Human milk microbiome: Difference between revisions
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The '''human milk microbiome''' refers to the community of microorganisms residing in the human mammary glands and breastmilk<ref name=":0" /> |
The '''human milk microbiome''' refers to the community of microorganisms residing in the human mammary glands and breastmilk.<ref name=":0" /> Human milk has been traditionally assumed to be sterile.<ref name=":0">{{cite journal | vauthors = Gomez-Gallego C, Garcia-Mantrana I, Salminen S, Collado MC | title = The human milk microbiome and factors influencing its composition and activity | journal = Seminars in Fetal & Neonatal Medicine | volume = 21 | issue = 6 | pages = 400–405 | date = December 2016 | pmid = 27286644 | doi = 10.1016/j.siny.2016.05.003 }}</ref><ref name=":1">{{cite journal | vauthors = Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM | title = The human milk microbiota: origin and potential roles in health and disease | journal = Pharmacological Research | volume = 69 | issue = 1 | pages = 1–10 | date = March 2013 | pmid = 22974824 | doi = 10.1016/j.phrs.2012.09.001 }}</ref> but more recently both culture and culture-independent techniques have confirmed that human milk contains diverse communities of bacteria which are distinct from other microbial communities inhabiting the human body.<ref name=":2">{{cite journal | vauthors = Martín R, Jiménez E, Heilig H, Fernández L, Marín ML, Zoetendal EG, Rodríguez JM | title = Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR | journal = Applied and Environmental Microbiology | volume = 75 | issue = 4 | pages = 965–9 | date = February 2009 | pmid = 19088308 | doi = 10.1128/aem.02063-08 }}</ref><ref name=":3">{{cite journal | vauthors = Díaz-Ropero MP, Martín R, Sierra S, Lara-Villoslada F, Rodríguez JM, Xaus J, Olivares M | title = Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response | journal = Journal of Applied Microbiology | volume = 102 | issue = 2 | pages = 337–43 | date = February 2007 | pmid = 17241338 | doi = 10.1111/j.1365-2672.2006.03102.x }}</ref><ref name=":4">{{cite journal | vauthors = Collado MC, Delgado S, Maldonado A, Rodríguez JM | title = Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR | journal = Letters in Applied Microbiology | volume = 48 | issue = 5 | pages = 523–8 | date = May 2009 | pmid = 19228290 | doi = 10.1111/j.1472-765x.2009.02567.x }}</ref> |
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== Taxonomic composition overview == |
== Taxonomic composition overview == |
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Bacteria commonly isolated in human milk samples include [[Bifidobacterium]], [[Lactobacillus]], [[Staphylococcus]], [[Streptococcus]], [[Bacteroides]], [[Clostridium]], [[Micrococcus]], [[Enterococcus]], and [[Escherichia]]<ref name=":3" /><ref name=":2" /><ref name=":4" />''.'' Metagenome analyses of human milk find it is dominated by ''Staphylococcus, Pseudomonas,'' and ''Edwardsiella''<ref>{{ |
Bacteria commonly isolated in human milk samples include [[Bifidobacterium]], [[Lactobacillus]], [[Staphylococcus]], [[Streptococcus]], [[Bacteroides]], [[Clostridium]], [[Micrococcus]], [[Enterococcus]], and [[Escherichia]]<ref name=":3" /><ref name=":2" /><ref name=":4" />''.'' Metagenome analyses of human milk find it is dominated by ''Staphylococcus, Pseudomonas,'' and ''Edwardsiella''<ref>{{cite journal | vauthors = Ward TL, Hosid S, Ioshikhes I, Altosaar I | title = Human milk metagenome: a functional capacity analysis | journal = BMC Microbiology | volume = 13 | pages = 116 | date = May 2013 | pmid = 23705844 | doi = 10.1186/1471-2180-13-116 }}</ref><ref name=":5">{{cite journal | vauthors = Jiménez E, de Andrés J, Manrique M, Pareja-Tobes P, Tobes R, Martínez-Blanch JF, Codoñer FM, Ramón D, Fernández L, Rodríguez JM | title = Metagenomic Analysis of Milk of Healthy and Mastitis-Suffering Women | journal = Journal of Human Lactation | volume = 31 | issue = 3 | pages = 406–15 | date = August 2015 | pmid = 25948578 | doi = 10.1177/0890334415585078 }}</ref>''.'' The human milk microbiome likely varies by population and between individual women,<ref name=":11">{{cite journal | vauthors = Kumar H, du Toit E, Kulkarni A, Aakko J, Linderborg KM, Zhang Y, Nicol MP, Isolauri E, Yang B, Collado MC, Salminen S | title = Distinct Patterns in Human Milk Microbiota and Fatty Acid Profiles Across Specific Geographic Locations | language = English | journal = Frontiers in Microbiology | volume = 7 | pages = 1619 | date = 2016 | pmid = 27790209 | doi = 10.3389/fmicb.2016.01619 }}</ref> however, a study based on a group of U.S. women observed the same 9 bacterial taxa in all samples from all of their participants, suggesting a common "core" of the milk microbiome, at least in that population.<ref name=":6">{{cite journal | vauthors = Hunt KM, Foster JA, Forney LJ, Schütte UM, Beck DL, Abdo Z, Fox LK, Williams JE, McGuire MK, McGuire MA | title = Characterization of the diversity and temporal stability of bacterial communities in human milk | journal = PloS One | volume = 6 | issue = 6 | pages = e21313 | date = 2011-06-17 | pmid = 21695057 | doi = 10.1371/journal.pone.0021313 }}</ref> Bacterial communities of human [[colostrum]] have been reported as being more diverse than those found in mature milk.<ref name=":0" /><ref name=":7">{{cite journal | vauthors = Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A | title = The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery | journal = The American Journal of Clinical Nutrition | volume = 96 | issue = 3 | pages = 544–51 | date = September 2012 | pmid = 22836031 | doi = 10.3945/ajcn.112.037382 }}</ref> |
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== Origins of establishment == |
== Origins of establishment == |
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While the origins of the human milk microbiome are not exactly known<ref name=":0" /> |
While the origins of the human milk microbiome are not exactly known,<ref name=":0" /> several hypotheses for its establishment have been proposed. Bacteria present in human milk may be derived from the surrounding breast skin<ref>{{cite journal | vauthors = West PA, Hewitt JH, Murphy OM | title = Influence of methods of collection and storage on the bacteriology of human milk | journal = The Journal of Applied Bacteriology | volume = 46 | issue = 2 | pages = 269–77 | date = April 1979 | pmid = 572360 | doi = 10.1111/j.1365-2672.1979.tb00820.x }}</ref><ref>{{cite journal | vauthors = Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA | title = Topographical and temporal diversity of the human skin microbiome | journal = Science | volume = 324 | issue = 5931 | pages = 1190–2 | date = May 2009 | pmid = 19478181 | doi = 10.1126/science.1171700 }}</ref> or the infant's oral cavity.<ref name=":6" /><ref name=":5" /><ref>{{cite journal | vauthors = Cephas KD, Kim J, Mathai RA, Barry KA, Dowd SE, Meline BS, Swanson KS | title = Comparative analysis of salivary bacterial microbiome diversity in edentulous infants and their mothers or primary care givers using pyrosequencing | journal = PloS One | volume = 6 | issue = 8 | pages = e23503 | date = 2011-08-10 | pmid = 21853142 | doi = 10.1371/journal.pone.0023503 }}</ref><ref>{{cite journal | vauthors = Nasidze I, Li J, Quinque D, Tang K, Stoneking M | title = Global diversity in the human salivary microbiome | journal = Genome Research | volume = 19 | issue = 4 | pages = 636–43 | date = April 2009 | pmid = 19251737 | doi = 10.1101/gr.084616.108 }}</ref> Retrograde backflow during nursing or suckling may also lead to bacterial establishment in the mammary duct,<ref>{{cite journal | vauthors = Rodríguez JM | title = The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation? | journal = Advances in Nutrition | volume = 5 | issue = 6 | pages = 779–84 | date = November 2014 | pmid = 25398740 | doi = 10.3945/an.114.007229 }}</ref> supported by the observation that a certain degree of flowback has been shown to occur during nursing using infrared photography<ref>{{cite journal | vauthors = Ramsay DT, Kent JC, Owens RA, Hartmann PE | title = Ultrasound imaging of milk ejection in the breast of lactating women | journal = Pediatrics | volume = 113 | issue = 2 | pages = 361–7 | date = February 2004 | pmid = 14754950 | doi = 10.1542/peds.113.2.361 }}</ref> Alternatively, bacteria may be translocated to the mammary duct from the maternal gastrointestinal tract via an entero-mammary pathway, facilitated by dendritic cells.<ref name=":1" /><ref name=":2" /><ref>{{cite journal | vauthors = Jeurink PV, van Bergenhenegouwen J, Jiménez E, Knippels LM, Fernández L, Garssen J, Knol J, Rodríguez JM, Martín R | title = Human milk: a source of more life than we imagine | journal = Beneficial Microbes | volume = 4 | issue = 1 | pages = 17–30 | date = March 2013 | pmid = 23271066 | doi = 10.3920/bm2012.0040 }}</ref> |
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== Factors shaping the human milk microbiome == |
== Factors shaping the human milk microbiome == |
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=== Geographic location === |
=== Geographic location === |
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Both the taxonomic composition and diversity of bacteria present in human milk likely vary by maternal geographic location<ref name=":0" /><ref name=":11" /><ref name=":6" /><ref>{{Cite journal|last=Lackey|first=Kimberly A|last2=Williams|first2=Janet E|last3=Meehan|first3=Courtney L|last4=Zachek|first4=Jessica A|last5=Benda|first5=Elizabeth D|last6=Price|first6=William J|last7=Foster|first7=James A|last8=Sellen|first8=Daniel W|last9=et al|first9=|date=|title=What's normal? Microbiomes in human milk and infant feces vary geographically and are related to each other |
Both the taxonomic composition and diversity of bacteria present in human milk likely vary by maternal geographic location<ref name=":0" /><ref name=":11" /><ref name=":6" /><ref>{{Cite journal|last=Lackey|first=Kimberly A|last2=Williams|first2=Janet E|last3=Meehan|first3=Courtney L|last4=Zachek|first4=Jessica A|last5=Benda|first5=Elizabeth D|last6=Price|first6=William J|last7=Foster|first7=James A|last8=Sellen|first8=Daniel W|last9=et al|first9=|date=|title=What's normal? Microbiomes in human milk and infant feces vary geographically and are related to each other|journal=|volume=Manuscript in preparation|pages=|separator=|via=}}</ref>, however, more large-scale studies are needed to better understand variation between populations.<ref name=":0" /> |
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=== Lactation stage === |
=== Lactation stage === |
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The human milk microbiome varies across lactation stage, with higher microbial diversity observed in colostrum than in mature milk<ref name=":0" /><ref name=":7" /> |
The human milk microbiome varies across lactation stage, with higher microbial diversity observed in colostrum than in mature milk.<ref name=":0" /><ref name=":7" /> Taxonomic composition of human milk also varies across the lactation period, initially dominated by ''Weisella, Leuconostoc, Staphylococcus, Streptococcus,'' and ''Lactococcus'' species<ref name=":7" />, and later comprised primarily of ''Veillonella, Prevotella, Leptotrichia, Lactobacillus, Streptococcus, Bifidobacterium,'' and ''Enterococcus''<ref name=":7" /><ref name=":8">{{cite journal | vauthors = Khodayar-Pardo P, Mira-Pascual L, Collado MC, Martínez-Costa C | title = Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota | journal = Journal of Perinatology | volume = 34 | issue = 8 | pages = 599–605 | date = August 2014 | pmid = 24674981 | doi = 10.1038/jp.2014.47 }}</ref> |
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=== Human milk oligosaccharides === |
=== Human milk oligosaccharides === |
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[[Human milk oligosaccharide]]<nowiki/>s, a primary component of human milk, are prebiotics which have been shown to promote growth of beneficial ''Bifidobacterium'' and ''Bacteroides'' species<ref>{{ |
[[Human milk oligosaccharide]]<nowiki/>s, a primary component of human milk, are prebiotics which have been shown to promote growth of beneficial ''Bifidobacterium'' and ''Bacteroides'' species.<ref>{{cite journal | vauthors = Bode L | title = Human milk oligosaccharides: prebiotics and beyond | journal = Nutrition Reviews | volume = 67 Suppl 2 | issue = suppl_2 | pages = S183-91 | date = November 2009 | pmid = 19906222 | doi = 10.1111/j.1753-4887.2009.00239.x }}</ref><ref>{{cite journal | vauthors = Jost T, Lacroix C, Braegger C, Chassard C | title = Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health | journal = Nutrition Reviews | volume = 73 | issue = 7 | pages = 426–37 | date = July 2015 | pmid = 26081453 | doi = 10.1093/nutrit/nuu016 }}</ref><ref name=":15" /> |
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=== Delivery mode === |
=== Delivery mode === |
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Mode of delivery may influence composition of the human milk microbiome, vaginal births being associated with high taxonomic diversity and high prevalence of ''Bifidobacterium'' and ''Lactobacillus,'' and the opposite trend being seen with Cesarean births<ref name=":7" /><ref name=":8" /><ref>{{ |
Mode of delivery may influence composition of the human milk microbiome, vaginal births being associated with high taxonomic diversity and high prevalence of ''Bifidobacterium'' and ''Lactobacillus,'' and the opposite trend being seen with Cesarean births,<ref name=":7" /><ref name=":8" /><ref>{{cite journal | vauthors = Cabrera-Rubio R, Mira-Pascual L, Mira A, Collado MC | title = Impact of mode of delivery on the milk microbiota composition of healthy women | journal = Journal of Developmental Origins of Health and Disease | volume = 7 | issue = 1 | pages = 54–60 | date = February 2016 | pmid = 26286040 | doi = 10.1017/S2040174415001397 }}</ref><ref name=":9">{{cite journal | vauthors = Soto A, Martín V, Jiménez E, Mader I, Rodríguez JM, Fernández L | title = Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors | journal = Journal of Pediatric Gastroenterology and Nutrition | volume = 59 | issue = 1 | pages = 78–88 | date = July 2014 | pmid = 24590211 | doi = 10.1097/mpg.0000000000000347 }}</ref><ref>{{cite journal | vauthors = Hoashi M, Meche L, Mahal LK, Bakacs E, Nardella D, Naftolin F, Bar-Yam N, Dominguez-Bello MG | title = Human Milk Bacterial and Glycosylation Patterns Differ by Delivery Mode | journal = Reproductive Sciences | volume = 23 | issue = 7 | pages = 902–7 | date = July 2016 | pmid = 26711314 | doi = 10.1177/1933719115623645 }}</ref> however, no relationship between delivery mode and the maternal milk microbiome has also been observed.<ref>{{cite journal | vauthors = Urbaniak C, Angelini M, Gloor GB, Reid G | title = Human milk microbiota profiles in relation to birthing method, gestation and infant gender | journal = Microbiome | volume = 4 | issue = 1 | pages = 1 | date = January 2016 | pmid = 26739322 | doi = 10.1186/s40168-015-0145-y }}</ref> |
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=== Gestational age === |
=== Gestational age === |
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Women delivering term and preterm show differences in their milk microbiome composition, with mothers of term-births showing lower abundances of ''Enterococcus'' species and higher amounts of ''Bifidobacterium'' species in their milk than mothers of pre-term births<ref name=":8" /> |
Women delivering term and preterm show differences in their milk microbiome composition, with mothers of term-births showing lower abundances of ''Enterococcus'' species and higher amounts of ''Bifidobacterium'' species in their milk than mothers of pre-term births.<ref name=":8" /> |
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=== Maternal health === |
=== Maternal health === |
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Maternal health status is associated with changes in the bacterial composition of milk. Higher maternal [[body mass index]] (BMI) and obesity are associated with changes in the levels of ''Bifidobacterium'' and ''Staphylococcus'' species and overall lower bacterial diversity<ref name=":7" /><ref>{{ |
Maternal health status is associated with changes in the bacterial composition of milk. Higher maternal [[body mass index]] (BMI) and obesity are associated with changes in the levels of ''Bifidobacterium'' and ''Staphylococcus'' species and overall lower bacterial diversity.<ref name=":7" /><ref>{{cite journal | vauthors = Collado MC, Laitinen K, Salminen S, Isolauri E | title = Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk | journal = Pediatric Research | volume = 72 | issue = 1 | pages = 77–85 | date = July 2012 | pmid = 22453296 | doi = 10.1038/pr.2012.42 }}</ref> Milk of women with celiac disease is observed to have reduced levels of ''Bacteroides'' and ''Bifidobacterium''<ref>{{cite journal | vauthors = Olivares M, Albrecht S, De Palma G, Ferrer MD, Castillejo G, Schols HA, Sanz Y | title = Human milk composition differs in healthy mothers and mothers with celiac disease | journal = European Journal of Nutrition | volume = 54 | issue = 1 | pages = 119–28 | date = February 2015 | pmid = 24700375 | doi = 10.1007/s00394-014-0692-1 }}</ref> Women who are HIV-positive show higher bacterial diversity and increased abundances of ''Lactobacillus'' in their milk than do non-HIV-positive women.<ref>{{cite journal | vauthors = González R, Maldonado A, Martín V, Mandomando I, Fumadó V, Metzner KJ, Sacoor C, Fernández L, Macete E, Alonso PL, Rodríguez JM, Menendez C | title = Breast milk and gut microbiota in African mothers and infants from an area of high HIV prevalence | journal = PloS One | volume = 8 | issue = 11 | pages = e80299 | date = 2013-11-26 | pmid = 24303004 | doi = 10.1371/journal.pone.0080299 }}</ref> [[Mastitis]] has been linked to changes in human milk microbiota at the phylum level, lower microbial diversity, and decreased abundance of obligate anaerobic taxa.<ref>{{cite journal | vauthors = Patel SH, Vaidya YH, Patel RJ, Pandit RJ, Joshi CG, Kunjadiya AP | title = Culture independent assessment of human milk microbial community in lactational mastitis | journal = Scientific Reports | volume = 7 | issue = 1 | pages = 7804 | date = August 2017 | pmid = 28798374 | doi = 10.1038/s41598-017-08451-7 }}</ref><ref>{{cite journal | vauthors = Delgado S, Arroyo R, Martín R, Rodríguez JM | title = PCR-DGGE assessment of the bacterial diversity of breast milk in women with lactational infectious mastitis | journal = BMC Infectious Diseases | volume = 8 | pages = 51 | date = April 2008 | pmid = 18423017 | doi = 10.1186/1471-2334-8-51 }}</ref><ref name=":5" /> |
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=== Antibiotic use === |
=== Antibiotic use === |
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Maternal perinatal antibiotic use is associated with changes in the prevalence of ''Lactobacillus, Bifidobacterium, Staphylococcus,'' and ''Eubacterium'' in milk<ref name=":9" /><ref>{{ |
Maternal perinatal antibiotic use is associated with changes in the prevalence of ''Lactobacillus, Bifidobacterium, Staphylococcus,'' and ''Eubacterium'' in milk.<ref name=":9" /><ref>{{cite journal | vauthors = Witt A, Mason MJ, Burgess K, Flocke S, Zyzanski S | title = A case control study of bacterial species and colony count in milk of breastfeeding women with chronic pain | journal = Breastfeeding Medicine | volume = 9 | issue = 1 | pages = 29–34 | date = 2014-01-23 | pmid = 23789831 | doi = 10.1089/bfm.2013.0012 }}</ref><ref>{{cite journal | vauthors = Urbaniak C, Cummins J, Brackstone M, Macklaim JM, Gloor GB, Baban CK, Scott L, O'Hanlon DM, Burton JP, Francis KP, Tangney M, Reid G | title = Microbiota of human breast tissue | journal = Applied and Environmental Microbiology | volume = 80 | issue = 10 | pages = 3007–14 | date = May 2014 | pmid = 24610844 | doi = 10.1128/aem.00242-14 }}</ref> |
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=== Maternal diet === |
=== Maternal diet === |
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Few studies have been conducted examining the influence of maternal diet on the milk microbiome<ref name=":0" /> |
Few studies have been conducted examining the influence of maternal diet on the milk microbiome,<ref name=":0" /> but diet is known to influence other aspects of milk composition, such as the lipid profile<ref>{{cite journal | vauthors = Nishimura RY, Barbieiri P, Castro GS, Jordão AA, Perdoná G, Sartorelli DS | title = Dietary polyunsaturated fatty acid intake during late pregnancy affects fatty acid composition of mature breast milk | journal = Nutrition | volume = 30 | issue = 6 | pages = 685–9 | date = June 2014 | pmid = 24613435 | doi = 10.1016/j.nut.2013.11.002 }}</ref><ref>{{cite journal | vauthors = Peng Y, Zhou T, Wang Q, Liu P, Zhang T, Zetterström R, Strandvik B | title = Fatty acid composition of diet, cord blood and breast milk in Chinese mothers with different dietary habits | journal = Prostaglandins, Leukotrienes, and Essential Fatty Acids | volume = 81 | issue = 5-6 | pages = 325–30 | pmid = 19709866 | doi = 10.1016/j.plefa.2009.07.004 }}</ref> which in turn could affect its microbial composition.<ref name=":0" /> Variation in the fat and carbohydrate content of the maternal diet may influence the taxonomic composition of the milk microbiome.<ref>{{Cite journal|last=Meyer|first=Kristen M.|last2=Mohammad|first2=Mahmoud|last3=Bode|first3=Lars|last4=Chu|first4=Derrick M.|last5=Ma|first5=Jun|last6=Haymond|first6=Morey |last7=Aagaard|first7=Kjersti | name-list-format = vanc |title=20: Maternal diet structures the breast milk microbiome in association with human milk oligosaccharides and gut-associated bacteria |journal=American Journal of Obstetrics and Gynecology|volume=216|issue=1|doi=10.1016/j.ajog.2016.11.911}}</ref> |
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=== Social influences === |
=== Social influences === |
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Social network density of mother-infant dyads was found to be associated with increased bacterial diversity in the milk microbiome of mothers in the Central African Republic<ref>{{ |
Social network density of mother-infant dyads was found to be associated with increased bacterial diversity in the milk microbiome of mothers in the Central African Republic.<ref>{{cite journal | vauthors = Meehan CL, Lackey KA, Hagen EH, Williams JE, Roulette J, Helfrecht C, McGuire MA, McGuire MK | title = Social networks, cooperative breeding, and the human milk microbiome | journal = American Journal of Human Biology | volume = in press | pages = e23131 | date = April 2018 | pmid = 29700885 | doi = 10.1002/ajhb.23131 }}</ref> |
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== Influences on infant health and development == |
== Influences on infant health and development == |
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Breastfeeding is thought to be an important driver of infant gut microbiome establishment<ref>{{ |
Breastfeeding is thought to be an important driver of infant gut microbiome establishment.<ref>{{cite journal | vauthors = Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, Belzer C, Delgado Palacio S, Arboleya Montes S, Mancabelli L, Lugli GA, Rodriguez JM, Bode L, de Vos W, Gueimonde M, Margolles A, van Sinderen D, Ventura M | title = The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota | journal = Microbiology and Molecular Biology Reviews | volume = 81 | issue = 4 | pages = e00036–17 | date = December 2017 | pmid = 29118049 | doi = 10.1128/mmbr.00036-17 }}</ref> The gut microbiome of breastfed infants is less diverse, contains higher amounts of ''Bifidobacterium'' and ''Lactobacillus'' species, and fewer potential pathogenic taxa than the gut microbiome of formula-fed infants.<ref>{{cite journal | vauthors = Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI | title = Human gut microbiome viewed across age and geography | journal = Nature | volume = 486 | issue = 7402 | pages = 222–7 | date = May 2012 | pmid = 22699611 | doi = 10.1038/nature11053 }}</ref><ref>{{cite journal | vauthors = O'Sullivan A, Farver M, Smilowitz JT | title = The Influence of Early Infant-Feeding Practices on the Intestinal Microbiome and Body Composition in Infants | journal = Nutrition and Metabolic Insights | volume = 8 | issue = Suppl 1 | pages = 1–9 | date = 2015 | pmid = 26715853 | pmc = 4686345 | doi = 10.4137/NMI.S29530 }}</ref><ref>{{cite journal | vauthors = Bezirtzoglou E, Tsiotsias A, Welling GW | title = Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH) | journal = Anaerobe | volume = 17 | issue = 6 | pages = 478–82 | date = December 2011 | pmid = 21497661 | doi = 10.1016/j.anaerobe.2011.03.009 }}</ref> Human milk bacteria may reduce risk of infection in breastfed infants by competitively excluding harmful bacteria,<ref name=":10">{{cite journal | vauthors = Olivares M, Díaz-Ropero MP, Martín R, Rodríguez JM, Xaus J | title = Antimicrobial potential of four Lactobacillus strains isolated from breast milk | journal = Journal of Applied Microbiology | volume = 101 | issue = 1 | pages = 72–9 | date = July 2006 | pmid = 16834593 | doi = 10.1111/j.1365-2672.2006.02981.x }}</ref><ref>{{cite journal | vauthors = Heikkilä MP, Saris PE | title = Inhibition of Staphylococcus aureus by the commensal bacteria of human milk | journal = Journal of Applied Microbiology | volume = 95 | issue = 3 | pages = 471–8 | date = 2003 | pmid = 12911694 }}</ref> and producing antimicrobial compounds which eliminate pathogenic strains,<ref>{{cite journal | vauthors = Beasley SS, Saris PE | title = Nisin-producing Lactococcus lactis strains isolated from human milk | journal = Applied and Environmental Microbiology | volume = 70 | issue = 8 | pages = 5051–3 | date = August 2004 | pmid = 15294850 | doi = 10.1128/aem.70.8.5051-5053.2004 }}</ref><ref>{{cite journal | vauthors = Martín R, Olivares M, Marín ML, Fernández L, Xaus J, Rodríguez JM | title = Probiotic potential of 3 Lactobacilli strains isolated from breast milk | journal = Journal of Human Lactation | volume = 21 | issue = 1 | pages = 8–17; quiz 18-21, 41 | date = February 2005 | pmid = 15681631 | doi = 10.1177/0890334404272393 }}</ref><ref>{{cite journal | vauthors = Martín R, Jiménez E, Olivares M, Marín ML, Fernández L, Xaus J, Rodríguez JM | title = Lactobacillus salivarius CECT 5713, a potential probiotic strain isolated from infant feces and breast milk of a mother-child pair | journal = International Journal of Food Microbiology | volume = 112 | issue = 1 | pages = 35–43 | date = October 2006 | pmid = 16843562 | doi = 10.1016/j.ijfoodmicro.2006.06.011 }}</ref><ref name=":10" /> Certain lactobacilli and bifidobacteria, the growth of which is stimulated by human milk oligosaccharides<ref>{{cite journal | vauthors = Bode L | title = Human milk oligosaccharides: every baby needs a sugar mama | journal = Glycobiology | volume = 22 | issue = 9 | pages = 1147–62 | date = September 2012 | pmid = 22513036 | doi = 10.1093/glycob/cws074 }}</ref> contribute to healthy metabolic and immune-related functioning in the infant gut.<ref>{{cite journal | vauthors = Zivkovic AM, German JB, Lebrilla CB, Mills DA | title = Human milk glycobiome and its impact on the infant gastrointestinal microbiota | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 Suppl 1 | issue = Supplement 1 | pages = 4653–8 | date = March 2011 | pmid = 20679197 | doi = 10.1073/pnas.1000083107 }}</ref><ref>{{cite journal | vauthors = Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, Kumagai H, Ashida H, Hirose J, Kitaoka M | title = Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria | journal = The Journal of Biological Chemistry | volume = 286 | issue = 40 | pages = 34583–92 | date = October 2011 | pmid = 21832085 | pmc = 3186357 | doi = 10.1074/jbc.M111.248138 }}</ref><ref name=":1" /><ref name=":12">{{cite journal | vauthors = Donnet-Hughes A, Perez PF, Doré J, Leclerc M, Levenez F, Benyacoub J, Serrant P, Segura-Roggero I, Schiffrin EJ | title = Potential role of the intestinal microbiota of the mother in neonatal immune education | journal = The Proceedings of the Nutrition Society | volume = 69 | issue = 3 | pages = 407–15 | date = August 2010 | pmid = 20633308 | doi = 10.1017/S0029665110001898 }}</ref> |
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== Evolutionary implications == |
== Evolutionary implications == |
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There is some indication of relationships between milk microbiota and other human milk components, including human milk oligosaccharides (HMOs), maternal cells, and nutrient profiles<ref name=":15">{{ |
There is some indication of relationships between milk microbiota and other human milk components, including human milk oligosaccharides (HMOs), maternal cells, and nutrient profiles.<ref name=":15">{{cite journal | vauthors = Williams JE, Price WJ, Shafii B, Yahvah KM, Bode L, McGuire MA, McGuire MK | title = Relationships Among Microbial Communities, Maternal Cells, Oligosaccharides, and Macronutrients in Human Milk | journal = Journal of Human Lactation | volume = 33 | issue = 3 | pages = 540–551 | date = August 2017 | pmid = 28609134 | doi = 10.1177/0890334417709433 }}</ref><ref name=":13">{{cite journal | vauthors = Boix-Amorós A, Collado MC, Mira A | title = Relationship between Milk Microbiota, Bacterial Load, Macronutrients, and Human Cells during Lactation | language = English | journal = Frontiers in Microbiology | volume = 7 | pages = 492 | date = 2016 | pmid = 27148183 | doi = 10.3389/fmicb.2016.00492 }}</ref> Specific bacterial genera have been shown to be associated with variation in levels of milk macronutrients such as lactose, proteins, and fats.<ref name=":13" /> HMOs selectively facilitate growth of particular beneficial bacteria, notably ''Bifidobacterium'' species.<ref>{{cite book|last1=Clancy|first1=Kathryn B.H.|last2=Hinde|first2=Katie|last3=Rutherford|first3=Julienne N. | name-list-format = vanc |title=Building babies: primate development in proximate and ultimate perspective|series=Developments in Primatology: Progress and Prospects|date=2013|publisher=Springer|location=New York|isbn=978-1-4614-4059-8|doi=10.1007/978-1-4614-4060-4_11}}</ref><ref>{{cite journal | vauthors = Sela DA, Mills DA | title = Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides | journal = Trends in Microbiology | volume = 18 | issue = 7 | pages = 298–307 | date = July 2010 | pmid = 20409714 | pmc = 2902656 | doi = 10.1016/j.tim.2010.03.008 }}</ref> Furthermore, as bifidobacterial genomes are uniquely equipped to metabolize HMOs<ref>{{cite journal | vauthors = Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, Price NP, Richardson PM, Mills DA | title = The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 105 | issue = 48 | pages = 18964–9 | date = December 2008 | pmid = 19033196 | pmc = 2596198 | doi = 10.1073/pnas.0809584105 }}</ref>, which are otherwise indigestible by enzymes of the infant gut, some have suggested a coevolutionary dynamic between HMOs and certain bacteria common in both the milk and infant gastrointestinal microbiomes.<ref>{{cite journal | vauthors = German JB, Freeman SL, Lebrilla CB, Mills DA | title = Human milk oligosaccharides: evolution, structures and bioselectivity as substrates for intestinal bacteria | journal = Nestle Nutrition Workshop Series. Paediatric Programme | volume = 62 | pages = 205–18; discussion 218-22 | date = 2008 | pmid = 18626202 | pmc = 2861563 | doi = 10.1159/000146322 }}</ref><ref name=":14">{{cite journal | vauthors = Allen-Blevins CR, Sela DA, Hinde K | title = Milk bioactives may manipulate microbes to mediate parent-offspring conflict | journal = Evolution, Medicine, and Public Health | volume = 2015 | issue = 1 | pages = 106–21 | date = April 2015 | pmid = 25835022 | pmc = 4512713 | doi = 10.1093/emph/eov007 }}</ref> Furthermore, relative to other mammalian milks, primate milk, particularly human milk, appears to be unique with respect to the complexity and diversity of its oligosaccharide repertoire. Human milk is typified by greater overall HMO diversity and predominance of oligosaccharides known to promote growth of ''Bifidobacterium'' in the infant gut.<ref>{{cite journal | vauthors = Urashima T, Odaka G, Asakuma S, Uemura Y, Goto K, Senda A, Saito T, Fukuda K, Messer M, Oftedal OT | title = Chemical characterization of oligosaccharides in chimpanzee, bonobo, gorilla, orangutan, and siamang milk or colostrum | journal = Glycobiology | volume = 19 | issue = 5 | pages = 499–508 | date = May 2009 | pmid = 19164487 | doi = 10.1093/glycob/cwp006 }}</ref> Milk microbiota are thought to play an essential role in programming the infant immune system, and tend to reduce the risk of adverse infant health outcomes.<ref name=":12" /> Differences in milk oligosaccharides between humans and non-human primates could be indicative of variation in pathogen exposure associated with increased sociality and group sizes.<ref>{{cite journal | vauthors = Tao N, Wu S, Kim J, An HJ, Hinde K, Power ML, Gagneux P, German JB, Lebrilla CB | title = Evolutionary glycomics: characterization of milk oligosaccharides in primates | journal = Journal of Proteome Research | volume = 10 | issue = 4 | pages = 1548–57 | date = April 2011 | pmid = 21214271 | pmc = 3070053 | doi = 10.1021/pr1009367 }}</ref> Together, these observations may indicate that milk microbial communities have coevolved with their human host.<ref name=":14" />, supported by the expectation that microbes which promote host health facilitate their own transmission and proliferation<ref>{{cite journal | vauthors = Funkhouser LJ, Bordenstein SR | title = Mom knows best: the universality of maternal microbial transmission | journal = PLoS Biology | volume = 11 | issue = 8 | pages = e1001631 | date = 2013 | pmid = 23976878 | pmc = 3747981 | doi = 10.1371/journal.pbio.1001631 }}</ref> |
||
== Known comparisons to other mammalian milk microbiomes == |
== Known comparisons to other mammalian milk microbiomes == |
||
Both human and macaque milks contains high abundances of ''Streptococcus'' and ''Lactobacillus'' bacteria, but differ in their respective relative abundances of these taxa<ref>{{ |
Both human and macaque milks contains high abundances of ''Streptococcus'' and ''Lactobacillus'' bacteria, but differ in their respective relative abundances of these taxa.<ref>{{cite journal | vauthors = Jin L, Hinde K, Tao L | title = Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta) | journal = Journal of Medical Primatology | volume = 40 | issue = 1 | pages = 52–8 | date = February 2011 | pmid = 20946146 | pmc = 3697067 | doi = 10.1111/j.1600-0684.2010.00450.x }}</ref> Bacteria observed to be most common in healthy bovine milk include ''Ralstonia'', ''Pseudomonas'', ''Sphingomonas'', ''Stenotrophomonas'', ''Psychrobacter'', ''Bradyrhizobium'', ''Corynebacterium'', ''Pelomonas'', ''Staphylococcus'', ''Fecalibacterium'', ''Lachnospiraceae'', ''Propionibacterium'', ''Aeribacillus'', ''Bacteroides'', ''Staphyloccus'', ''Streptococcus'', ''Anaerococcus'', ''Lactobacillus'', ''Porphyromonas'', ''Comamonas'', ''Fusobacterium'', and ''Enterococcus''.<ref>{{cite journal | vauthors = Kuehn JS, Gorden PJ, Munro D, Rong R, Dong Q, Plummer PJ, Wang C, Phillips GJ | title = Bacterial community profiling of milk samples as a means to understand culture-negative bovine clinical mastitis | journal = PloS One | volume = 8 | issue = 4 | pages = e61959 | date = 2013-04-25 | pmid = 23634219 | doi = 10.1371/journal.pone.0061959 }}</ref><ref>{{cite journal | vauthors = Oikonomou G, Bicalho ML, Meira E, Rossi RE, Foditsch C, Machado VS, Teixeira AG, Santisteban C, Schukken YH, Bicalho RC | title = Microbiota of cow's milk; distinguishing healthy, sub-clinically and clinically diseased quarters | journal = PloS One | volume = 9 | issue = 1 | pages = e85904 | date = 2014 | pmid = 24465777 | pmc = 3896433 | doi = 10.1371/journal.pone.0085904 }}</ref><ref>{{cite journal | vauthors = Zhang R, Huo W, Zhu W, Mao S | title = Characterization of bacterial community of raw milk from dairy cows during subacute ruminal acidosis challenge by high-throughput sequencing | journal = Journal of the Science of Food and Agriculture | volume = 95 | issue = 5 | pages = 1072–9 | date = March 2015 | pmid = 24961605 | doi = 10.1002/jsfa.6800 }}</ref><ref>{{cite journal | vauthors = Addis MF, Tanca A, Uzzau S, Oikonomou G, Bicalho RC, Moroni P | title = The bovine milk microbiota: insights and perspectives from -omics studies | journal = Molecular bioSystems | volume = 12 | issue = 8 | pages = 2359–72 | date = July 2016 | pmid = 27216801 | doi = 10.1039/c6mb00217j }}</ref> |
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== See also == |
== See also == |
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== References == |
== References == |
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Revision as of 16:36, 2 May 2018
The human milk microbiome refers to the community of microorganisms residing in the human mammary glands and breastmilk.[1] Human milk has been traditionally assumed to be sterile.[1][2] but more recently both culture and culture-independent techniques have confirmed that human milk contains diverse communities of bacteria which are distinct from other microbial communities inhabiting the human body.[3][4][5]
Taxonomic composition overview
Bacteria commonly isolated in human milk samples include Bifidobacterium, Lactobacillus, Staphylococcus, Streptococcus, Bacteroides, Clostridium, Micrococcus, Enterococcus, and Escherichia[4][3][5]. Metagenome analyses of human milk find it is dominated by Staphylococcus, Pseudomonas, and Edwardsiella[6][7]. The human milk microbiome likely varies by population and between individual women,[8] however, a study based on a group of U.S. women observed the same 9 bacterial taxa in all samples from all of their participants, suggesting a common "core" of the milk microbiome, at least in that population.[9] Bacterial communities of human colostrum have been reported as being more diverse than those found in mature milk.[1][10]
Origins of establishment
While the origins of the human milk microbiome are not exactly known,[1] several hypotheses for its establishment have been proposed. Bacteria present in human milk may be derived from the surrounding breast skin[11][12] or the infant's oral cavity.[9][7][13][14] Retrograde backflow during nursing or suckling may also lead to bacterial establishment in the mammary duct,[15] supported by the observation that a certain degree of flowback has been shown to occur during nursing using infrared photography[16] Alternatively, bacteria may be translocated to the mammary duct from the maternal gastrointestinal tract via an entero-mammary pathway, facilitated by dendritic cells.[2][3][17]
Factors shaping the human milk microbiome
Geographic location
Both the taxonomic composition and diversity of bacteria present in human milk likely vary by maternal geographic location[1][8][9][18], however, more large-scale studies are needed to better understand variation between populations.[1]
Lactation stage
The human milk microbiome varies across lactation stage, with higher microbial diversity observed in colostrum than in mature milk.[1][10] Taxonomic composition of human milk also varies across the lactation period, initially dominated by Weisella, Leuconostoc, Staphylococcus, Streptococcus, and Lactococcus species[10], and later comprised primarily of Veillonella, Prevotella, Leptotrichia, Lactobacillus, Streptococcus, Bifidobacterium, and Enterococcus[10][19]
Human milk oligosaccharides
Human milk oligosaccharides, a primary component of human milk, are prebiotics which have been shown to promote growth of beneficial Bifidobacterium and Bacteroides species.[20][21][22]
Delivery mode
Mode of delivery may influence composition of the human milk microbiome, vaginal births being associated with high taxonomic diversity and high prevalence of Bifidobacterium and Lactobacillus, and the opposite trend being seen with Cesarean births,[10][19][23][24][25] however, no relationship between delivery mode and the maternal milk microbiome has also been observed.[26]
Gestational age
Women delivering term and preterm show differences in their milk microbiome composition, with mothers of term-births showing lower abundances of Enterococcus species and higher amounts of Bifidobacterium species in their milk than mothers of pre-term births.[19]
Maternal health
Maternal health status is associated with changes in the bacterial composition of milk. Higher maternal body mass index (BMI) and obesity are associated with changes in the levels of Bifidobacterium and Staphylococcus species and overall lower bacterial diversity.[10][27] Milk of women with celiac disease is observed to have reduced levels of Bacteroides and Bifidobacterium[28] Women who are HIV-positive show higher bacterial diversity and increased abundances of Lactobacillus in their milk than do non-HIV-positive women.[29] Mastitis has been linked to changes in human milk microbiota at the phylum level, lower microbial diversity, and decreased abundance of obligate anaerobic taxa.[30][31][7]
Antibiotic use
Maternal perinatal antibiotic use is associated with changes in the prevalence of Lactobacillus, Bifidobacterium, Staphylococcus, and Eubacterium in milk.[24][32][33]
Maternal diet
Few studies have been conducted examining the influence of maternal diet on the milk microbiome,[1] but diet is known to influence other aspects of milk composition, such as the lipid profile[34][35] which in turn could affect its microbial composition.[1] Variation in the fat and carbohydrate content of the maternal diet may influence the taxonomic composition of the milk microbiome.[36]
Social influences
Social network density of mother-infant dyads was found to be associated with increased bacterial diversity in the milk microbiome of mothers in the Central African Republic.[37]
Influences on infant health and development
Breastfeeding is thought to be an important driver of infant gut microbiome establishment.[38] The gut microbiome of breastfed infants is less diverse, contains higher amounts of Bifidobacterium and Lactobacillus species, and fewer potential pathogenic taxa than the gut microbiome of formula-fed infants.[39][40][41] Human milk bacteria may reduce risk of infection in breastfed infants by competitively excluding harmful bacteria,[42][43] and producing antimicrobial compounds which eliminate pathogenic strains,[44][45][46][42] Certain lactobacilli and bifidobacteria, the growth of which is stimulated by human milk oligosaccharides[47] contribute to healthy metabolic and immune-related functioning in the infant gut.[48][49][2][50]
Evolutionary implications
There is some indication of relationships between milk microbiota and other human milk components, including human milk oligosaccharides (HMOs), maternal cells, and nutrient profiles.[22][51] Specific bacterial genera have been shown to be associated with variation in levels of milk macronutrients such as lactose, proteins, and fats.[51] HMOs selectively facilitate growth of particular beneficial bacteria, notably Bifidobacterium species.[52][53] Furthermore, as bifidobacterial genomes are uniquely equipped to metabolize HMOs[54], which are otherwise indigestible by enzymes of the infant gut, some have suggested a coevolutionary dynamic between HMOs and certain bacteria common in both the milk and infant gastrointestinal microbiomes.[55][56] Furthermore, relative to other mammalian milks, primate milk, particularly human milk, appears to be unique with respect to the complexity and diversity of its oligosaccharide repertoire. Human milk is typified by greater overall HMO diversity and predominance of oligosaccharides known to promote growth of Bifidobacterium in the infant gut.[57] Milk microbiota are thought to play an essential role in programming the infant immune system, and tend to reduce the risk of adverse infant health outcomes.[50] Differences in milk oligosaccharides between humans and non-human primates could be indicative of variation in pathogen exposure associated with increased sociality and group sizes.[58] Together, these observations may indicate that milk microbial communities have coevolved with their human host.[56], supported by the expectation that microbes which promote host health facilitate their own transmission and proliferation[59]
Known comparisons to other mammalian milk microbiomes
Both human and macaque milks contains high abundances of Streptococcus and Lactobacillus bacteria, but differ in their respective relative abundances of these taxa.[60] Bacteria observed to be most common in healthy bovine milk include Ralstonia, Pseudomonas, Sphingomonas, Stenotrophomonas, Psychrobacter, Bradyrhizobium, Corynebacterium, Pelomonas, Staphylococcus, Fecalibacterium, Lachnospiraceae, Propionibacterium, Aeribacillus, Bacteroides, Staphyloccus, Streptococcus, Anaerococcus, Lactobacillus, Porphyromonas, Comamonas, Fusobacterium, and Enterococcus.[61][62][63][64]
See also
References
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