62.
32. Otto M. Staphylococcus epidermidis; the 'accidental' pathogen. Nat Rev Microbiol 2009;7:555-67.
33. Iwase T,Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T,Mizunoe Y. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010;465:346-9.
34. Park B, Iwase T, Liu GY. Intranasal application of S. epidermidis prevents colonization by methicillin-resistant Staphylococcus aureus in mice. PLoS ONE 2011;6:e25880.
35. 2 produced by viridans group streptococci may contribute to inhibition of methicillin-resistant Staphylococcus aureus colonization of oral cavities in newborns. Clin Infect Dis 2001;32:1408-13.
36. Nickerson SC, Boddie RL. Effect of naturally occurring coagulase-negative staphylococcal infections on experimental challenge with major mastitis pathogens. J Dairy Sci 1994;77:2526-36.
37. Gueimonde M, Laitinen K, Salminen S, Isolauri E. Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 2007;92:64-6.
38. Perez PF, Doré J, Leclerc M, Levenez F, Benyacoub J, Serrant P, Segura-Roggero I, Schiffrin EJ, Donnet-Hughes A. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics 2007; 119:e724-32.
39. Kulagina EV, Shkoporov AN, Kafarskaia LI, Khokhlova EV, Volodin NN, Donskikh EE, Korshunova OV, Efimov BA. Molecular genetic study of species and strain variability in bifidobacteria population in intestinal microflora of breastfed infants and their mothers. Bull Exp Biol Med 2010;150:61-4.
40. Takahashi H, Mikami K, Nishino R, Matsuoka T, Kimura M, Koga Y. Comparative analysis of the properties of bifidobacterial isolates from fecal samples of mother-infant pairs. J Pediatr Gastroenterol Nutr 2010;51:653-60.
41. Makino H, Kushiro A, Ishikawa E, Muylaert D, Kubota H, Sakai T, Oishi K, Martin R, Ben Amor K, Oozeer R, et al. Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism. Appl Environ Microbiol 2011;77:6788-93.
42. Jiménez E, Fernández L, Maldonado A, Martín R, Olivares M, Xaus J, Rodríguez JM. Oral administration of lactobacilli strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Appl Environ Microbiol 2008;74:4650-5.
43. Abrahamsson TR, Sinkiewicz G, Jakobsson T, Fredrikson M, Björkstén B. Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr 2009;49:349-54.
44. Arroyo R, Martín V, Maldonado A, Jiménez E, Fernández L, Rodríguez JM. Treatment of infectious mastitis during lactation: antibiotics versus oral administration of lactobacilli isolated from breast milk. Clin Infect Dis 2010;50:1551-8.
45. Ouwehand AC, Isolauri E, He F, Hashimoto H, Benno Y, Salminen S. Differences in Bifidobacterium flora composition in allergic and healthy infants. J Allergy Clin Immunol 2001;108:144-5.
46. Vankerckhoven VV, Autgaerden TA, Huys G, Vancanneyt M, Swings J, Goossens H. Establishment of the PROSAFE collection of probiotic and human lactic acid bacteria. Microb Ecol Health Dis 2004;16:131-6.
47. Begier EM, Barrett NL, Mshar PA, Johnson DG, Hadler JL Connecticut Bioterrorism Field Epidemiology Response Team. Gram-positive rod surveillance for early anthrax detection. Emerg Infect Dis 2005;11: 1483-6.
48. Dasanayake AP, Li Y, Wiener H, Ruby JD, Lee MJ. Salivary Actinomyces naeslundii genospecies 2 and Lactobacillus casei levels predict pregnancy outcomes. J Periodontol 2005;76:171-7.
49. Rescigno M, Urbano M, Valzasina B, Francolín M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl J, Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001;2:361-7.
50. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT, Fang FC. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 1999;401:804-8.
51. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662-5.
52. Roitt I. Essential immunology. Oxford (UK): Blackwell Scientific Publications; 2001.
53. Bertotto A, Gerli R, Castellucci G, Scalise F, Vaccaro R. Human milk lymphocytes bearing the gamma/delta T-cell receptor are mostly delta TCS1-positive cells. Immunology 1991;74:360-1.
54. Newburg DS. Innate immunity and human milk. J Nutr 2005;135: 1308-12.
55. Langa S. Interactions between lactic acid bacteria, intestinal epithelial cells and immune cells: development of in vitro models [dissertation]. Madrid (Spain): Complutense University of Madrid; 2006.
56. Langa S, Maldonado A, Delgado S, Martín R, Martín V, Jiménez E, Ruíz-Barba JL, Mayo B, Connor RI, Suárez E, et al. Characterization of Lactobacillus salivarius CECT 5713, a strain isolated from human milk: from genotype to phenotype. Appl Microbiol Biotechnol 2012;94:1279-87.
57. Schweinburg FB, Seligman AM, Fine J. Transmural migration of intestinal bacteria: study based on use of radioactive Escherichia coli. N Engl J Med 1950;242:747-51.
58. Wolochow H, Hildebrand GJ, Lammanna C. Translocation of microorganism across the intestinal wall in rats: effect of microbial size and concentration. J Infect Dis 1966;116:523-8.
59. Berg RD, Garlington AW. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 1979;23:403-11.
60. Lichtman SM. Bacterial translocation in humans. J Pediatr Gastroenterol Nutr 2001;33:1-10.
61. Berg RD. Bacterial translocation from the gastrointestinal tract. Trends Microbiol 1995;3:149-54.
62. Rodriguez AV, Baigorí MD, Alvarez S, Castro GR, Oliver G. Phosphatidylinositol-specific phospholipase C activity in Lactobacillus rhamnosus with capacity to translocate. FEMS Microbiol Lett 2001;204:33-8.
63. Moore FA, Moore EE, Poggetti RS, Read RA. Postinjury shock and early bacteremia: a lethal combination. Arch Surg 1992;127:893-7.
64. Kernéis S, Caliot E, Stubbe H, Bogdanova A, Kraehenbuhl J, Pringault E. Molecular studies of the intestinal mucosal barrier physiopathology using cocultures of epithelial and immune cells: a technical update. Microbes Infect 2000;2:1119-24.
65. Jepson MA, Clark MA. The role of M cells in Salmonella infection. Microbes Infect 2001;3:1183-90.
66. Bengmark S, Jeppsson B. Gastrointestinal surface protection and mucosa reconditioning. JPEN J Parenter Enteral Nutr. 1995;19:410-5.
67. MacFie J. Current status of bacterial translocation as a cause of surgical sepsis. Br Med Bull 2004;71:1-11.
68. Hammond KA. Adaptation of the maternal intestine during lactation. J Mammary Gland Biol Neoplasia 1997;2:243-52.
69. Beischer NA, Mackay EV, Colditz PB. Obstetrics and the newborn. Philadelphia: W.B. Saunders Company; 1997.
70. Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol. 2012;9:565-76.