The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery
Open accessAbstract
Background Breast milk is recognized as the most important postpartum element in metabolic and immunologic programming of health of neonates. The factors influencing the milk microbiome and the potential impact of microbes on infant health have not yet been uncovered.Objective Our objective was to identify pre- and postnatal factors that can potentially influence the bacterial communities inhabiting human milk.Design We characterized the milk microbial community at 3 different time points by pyrosequencing and quantitative polymerase chain reaction in mothers (n = 18) who varied in BMI, weight gain, and mode of delivery.Results We found that the human milk microbiome changes over lactation. Weisella, Leuconostoc, Staphylococcus, Streptococcus, and Lactococcus were predominant in colostrum samples, whereas in 1- and 6-mo milk samples the typical inhabitants of the oral cavity (eg, Veillonella, Leptotrichia, and Prevotella) increased significantly. Milk from obese mothers tended to contain a different and less diverse bacterial community compared with milk from normal-weight mothers. Milk samples from elective but not from nonelective mothers who underwent cesarean delivery contained a different bacterial community than did milk samples from individuals giving birth by vaginal delivery, suggesting that it is not the operation per se but rather the absence of physiological stress or hormonal signals that could influence the microbial transmission process to milk.Conclusions Our results indicate that milk bacteria are not contaminants and suggest that the milk microbiome is influenced by several factors that significantly skew its composition. Because bacteria present in breast milk are among the very first microbes entering the human body, our data emphasize the necessity to understand the biological role that the milk microbiome could potentially play for human health.
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Human milk harbors a unique microbial community, including commensal, mutualistic, and probiotic bacteria, some of which can be found as first colonizers of the neonatal gut.
“Human milk harbors a unique microbial community, including commensal, mutualistic, and probiotic bacteria, some of which can be found as first colonizers of the neonatal gut (258, 259).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [258]
Cites
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
Cole, J., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A., Mcgarrell, D., Marsh, T., Garrity, G., et al. (2008) · Nucleic Acids Res. · doi:10.1093/nar/gkn879 · Cited by 4,940 · see citing works
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002601107 · Cited by 4,774 · see citing works
UniFrac – An online tool for comparing microbial community diversity in a phylogenetic context
Lozupone, C., Hamady, M., & Knight, R. D. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-371 · Cited by 1,454 · see citing works
Early differences in fecal microbiota composition in children may predict overweight
Kalliomäki, M. A., Collado, M. C., Salminen, S., & Isolauri, E. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.3.534 · Cited by 1,056 · see citing works
Self-citationAccurate determination of microbial diversity from 454 pyrosequencing data
Quince, C., Lanzén, A., Curtis, T. P., Davenport, R. J., Hall, N., Head, I. M., Read, L. F., & Sloan, W. T. (2009) · Nature Methods · doi:10.1038/nmeth.1361 · Cited by 999 · see citing works
Yarza, P., Richter, M., Peplies, J., Euzéby, J. P., Amann, R., SCHLEIFER, K. H., Ludwig, W., Glöckner, F. O., & Rossello-Mora, R. A. (2008) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2008.07.001 · Cited by 932 · see citing works
Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women
Collado, M. C., Isolauri, E., Laitinen, K., & Salminen, S. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/88.4.894 · Cited by 863 · see citing works
Self-citationCharacterization of the Diversity and Temporal Stability of Bacterial Communities in Human Milk
Hunt, K. M., Foster, J. A., Forney, L. J., Schütte, U. M. E., Beck, D. L., Abdo, Z., Fox, L. K., Williams, J. E., McGuire, M. K., & McGuire, M. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021313 · Cited by 765 · see citing works
Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
Pérez, P. F., Dore, J. M., Leclerc, M., Levenez, F., Benyacoub, J., Serrant, P., Segura-Roggero, I., Schiffrin, E. J., & Donnet‐Hughes, A. (2007) · PEDIATRICS · doi:10.1542/peds.2006-1649 · Cited by 676 · see citing works
A meta‐analysis of the association between Caesarean section and childhood asthma
Thavagnanam, S., Fleming, J., Bromley, A., Shields, M. D., & Cardwell, C. R. (2008) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2007.02780.x · Cited by 651 · see citing works
The oral metagenome in health and disease
Belda‐Ferre, P., Alcaraz, L. D., Cabrera‐Rubio, R., Romero, H., Simón‐Soro, Á., Pignatelli, M., & Mira, Á. (2011) · The ISME Journal · doi:10.1038/ismej.2011.85 · Cited by 540 · see citing works
Self-citationBreast Milk as the Gold Standard for Protective Nutrients
Walker, A. W. (2010) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2009.11.021 · Cited by 517 · see citing works
Sipos, R., Székely, A. J., Palatinszky, M., Révész, S., Màrialigeti, K., & Nikolausz, M. (2007) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2007.00283.x · Cited by 464 · see citing works
The Macaque Gut Microbiome in Health, Lentiviral Infection, and Chronic Enterocolitis
McKenna, P. M., Hoffmann, C., Minkah, N. K., Aye, P. P., Lackner, A. A., Liu, Z. Z., Lozupone, C., Hamady, M., Knight, R. D., & Bushman, F. D. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040020 · Cited by 438 · see citing works
Martı́n, R., Jiménez, E., Heilig, H. G. H. J., Fernández, L., Marín, M. L., Zoetendal, E. G., & Rodríguez, J. M. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02063-08 · Cited by 434 · see citing works
Collado, M. C., Isolauri, E., Laitinen, K., & Salminen, S. (2010) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2010.29877 · Cited by 381 · see citing works
Self-citationMode of Delivery – Effects on Gut Microbiota and Humoral Immunity
Huurre, A., Kalliomäki, M. A., Rautava, S., Rinne, M., Salminen, S., & Isolauri, E. (2007) · Neonatology · doi:10.1159/000111102 · Cited by 354 · see citing works
Self-citationLaitinen, K., Poussa, T. A., Isolauri, E., & the Nutrition, A. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508111461 · Cited by 309 · see citing works
Self-citationDendritic Cells Shuttle Microbes Across Gut Epithelial Monolayers
Rescigno, M., Rotta, G., Valzasina, B., & Ricciardi-Castagnoli, P. (2001) · Immunobiology · doi:10.1078/0171-2985-00094 · Cited by 296 · see citing works
Roger, L. C., Costabile, A., Holland, D. T., Hoyles, L., & McCartney, A. L. (2010) · Microbiology · doi:10.1099/mic.0.043224-0 · Cited by 291 · see citing works
Grönlund, M., Gueimonde, M., Laitinen, K., Kociubinski, G., Grönroos, T., Salminen, S., & Isolauri, E. (2007) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2007.02849.x · Cited by 277 · see citing works
Self-citationCesarean Delivery Is Associated With Celiac Disease but Not Inflammatory Bowel Disease in Children
Decker, E., Engelmann, G., Findeisen, A., Gerner, P., Laass, M. W., Ney, D., Posovszky, C., Hoy, L., & Hornef, M. W. (2010) · PEDIATRICS · doi:10.1542/peds.2009-2260 · Cited by 275 · see citing works
The Mammary Gland and Its Origin During Synapsid Evolution
Oftedal, O. T. (2002) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1023/a:1022896515287 · Cited by 249 · see citing works
The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics
Martı́n, R., Langa, S., Reviriego, C., Jiménez, E., Marı́n, M. L., Olivares, M. M., Bozá, J., Jiménez, J., Fernández, L., Xaus, J., et al. (2003) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2003.09.010 · Cited by 243 · see citing works
Potential role of the intestinal microbiota of the mother in neonatal immune education
Donnet‐Hughes, A., Pérez, P. F., Dore, J. M., Leclerc, M., Levenez, F., Benyacoub, J., Serrant, P., Segura-Roggero, I., & Schiffrin, E. J. (2010) · Proceedings of The Nutrition Society · doi:10.1017/s0029665110001898 · Cited by 216 · see citing works
Compartmentalization of the Mucosal Immune Responses to Commensal Intestinal Bacteria
Macpherson, A. J., & Uhr, T. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1309.005 · Cited by 197 · see citing works
Bouder, E. L., Nores, J. E. R., Raby, A., Affolter, M., Vidal, K., Thornton, C. A., & Labéta, M. O. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.6.3742 · Cited by 133 · see citing works
Durbán, A., Abellan, J. J., Jiménez‐Hernández, N., Salgado, P., Ponce, M., Ponce, J. D. C., Garrigues, V., Latorre, A., & Moyá, A. (2012) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2012.00327.x · Cited by 110 · see citing works
Development: Mother's milk: A rich opportunity
Petherick, A. (2010) · Nature · doi:10.1038/468s5a · Cited by 105 · see citing works
Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum
Green, B. T., Lyte, M., Kulkarni, A. P., & Brown, D. R. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00225-x · Cited by 98 · see citing works
Aaltonen, J., Ojala, T. H., Laitinen, K., Poussa, T. A., Ozanne, S. E., & Isolauri, E. (2010) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2010.225 · Cited by 85 · see citing works
Self-citationQutaishat, S. S., Stemper, M. E., Spencer, S. K., et al. (2003) · PEDIATRICS · doi:10.1542/peds.111.6.1442 · Cited by 64 · see citing works
Establishment of intestinal homeostasis during the neonatal period
Stockinger, S., Hornef, M. W., & Chassin, C. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0831-2 · Cited by 58 · see citing works
Hoppu, U., Isolauri, E., Laakso, P., Matomäki, J., & Laitinen, K. (2011) · European Journal of Nutrition · doi:10.1007/s00394-011-0209-0 · Cited by 54 · see citing works
Self-citationModulation of dendritic cells and toll-like receptors by marathon running
Nickel, T., Emslander, I., Sisic, Z., David, R., Schmaderer, C., Marx, N., Schmidt‐Trucksäss, A., Hoster, E., Halle, M., Weis, M., et al. (2011) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2140-8 · Cited by 49 · see citing works
Brandtzæg, P. (2009) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000235781 · Cited by 23 · see citing works
Gut microbes extend reach to systemic innate immunity
Philpott, D. J., & Girardin, S. E. (2010) · Nature Medicine · doi:10.1038/nm0210-160 · Cited by 18 · see citing works
Flagged first, then by citations
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The Complex Microbiota of Raw Milk
Quigley, L., O'Sullivan, O., Stanton, C., Beresford, T. P., Ross, R. P., Fitzgerald, G. F., & Cotter, P. D. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12030 · Cited by 919 · see citing works
The Human Microbiome and Child Growth – First 1000 Days and Beyond
Robertson, R. C., Manges, A. R., Finlay, B. B., & Prendergast, A. J. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2018.09.008 · Cited by 793 · see citing works
Development of the gut microbiota in infancy and its impact on health in later life
Tanaka, M., & Nakayama, J. (2017) · Allergology International · doi:10.1016/j.alit.2017.07.010 · Cited by 639 · see citing works
Breast milk, a source of beneficial microbes and associated benefits for infant health
Lyons, K. E., Ryan, C. A., Dempsey, E. M., Ross, R. P., & Stanton, C. (2020) · Nutrients · doi:10.3390/nu12041039 · Cited by 613 · see citing works
Microbial Dysbiosis Is Associated with Human Breast Cancer
Xuan, C., Shamonki, J. M., Chung, A., DiNome, M. L., Chung, M., Sieling, P. A., & Lee, D. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083744 · Cited by 543 · see citing works
Mother’s Milk: A purposeful contribution to the development of the infant microbiota and immunity
Le Doare, K., Holder, B., Bassett, A., & Pannaraj, P. S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00361 · Cited by 475 · see citing works
Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
Asnicar, F., Manara, S., Zolfo, M., Truong, D. T., Scholz, M., Armanini, F., Ferretti, P., Gorfer, V., Pedrotti, A., Tett, A., et al. (2017) · mSystems · doi:10.1128/msystems.00164-16 · Cited by 445 · see citing works
Role of priority effects in the early-life assembly of the gut microbiota
Sprockett, D., Fukami, T., & Relman, D. A. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.173 · Cited by 419 · see citing works
The Microbiome and Human Biology
Knight, R., Callewaert, C., Marotz, C., Hyde, E. R., Debelius, J. W., McDonald, D., & Sogin, M. L. (2017) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-083115-022438 · Cited by 373 · see citing works
Boix-Amorós, A., Collado, M. C., & Mira, A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00492 · Cited by 283 · see citing works
Self-citationDzidic, M., Collado, M. C., Abrahamsson, T., Artacho, A., Stensson, M., Jenmalm, M. C., & Mira, A. (2018) · The ISME Journal · doi:10.1038/s41396-018-0204-z · Cited by 279 · see citing works
Self-citationJost, T., Lacroix, C., Braegger, C., & Chassard, C. (2015) · Nutrition Reviews · doi:10.1093/nutrit/nuu016 · Cited by 267 · see citing works
Maternal vertical transmission affecting early-life microbiota development
Wang, S., Ryan, C. A., Boyaval, P., Dempsey, E. M., Ross, R. P., & Stanton, C. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2019.07.010 · Cited by 243 · see citing works
Garrido, D., Dallas, D. C., & Mills, D. A. (2013) · Microbiology · doi:10.1099/mic.0.064113-0 · Cited by 228 · see citing works
The gut microbiota and its role in the development of allergic disease: A wider perspective
West, C. E., Jenmalm, M. C., & Prescott, S. L. (2015) · Clinical & Experimental Allergy · doi:10.1111/cea.12332 · Cited by 223 · see citing works
Davis, E. C., Wang, M., & Donovan, S. M. (2017) · Gut Microbes · doi:10.1080/19490976.2016.1278104 · Cited by 169 · see citing works
Yeoman, C. J., Ishaq, S. L., Bichi, E., Olivo, S. K., Lowe, J., & Aldridge, B. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-21440-8 · Cited by 168 · see citing works
Cenit, M. C., Nuevo, I. C., Codoñer-Franch, P., Dinan, T. G., & Sanz, Y. (2017) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-0969-z · Cited by 163 · see citing works
Costantini, L., Magno, S., Albanese, D., Donati, C., Molinari, R., Filippone, A., Masetti, R., & Merendino, N. (2018) · Scientific Reports · doi:10.1038/s41598-018-35329-z · Cited by 144 · see citing works
Factors influencing the gut microbiome in children: from infancy to childhood
Kumbhare, S. V., Patangia, D. V., Patil, R. H., Shouche, Y. S., & Patil, N. P. (2019) · Journal of Biosciences · doi:10.1007/s12038-019-9860-z · Cited by 143 · see citing works
Nash, M. J., Frank, D. N., & Friedman, J. E. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00349 · Cited by 101 · see citing works
Maternal modifiers of the infant gut microbiota: Metabolic consequences
Mulligan, C. M., & Friedman, J. E. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0303 · Cited by 101 · see citing works
Gut microbiota: a source of novel tools to reduce the risk of human disease?
Collado, M. C., Rautava, S., Isolauri, E., & Salminen, S. (2015) · Pediatric Research · doi:10.1038/pr.2014.173 · Cited by 93 · see citing works
Self-citationValverde-Molina, J., & García-Marcos, L. (2023) · Nutrients · doi:10.3390/nu15030486 · Cited by 92 · see citing works
Childhood Obesity: Immune Response and Nutritional Approaches
Magrone, T., & Jirillo, E. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00076 · Cited by 67 · see citing works
“In this framework, evidence has been provided that milk from obese mothers is enriched in Staphylococcus and Lactobacillus with lower counts of Bifidobacterium when compared to that of normal weight women over the first 6 months of breastfeeding (150).”
BackgroundDietary Habits of 2- to 9-Year-Old American Children Are Associated with Gut Microbiome Composition
Herman, D. R., Rhoades, N., Mercado, J., Argueta, P., Lopez, U., & Flores, G. E. (2020) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2019.07.024 · Cited by 50 · see citing works
High-Resolution Analyses of Overlap in the Microbiota Between Mothers and Their Children
Schanche, M., Avershina, E., Dotterud, C., Øien, T., Storrø, O., Johnsen, R., & Rudi, K. (2015) · Current Microbiology · doi:10.1007/s00284-015-0843-5 · Cited by 35 · see citing works
Zacarías, M. F., Binetti, A., Bockelmann, W., Reinheimer, J., Heller, K., & Vinderola, G. (2019) · International Microbiology · doi:10.1007/s10123-018-00046-0 · Cited by 10 · see citing works
The road not taken: host genetics in shaping intergenerational microbiomes
Zeng, S., Wang, S., Ross, R. P., & Stanton, C. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.05.016 · Cited by 9 · see citing works
Assessing the Influence of Dietary History on Gut Microbiota
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- Authors
- Cabrera-Rubio, R., Collado, M. C., Laitinen, K., Salminen, S., Isolauri, E., & Mira, A.
- Corresponding author
- Collado, M Carmen
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 96
- Issue
- 3
- Pages
- 544-551
- ISSN
- 0002-9165 (ISSN-L)
- OpenAlex
- W2116758389
- Cited by
- 886
- References
- 38
- Citations by year
- 2026: 24 · 2025: 52 · 2024: 56 · 2023: 53 · 2022: 66 · 2021: 84 · 2020: 94 · 2019: 72 · 2018: 73 · 2017: 74 · 2016: 72 · 2015: 77 · 2014: 45 · 2013: 35 · 2012: 8
- FWCI
- 49.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Epidemiology › Breastfeeding Practices and Influences
- Keywords
- human milk microbiome, lactation, maternal obesity, gestational weight gain, mode of delivery, cesarean section, vaginal delivery, colostrum, bacterial community composition, Leuconostoc, Veillonella, Prevotella, Leptotrichia, Staphylococcus, Streptococcus, Lactococcus, infant health, neonatal microbiome
- MeSH terms
- Adult, Colostrum, Feeding Methods, Female, Follow-Up Studies, Gram-Negative Bacteria, Gram-Positive Bacteria, Humans, Lactation, Milk, Human, Obesity, Pregnancy, Pregnancy Complications, Weight Gain, Body Mass Index, Principal Component Analysis, Delivery, Obstetric, Molecular Typing
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