Relationship between Milk Microbiota, Bacterial Load, Macronutrients, and Human Cells during Lactation
Open accessAbstract
Human breast milk is considered the optimal nutrition for infants, providing essential nutrients and a broad range of bioactive compounds, as well as its own microbiota. However, the interaction among those components and the biological role of milk microorganisms is still uncovered. Thus, our aim was to identify the relationships between milk microbiota composition, bacterial load, macronutrients, and human cells during lactation. Bacterial load was estimated in milk samples from a total of 21 healthy mothers through lactation time by bacteria-specific qPCR targeted to the single-copy gene fusA. Milk microbiome composition and diversity was estimated by 16S-pyrosequencing and the structure of these bacteria in the fluid was studied by flow cytometry, qPCR, and microscopy. Fat, protein, lactose, and dry extract of milk as well as the number of somatic cells were also analyzed. We observed that milk bacterial communities were generally complex, and showed individual-specific profiles. Milk microbiota was dominated by Staphylococcus, Pseudomonas, Streptococcus, and Acinetobacter. Staphylococcus aureus was not detected in any of these samples from healthy mothers. There was high variability in composition and number of bacteria per milliliter among mothers and in some cases even within mothers at different time points. The median bacterial load was 10(6) bacterial cells/ml through time, higher than those numbers reported by 16S gene PCR and culture methods. Furthermore, milk bacteria were present in a free-living, "planktonic" state, but also in equal proportion associated to human immune cells. There was no correlation between bacterial load and the amount of immune cells in milk, strengthening the idea that milk bacteria are not sensed as an infection by the immune system.
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Streptococcal species constitute the majority of the infant oral microbiota.
“As such, streptococcal species constitute the majority of the infant oral microbiota.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [144]
Streptococci are capable of adhering to epithelial cells and are a dominant bacterial group in breast milk.
“Streptococci are capable of adhering to epithelial cells and are a dominant bacterial group in breast milk.144”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [144]
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Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 19,770 · see citing works
UCHIME improves sensitivity and speed of chimera detection
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr381 · Cited by 15,114 · see citing works
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
Li, W.-Z., & Godzik, A. (2006) · Bioinform. · doi:10.1093/bioinformatics/btl158 · Cited by 10,994 · 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
Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life
Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.004 · Cited by 3,315 · 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
Cabrera-Rubio, R., Collado, M. C., Laitinen, K., Salminen, S., Isolauri, E., & Mira, A. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.037382 · Cited by 886 · see citing works
Self-citationThe human milk microbiota: Origin and potential roles in health and disease
Fernández, L., Langa, S., Martín, V., Maldonado‐Barragán, A., Jiménez, E., Martı́n, R., & Rodríguez, J. M. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.09.001 · Cited by 849 · see citing works
Characterization 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
Functional Redundancy-Induced Stability of Gut Microbiota Subjected to Disturbance
Moya, A., & Ferrer, M. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.02.002 · Cited by 690 · 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
FunGene: the functional gene pipeline and repository
Fish, J. A., Chai, B., Wang, Q., Sun, Y., Brown, C. T., Tiedje, J. M., & Cole, J. R. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00291 · Cited by 631 · see citing works
The Microbiota of Breast Tissue and Its Association with Breast Cancer
Urbaniak, C., Gloor, G. B., Brackstone, M., Scott, L., Tangney, M., & Reid, G. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01235-16 · Cited by 625 · see citing works
Breast 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
Inhibition of Staphylococcus aureus by the commensal bacteria of human milk
Heikkilä, M., & Saris, P. E. J. (2003) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2003.02002.x · Cited by 501 · see citing works
Lewis, Z. T., Totten, S. M., Smilowitz, J. T., Popović, M., Parker, E. A., Lemay, D. G., Tassell, M. L. V., Miller, M. J., Jin, Y., German, J. B., et al. (2015) · Microbiome · doi:10.1186/s40168-015-0071-z · Cited by 412 · see citing works
Arroyo, R., Martín, V., Maldonado‐Barragán, A., Jiménez, E., Fernández, L., & Rodríguez, J. M. (2010) · Clinical Infectious Diseases · doi:10.1086/652763 · Cited by 365 · see citing works
Jost, T., Lacroix, C., Braegger, C., & Chassard, C. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513000597 · Cited by 356 · see citing works
Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota
Peterson, C. T., Sharma, V., Elmén, L., & Peterson, S. N. (2014) · Clinical & Experimental Immunology · doi:10.1111/cei.12474 · Cited by 318 · see citing works
Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota
Khodayar‐Pardo, P., Mira‐Pascual, L., Collado, M. C., & Martínez‐Costa, C. (2014) · Journal of Perinatology · doi:10.1038/jp.2014.47 · Cited by 302 · see citing works
Self-citationMetagenomic Analysis of Milk of Healthy and Mastitis-Suffering Women
Jiménez, E., de Andrés, J., Manrique, M., Pareja-Tobes, P., Tobes, R., Martínez-Blanch, J. F., Codoñer, F. M., Ramón, D., Fernández, L., & Rodríguez, J. M. (2015) · Journal of Human Lactation · doi:10.1177/0890334415585078 · Cited by 269 · see citing works
Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR
Collado, M. C., Delgado, S., Maldonado‐Barragán, A., & Rodríguez, J. M. (2009) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2009.02567.x · Cited by 259 · see citing works
Self-citationThe 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
Santos, S. R., & Ochman, H. (2004) · Environmental Microbiology · doi:10.1111/j.1462-2920.2004.00617.x · Cited by 240 · see citing works
Maternal and infant infections stimulate a rapid leukocyte response in breastmilk
Hassiotou, F., Hepworth, A. R., Metzger, P., et al. (2013) · Clinical & Translational Immunology · doi:10.1038/cti.2013.1 · Cited by 238 · see citing works
Characterization of the microbiome of nipple aspirate fluid of breast cancer survivors
Chan, A. A., Bashir, M., Rivas, M. N., Duvall, K., Sieling, P. A., Pieber, T. R., Vaishampayan, P., Love, S. M., & Lee, D. J. (2016) · Scientific Reports · doi:10.1038/srep28061 · Cited by 223 · see citing works
Human milk metagenome: a functional capacity analysis
Ward, T., Hosid, S., Ioshikhes, I. P., & Altosaar, I. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-116 · Cited by 220 · 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
Microbiome Diversity in the Bronchial Tracts of Patients with Chronic Obstructive Pulmonary Disease
Cabrera‐Rubio, R., García-Núñez, M., Setó, L., Antó, J. M., Moyá, A., Monsó, E., & Mira, Á. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.00767-12 · Cited by 213 · see citing works
Improved Detection of Bifidobacteria with Optimised 16S rRNA-Gene Based Pyrosequencing
Sim, K., Cox, M. J., Wopereis, H., Martı́n, R., Knol, J., Li, M., Cookson, W., Moffatt, M. F., & Kroll, J. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032543 · Cited by 196 · see citing works
Microbiota diversity and gene expression dynamics in human oral biofilms
Benítez‐Páez, A., Belda‐Ferre, P., Simón‐Soro, Á., & Mira, Á. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-311 · Cited by 192 · see citing works
Impact of mode of delivery on the milk microbiota composition of healthy women
Cabrera‐Rubio, R., Mira‐Pascual, L., Mira, Á., & Collado, M. C. (2015) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174415001397 · Cited by 176 · see citing works
Self-citationHuman Milk Components Modulate Toll-Like Receptor–Mediated Inflammation
He, Y., Lawlor, N. T., & Newburg, D. S. (2016) · Advances in Nutrition · doi:10.3945/an.115.010090 · Cited by 175 · see citing works
Metatranscriptomics reveals overall active bacterial composition in caries lesions
Simón‐Soro, Á., Navarro, M. G., & Mira, Á. (2014) · Journal of Oral Microbiology · doi:10.3402/jom.v6.25443 · Cited by 170 · see citing works
Delgado, S., Arroyo, R., Martı́n, R., et al. (2008) · BMC Infectious Diseases · doi:10.1186/1471-2334-8-51 · Cited by 119 · see citing works
Development: Mother's milk: A rich opportunity
Petherick, A. (2010) · Nature · doi:10.1038/468s5a · Cited by 105 · see citing works
Human Milk Oligosaccharides Promote the Growth of Staphylococci
Hunt, K. M., Preuss, J., Nissan, C., Davlin, C. A., Williams, J. E., Shafii, B., Richardson, A. D., McGuire, S., Bode, L., & McGuire, M. A. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00477-12 · Cited by 102 · see citing works
Rate of establishing the gut microbiota in infancy has consequences for future health
Dogra, S. K., Sakwińska, O., Soh, S., Ngom‐Bru, C., Brück, W. M., Berger, B. W., Brüssow, H., Karnani, N., Lee, Y. S., Yap, F. K. P., et al. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1078051 · Cited by 93 · see citing works
Chow, J., Panasevich, M. R., Alexander, D. C., Boler, B. M. V., Serao, M. C. R., Faber, T. A., Bauer, L. L., & Fahey, G. C., Jr. (2014) · Journal of Proteome Research · doi:10.1021/pr500011w · Cited by 75 · see citing works
Inter‐bacterial correlations in subgingival biofilms: a large‐scale survey
Loozen, G., Özçelik, O., Boon, N., Mol, A. D., Schoen, C., Quirynen, M., & Teughels, W. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12167 · Cited by 70 · see citing works
Ma, Z. S., Guan, Q., Ye, C., Zhang, C., Foster, J. A., & Forney, L. J. (2015) · Scientific Reports · doi:10.1038/srep08275 · Cited by 63 · see citing works
Hunt, K. M., Williams, J. E., Shafii, B., Hunt, M. K., Behre, R., Ting, R., McGuire, M. K., & McGuire, M. A. (2012) · Breastfeeding Medicine · doi:10.1089/bfm.2011.0141 · Cited by 63 · see citing works
Benítez‐Páez, A., Álvarez-Fernández, M., Belda‐Ferre, P., Rubido, S., Mira, Á., & Tomás, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057782 · Cited by 62 · see citing works
Lyra, G. D. M., Costa, E. D. S., de Jesus, P. B., de Matos, J. C. G., Caires, T. A., Oliveira, M. C., de Oliveira, E. C., Xi, Z., Nunes, J. M. D. C., & Davis, C. “. (2015) · Journal of Phycology · doi:10.1111/jpy.12281 · Cited by 59 · see citing works
Metabolite profiles of formula milk compared to breast milk
Scano, P., Murgia, A., Demuru, M., et al. (2016) · Food Research International · doi:10.1016/j.foodres.2016.06.024 · Cited by 47 · see citing works
Colostrum of Healthy Slovenian Mothers: Microbiota Composition and Bacteriocin Gene Prevalence
Obermajer, T., Lipoglavšek, L., Tompa, G., Treven, P., Lorbeg, P. M., Matijašić, B. B., & Rogelj, I. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123324 · Cited by 38 · see citing works
Somatic Cells Count in Cow’s Bulk Tank Milk
Olechnowicz, J., & Jaśkowski, J. M. (2012) · Journal of Veterinary Medical Science · doi:10.1292/jvms.11-0506 · Cited by 37 · see citing works
Revealing microbial recognition by specific antibodies
Simón‐Soro, Á., D’Auria, G., Collado, M. C., Džunková, M., Culshaw, S., & Mira, Á. (2015) · BMC Microbiology · doi:10.1186/s12866-015-0456-y · Cited by 34 · see citing works
Self-citationHagi, T., Sasaki, K., Aso, H., et al. (2013) · Folia Microbiologica · doi:10.1007/s12223-013-0240-z · Cited by 25 · see citing works
Ma, Z. S., Li, L., Li, W., et al. (2016) · Scientific Reports · doi:10.1038/srep28048 · Cited by 16 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Langa S. (2006). Interactions Between Lactic Acid Bacteria, Intestinal Epithelial Cells and Immune Cells. Development of In vitro Models. Ph.D. Thesis, Madrid: Complutense University of Madrid.
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Sanguinetti, E., Guzzardi, M. A., Tripodi, M., Panetta, D., Selma-Royo, M., Zega, A., Telleschi, M., Collado, M. C., & Iozzo, P. (2019) · Scientific Reports · doi:10.1038/s41598-019-48090-8 · Cited by 45 · see citing works
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- Authors
- Boix-Amorós, A., Collado, M. C., & Mira, A.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- ORCID
- Boix-Amorós, Alba
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2016-04-20
- Volume
- 7
- Pages
- 1281-1281
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC4837678
- OpenAlex
- W2337004060
- Cited by
- 283
- References
- 51
- Citations by year
- 2026: 11 · 2025: 20 · 2024: 27 · 2023: 24 · 2022: 42 · 2021: 40 · 2020: 42 · 2019: 33 · 2018: 26 · 2017: 14 · 2016: 4
- FWCI
- 26.81
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- RiuNet (Universitat Politècnica de València) (submittedVersion, cc-by-nc-nd)
- Funders
- European Research Council (639226)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Milk Quality and Mastitis in Dairy Cows
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- breast milk microbiota, lactation, bacterial load, somatic cells, bacterioplankton, immune cells, Staphylococcus, Pseudomonas, Streptococcus, Acinetobacter, bacterial diversity, infant nutrition
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