Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW (Open Access)

Prenatal establishment of the foal gut microbiota: a critique of the in utero colonisation hypothesis

Kirsty L. Mols https://orcid.org/0000-0002-5177-970X A C , Gry B. Boe-Hansen https://orcid.org/0000-0003-2453-1992 B , Deirdre Mikkelsen A , Wayne L. Bryden A and A. Judy Cawdell-Smith A
+ Author Affiliations
- Author Affiliations

A Equine Research Unit, School of Agriculture and Food Sciences, The University of Queensland, Gatton, Qld 4343, Australia.

B School of Veterinary Science, The University of Queensland, Gatton, Qld 4343, Australia.

C Corresponding author. Email: k.mols@uq.edu.au

Animal Production Science 60(18) 2080-2092 https://doi.org/10.1071/AN20010
Submitted: 7 January 2020  Accepted: 12 June 2020   Published: 23 November 2020

Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND

Abstract

Bacteria colonisation of the foal’s gastrointestinal tract (GIT) is a critical developmental stage, effecting subsequent immunological and health outcomes. It has long been thought that the equine fetus develops in a sterile intrauterine environment and GIT colonisation commences at birth. Research now suggests that bacteria isolated from amniotic fluid are the initial colonisers of the fetal GIT, and exposure to the dam’s microbiota and the external environment during birth provide supplementary colonisation. This in utero colonisation hypothesis has only recently been examined in the horse and microbiota were detected in the amniotic fluid and meconium of healthy equine pregnancies. This review highlights the possible colonisation routes of these bacteria into the fetal compartments and examines their likely origins from the existing maternal microbiome. However, the current data describing the amniotic microbiota of the horse are limited and there is a need for research to fill this gap. Understanding the significance of intrauterine microbes for foal GIT colonisation may provide strategies to improve neonatal health.

Keywords: amniotic fluid, gastrointestinal tract, meconium, sterile womb.


References

Aagaard K, Ma J, Antony K, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Science Translational Medicine 6, 1–11.
The placenta harbors a unique microbiome.Crossref | GoogleScholarGoogle Scholar |

Aagaard K, Ma J, Prince A, Chu D, Showalter L, Antony K, Versalovic J (2015) Association of preterm birth with alterations in the microbiome and linkage to host mtDNA variants. American Journal of Obstetrics and Gynecology 212, S10–S10.
Association of preterm birth with alterations in the microbiome and linkage to host mtDNA variants.Crossref | GoogleScholarGoogle Scholar |

Aatsinki A-K, Lahti L, Uusitupa H-M, Munukka E, Keskitalo A, Nolvi S, O’Mahony S, Pietilä S, Elo LL, Eerola E, Karlsson H, Karlsson L (2019) Gut microbiota composition is associated with temperament traits in infants. Brain, Behavior, and Immunity 80, 849–858.
Gut microbiota composition is associated with temperament traits in infants.Crossref | GoogleScholarGoogle Scholar | 31132457PubMed |

Alipour MJ, Jalanka J, Pessa-Morikawa T, Kokkonen T, Satokari R, Hynönen U, Iivanainen A, Niku M (2018) The composition of the perinatal intestinal microbiota in cattle. Scientific Reports 8, 1–14.
The composition of the perinatal intestinal microbiota in cattle.Crossref | GoogleScholarGoogle Scholar |

Ardissone AN, de la Cruz AG, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, Murgas-Torrazza R, Sharma R, Hudak ML, Triplett EW, Neu J (2014) Meconium microbiome analysis indentifies bacteria correlated with premature birth. PLoS One 9, 1–8.
Meconium microbiome analysis indentifies bacteria correlated with premature birth.Crossref | GoogleScholarGoogle Scholar |

Borre YE, O’keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF (2014) Microbiota and neurodevelopmental windows: implications for brain disorders. Trends in Molecular Medicine 20, 509–518.
Microbiota and neurodevelopmental windows: implications for brain disorders.Crossref | GoogleScholarGoogle Scholar | 24956966PubMed |

Burrage S (1927) Bacteria in the supposedly sterile meconium. Journal of Bacteriology 13, 47–48.

Cao B, Stout MJ, Lee I, Mysorekar IU (2014) Placental microbiome and its role in preterm birth. NeoReviews 15, e537–e545.
Placental microbiome and its role in preterm birth.Crossref | GoogleScholarGoogle Scholar | 25635174PubMed |

Cellini C, Xu J, Buchmiller TL (2006) Effect of esophageal ligation on small intestinal development in normal and growth-retarded fetal rabbits. Journal of Pediatric Gastroenterology and Nutrition 43, 291–298.
Effect of esophageal ligation on small intestinal development in normal and growth-retarded fetal rabbits.Crossref | GoogleScholarGoogle Scholar | 16954949PubMed |

Charbonneau MR, Blanton LV, DiGiulio DB, Relham DA, Lebrilla CB, Mills DA, Gordon JI (2016) A microbial perspective of human developmental biology. Nature 535, 48–55.
A microbial perspective of human developmental biology.Crossref | GoogleScholarGoogle Scholar | 27383979PubMed |

Chu D, Stewart C, Seferovic M, Suter M, Cox J, Vidaeff A, Aagard K (2017) Profiling of microbiota in second trimester amniotic fluid reveals a distinctive community present in the mid trimester and predictive of the placental microbiome at parturition. American Journal of Obstetrics and Gynecology 216, S18–S19.
Profiling of microbiota in second trimester amniotic fluid reveals a distinctive community present in the mid trimester and predictive of the placental microbiome at parturition.Crossref | GoogleScholarGoogle Scholar |

Collado MC, Rautava S, Isolari E, Salminen S (2016) Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Scientific Reports 6, 1–13.
Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid.Crossref | GoogleScholarGoogle Scholar |

Costa MC, Weese JS (2012) The equine intestinal microbiome. Animal Health Research Reviews 13, 121–128.
The equine intestinal microbiome.Crossref | GoogleScholarGoogle Scholar | 22626511PubMed |

Costa MC, Weese JS (2018) Understanding the intestinal microbiome in health and disease. The Veterinary Clinics of North America. Equine Practice 34, 1–12.
Understanding the intestinal microbiome in health and disease.Crossref | GoogleScholarGoogle Scholar | 29402480PubMed |

Costa MC, Stampfli HR, Allen-Vercoe E, Weese JS (2016) Development of the faecal microbiota in foals. Equine Veterinary Journal 48, 681–688.
Development of the faecal microbiota in foals.Crossref | GoogleScholarGoogle Scholar | 26518456PubMed |

De La Torre U, Henderson JD, Furtado KL, Pedroja M, Elenamarie O, Mora A, Pechanec MY, Maga EA, Mienaltowski IMJ (2019) Utilizing the fecal microbiota to understand foal gut transitions from birth to weaning. PLoS One 14, 1–18.
Utilizing the fecal microbiota to understand foal gut transitions from birth to weaning.Crossref | GoogleScholarGoogle Scholar |

Diel de Amorim M, Gartley CJ, Foster RA, Hill A, Scholtz EL, Hayes A, Chenier TS (2016) Comparison of clinical signs, endometrial culture, endometrial cytology, uterine low-volume lavage, and uterine biopsy and combinations in the diagnosis of equine endometritis. Journal of Equine Veterinary Science 44, 54–61.
Comparison of clinical signs, endometrial culture, endometrial cytology, uterine low-volume lavage, and uterine biopsy and combinations in the diagnosis of equine endometritis.Crossref | GoogleScholarGoogle Scholar |

Fardini Y, Chung P, Dumm R, Joshi N, Han YW (2010) Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infection and Immunity 78, 1789–1796.
Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection.Crossref | GoogleScholarGoogle Scholar | 20123706PubMed |

Foote AK, Ricketts SW, Whitwell KE (2012) A racing start in life? The hurdles of equine feto-placental pathology. Equine Veterinary Journal 44, 120–129.
A racing start in life? The hurdles of equine feto-placental pathology.Crossref | GoogleScholarGoogle Scholar |

Foti M, Ricciardi-Castagnoli P (2005) Antigen sampling by mucosal dendritic cells. Trends in Molecular Medicine 11, 394–396.
Antigen sampling by mucosal dendritic cells.Crossref | GoogleScholarGoogle Scholar | 16087403PubMed |

Fraga M, Perelmuter K, Delucchi L, Cidade E, Zunino P (2008) Vaginal lactic acid bacteria in the mare: evaluation of the probiotic potential of native Lactobacillus spp. and Enterococcus spp. strains. Antonie van Leeuwenhoek 93, 71–78.
Vaginal lactic acid bacteria in the mare: evaluation of the probiotic potential of native Lactobacillus spp. and Enterococcus spp. strains.Crossref | GoogleScholarGoogle Scholar | 17588124PubMed |

Franciolli ALR, Cordeiro BM, da Fonseca ET, Rodrigues MN, Sarmento CAP, Ambrosio CE, de Carvalho AF, Miglino MA, Silva LA (2011) Characteristics of the equine embryo and fetus from days 15 to 107 of pregnancy. Theriogenology 76, 819–832.
Characteristics of the equine embryo and fetus from days 15 to 107 of pregnancy.Crossref | GoogleScholarGoogle Scholar |

Gaivão MMF, Rambags BPB, Stout TAE (2014) Gastrulation and the establishment of the three germ layers in the early horse conceptus. Theriogenology 82, 354–365.
Gastrulation and the establishment of the three germ layers in the early horse conceptus.Crossref | GoogleScholarGoogle Scholar |

Gao W, Chan Y, You M, Lacap-Bugler DC, Leung WK, Watt RM (2016) In-depth snapshot of the equine subgingival microbiome. Microbial Pathogenesis 94, 76–89.
In-depth snapshot of the equine subgingival microbiome.Crossref | GoogleScholarGoogle Scholar | 26550763PubMed |

Hall IC, O’Toole E (1934) Bacterial flora of first specimens of meconium passed by fifty new-born infants. American Journal of Diseases of Children 47, 1279–1285.

Han YW, Fardini Y, Chen C, Iacampo KH, Peraino VA, Shamonki JM, Redline RW (2010) Term stillbirth caused by oral Fusobacterium nucleatum. Obstetrics and Gynecology 115, 442–445.
Term stillbirth caused by oral Fusobacterium nucleatum.Crossref | GoogleScholarGoogle Scholar | 20093874PubMed |

Heil BA, Thompson SK, Davolli GM, King G, Sones JL (2018) Metagenetic characterization of the resident equine uterine microbiome using multiple techniques. Journal of Equine Veterinary Science 66, 111
Metagenetic characterization of the resident equine uterine microbiome using multiple techniques.Crossref | GoogleScholarGoogle Scholar |

Hemberg E, Einarsson S, Kútvölgyi G, Lundeheim N, Bagge E, Båverud V, Jones B, Morrell JM (2015) Occurrence of bacteria and polymorphonuclear leukocytes in fetal compartments at parturition; relationships with foal and mare health in the peripartum period. Theriogenology 84, 163–169.
Occurrence of bacteria and polymorphonuclear leukocytes in fetal compartments at parturition; relationships with foal and mare health in the peripartum period.Crossref | GoogleScholarGoogle Scholar | 25850610PubMed |

Hitti J, Hillier SL, Agnew KJ, Krohn MA, Reisner DP, Eschenbach DA (2001) Vaginal indicators of amniotic fluid infection in preterm labor. Obstetrics and Gynecology 97, 211–219.

Hong CB, Donahue JM, Giles RCJ, Petrites-Murphy MB, Poonacha KB, Roberts AW, Smith BJ, Tramontin RR, Tuttle PA, Swerczek TW (1993) Equine abortion and stillbirth in central Kentucky during 1988 and 1989 foaling seasons. Journal of Veterinary Diagnostic Investigation 5, 560–566.
Equine abortion and stillbirth in central Kentucky during 1988 and 1989 foaling seasons.Crossref | GoogleScholarGoogle Scholar | 8286455PubMed |

Hoyles L, Ortman K, Cardew S, Foster G, Rogerson F, Falsen E (2013) Corynebacterium uterequi sp. nov., a non-lipophilic bacterium isolated from urogenital samples from horses. Veterinary Microbiology 165, 469–474.
Corynebacterium uterequi sp. nov., a non-lipophilic bacterium isolated from urogenital samples from horses.Crossref | GoogleScholarGoogle Scholar | 23618836PubMed |

Jacquay E, Zeglin L, Lillich J, Jones E, Kouba J (2018) Characterization of foal fecal microbiome from birth to weaning and the relationship to mare milk and mare feces. Journal of Animal Science 96, 33
Characterization of foal fecal microbiome from birth to weaning and the relationship to mare milk and mare feces.Crossref | GoogleScholarGoogle Scholar |

Jeon SJ, Cunha F, Vieira-Neto A, Bicalho RC, Lima S, Bicalho ML, Galvão KN (2017) Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome 5, 1–13.
Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows.Crossref | GoogleScholarGoogle Scholar |

Jiménez E, Marín ML, Martín R, Odriozola JM, Olivares M, Xaus J, Fernández L, Rodríguez JM (2008) Is meconium from health newborns actually sterile? Research in Microbiology 159, 187–193.
Is meconium from health newborns actually sterile?Crossref | GoogleScholarGoogle Scholar | 18281199PubMed |

Kennedy R, Lappin DF, Dixon PM, Buijs MJ, Zaura WC, O’Donnell L, Bennett D, Brandt BW, Riggio MP (2016) The microbiome associated with equine periodontitis and oral health. Veterinary Research 47, 1–9.
The microbiome associated with equine periodontitis and oral health.Crossref | GoogleScholarGoogle Scholar |

Kraimi N, Dawkins M, Gebhardt-Henrich SG, Velge P, Rychlik I, Volf J, Creach P, Smith A, Colles F, Leterrier C (2019) Influence of the microbiota–gut–brain axis on behavior and welfare in farm animals: a review. Physiology and Behavior 210, 1–12.
Influence of the microbiota–gut–brain axis on behavior and welfare in farm animals: a review.Crossref | GoogleScholarGoogle Scholar |

Kuhl J, Winterhoff N, Wulf M, Schweigert FJ, Schwendenwein I, Bruckmaier RM, Aurich JE, Kutzer P, Aurich C (2011) Changes in faecal bacteria and metabolic parameters in foals during the first six weeks of life. Veterinary Microbiology 151, 321–328.
Changes in faecal bacteria and metabolic parameters in foals during the first six weeks of life.Crossref | GoogleScholarGoogle Scholar | 21511405PubMed |

Layman QD, Rezabek GB, Ramachandran A, Love BC, Confer AW (2014) A retrospective study of equine actinobacillosis cases: 1999–2011. Journal of Veterinary Diagnostic Investigation 26, 365–375.
A retrospective study of equine actinobacillosis cases: 1999–2011.Crossref | GoogleScholarGoogle Scholar | 24742921PubMed |

Martin EJ, Reed KJ, Kunz IGZ, Coleman RJ, Coleman SJ (2017) Normal variation and changes over time in the equine intestinal microbiome. Journal of Equine Veterinary Science 52, 60
Normal variation and changes over time in the equine intestinal microbiome.Crossref | GoogleScholarGoogle Scholar |

Mesa F, Pozo E, Blanc V, Puertas A, Bravo M, O’Valle F (2013) Are periodontal bacterial profiles and placental inflammatory infiltrate in pregnancy related to birth outcomes? Journal of Periodontology 84, 1327–1336.
Are periodontal bacterial profiles and placental inflammatory infiltrate in pregnancy related to birth outcomes?Crossref | GoogleScholarGoogle Scholar | 23121458PubMed |

Meyer W, Kacza J, Schnapper A, Verspohl J, Hornickel I, Seeger J (2010) A first report on the microbial colonisation of the equine oesophagus. Annals of Anatomy 192, 42–51.
A first report on the microbial colonisation of the equine oesophagus.Crossref | GoogleScholarGoogle Scholar | 19942420PubMed |

Moreno I, Franasiak JM (2017) Endometrial microbiota: new player in town. Fertility and Sterility 108, 32–39.
Endometrial microbiota: new player in town.Crossref | GoogleScholarGoogle Scholar | 28602480PubMed |

Mulvihill SJ, Stone MM, Fonkalsrud EW, Debas HT (1986) Trophic effect of amniotic fluid on fetal gastrointestinal development. The Journal of Surgical Research 40, 291–296.
Trophic effect of amniotic fluid on fetal gastrointestinal development.Crossref | GoogleScholarGoogle Scholar | 3702386PubMed |

Nicoletti C, Regoli M, Bertelli E (2009) Dendritic cells in the gut: to sample and to exclude? Mucosal Immunology 2, 462
Dendritic cells in the gut: to sample and to exclude?Crossref | GoogleScholarGoogle Scholar | 19687786PubMed |

Panelli S, Schneider L, Bandi C, Zuccotti GV, D’Auria E (2018) Is there life in the meconium? A challenging, burning question. Pharmacological Research 137, 148–149.
Is there life in the meconium? A challenging, burning question.Crossref | GoogleScholarGoogle Scholar | 30296570PubMed |

Pararas MV, Skevaki CL, Kafetzis DA (2006) Preterm birth due to maternal infection: causative pathogens and modes of prevention. European Journal of Clinical Microbiology & Infectious Diseases 25, 562–569.
Preterm birth due to maternal infection: causative pathogens and modes of prevention.Crossref | GoogleScholarGoogle Scholar |

Pelzer E, Gomez-Arango LF, Barrett HL, Nitert MD (2017) Review: maternal health and the placental microbiome. Placenta 54, 30–37.
Review: maternal health and the placental microbiome.Crossref | GoogleScholarGoogle Scholar | 28034467PubMed |

Perez-Muñoz ME, Arrieta M, Ramer-Tait AE, Walter J (2017) A critical assessment of the ‘sterile womb’ and ‘in utero colonization’ hypotheses: implications for research on the pioneer infant microbiome Microbiome 5, 1–19.
A critical assessment of the ‘sterile womb’ and ‘in utero colonization’ hypotheses: implications for research on the pioneer infant microbiomeCrossref | GoogleScholarGoogle Scholar |

Platt H (1984) Growth of the equine foetus. Equine Veterinary Journal 16, 247–252.
Growth of the equine foetus.Crossref | GoogleScholarGoogle Scholar | 6383808PubMed |

Prince A, Chu D, Seferovic M, Antony K, Ma J, Aagaard K (2015) The perinatal microbiome and pregnancy: moving beyond the vaginal microbiome. Cold Spring Harbor Perspectives in Medicine 5, 1–24.
The perinatal microbiome and pregnancy: moving beyond the vaginal microbiome.Crossref | GoogleScholarGoogle Scholar |

Pugh G (2018) ‘The role of microbial diversity in female reproductive health: an analysis of the microbiome’s influence on pregnancy outcomes in postparturient mares.’ (ProQuest Dissertations Publishing, Michigan, USA)

Quercia S, Freccero F, Castagnetti C, Soverini M, Turroni S, Biagi E, Rampelli S, Lanci A, Mariella J, Chinellato E, Brigidi P, Candela M (2019) Early colonisation and temporal dynamics of the gut microbial ecosystem in Standardbred foals. Equine Veterinary Journal 51, 231–237.
Early colonisation and temporal dynamics of the gut microbial ecosystem in Standardbred foals.Crossref | GoogleScholarGoogle Scholar | 29931762PubMed |

Rehbinder EM, Lodrup Carlsen KC, Staff AC, Angel IL, Landro L, Hilde K, Gaustad P, Rudi K (2018) Is amniotic fluid of women with uncomplicted term pregnancices free of bacteria? American Journal of Obstetrics and Gynecology 219, 289.e1–289.e12.
Is amniotic fluid of women with uncomplicted term pregnancices free of bacteria?Crossref | GoogleScholarGoogle Scholar |

Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl J, Ricciardi-Castagnoli P (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunology 2, 361–367.
Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria.Crossref | GoogleScholarGoogle Scholar | 11276208PubMed |

Rose BV, Firth M, Morris B, Roach JM, Wathes DC, Verheyen KLP, de Mestre AM (2018) Descriptive study of current therapeutic practises, clinical reproductive findings and incidence of pregnancy loss in intensively managed thoroughbred mares. Animal Reproduction Science 188, 74–84.
Descriptive study of current therapeutic practises, clinical reproductive findings and incidence of pregnancy loss in intensively managed thoroughbred mares.Crossref | GoogleScholarGoogle Scholar | 29146097PubMed |

Sangild PT, Schmidt M, Elnif J, Björnvad CR, Weström BR, Buddington RK (2002) Prenatal develoment of gastrointestinal function in the pig and the effects of fetal esophageal obstruction. Pediatric Research 52, 416–424.
Prenatal develoment of gastrointestinal function in the pig and the effects of fetal esophageal obstruction.Crossref | GoogleScholarGoogle Scholar | 12193678PubMed |

Schmidt AR, Williams MA, Carleton CL, Darien BJ, Derksen FJ (1991) Evaluation of transabdominal ultrasound-guided amniocentesis in the late gestational mare. Equine Veterinary Journal 23, 261–265.
Evaluation of transabdominal ultrasound-guided amniocentesis in the late gestational mare.Crossref | GoogleScholarGoogle Scholar | 1915224PubMed |

Schoster A (2018) Probiotic use in equine gastrointestinal disease. The Veterinary Clinics of North America. Equine Practice 34, 13–24.
Probiotic use in equine gastrointestinal disease.Crossref | GoogleScholarGoogle Scholar | 29402478PubMed |

Schoster A, Arroyo LG, Staempfli HR, Weese JS (2013) Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism. BMC Research Notes 6, 1–9.
Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism.Crossref | GoogleScholarGoogle Scholar |

Stinson LF, Keelan JA, Payne MS (2018) Comparison of meconium DNA extraction methods for use in microbiome studies. Frontiers in Microbiology 9, 1–14.
Comparison of meconium DNA extraction methods for use in microbiome studies.Crossref | GoogleScholarGoogle Scholar |

Torrazza RM, Neu J (2011) The developing intestinal microbiome and its relationship to health and disease in the neonate. Journal of Perinatology 31, S29–S34.
The developing intestinal microbiome and its relationship to health and disease in the neonate.Crossref | GoogleScholarGoogle Scholar |

Trahair JF, Sangild PT (2000) Fetal organ growth in response to oesophageal infusion of amniotic fluid, colostrum, milk or gastrin-releasing peptide: a study in fetal sheep. Reproduction, Fertility and Development 12, 87–95.
Fetal organ growth in response to oesophageal infusion of amniotic fluid, colostrum, milk or gastrin-releasing peptide: a study in fetal sheep.Crossref | GoogleScholarGoogle Scholar |

Wallace JG, Gohir W, Sloboda DM (2016) The impact of early life gut colonisation on metabolic and obesogenic outcomes: what have animal models shown us? Journal of Developmental Origins of Health and Disease 7, 15–24.
The impact of early life gut colonisation on metabolic and obesogenic outcomes: what have animal models shown us?Crossref | GoogleScholarGoogle Scholar | 26399435PubMed |

Wassenaar TM, Panigrahi P (2014) Is a foetus developing in a sterile environment? Letters in Applied Microbiology 59, 572–579.
Is a foetus developing in a sterile environment?Crossref | GoogleScholarGoogle Scholar | 25273890PubMed |

Whitwell KE, Jeffcott LB (1975) Morphological studies on the fetal membranes of the normal singleton foal at term. Research in Veterinary Science 19, 44–55.
Morphological studies on the fetal membranes of the normal singleton foal at term.Crossref | GoogleScholarGoogle Scholar | 1153897PubMed |

Willing B, Vörös A, Roos S, Jones C, Jansson A, Lindberg JE (2009) Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training. Equine Veterinary Journal 41, 908–914.
Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training.Crossref | GoogleScholarGoogle Scholar | 20383990PubMed |

Wohlfender FD, Barrelet FE, Doherr MG, Straub R, Meier HP (2009) Diseases in neonatal foals. Part 1: the 30-day incidence of disease and the effect of prophylactic antimicrobial drug treatment during the first three days post partum Equine Veterinary Journal 41, 179–185.

Woźniak MK, Jaszczak E, Wiergowski M, Polkowska Ż, Namieśnik J, Biziuk M (2018) Meconium analysis as a promising diagnostic tool for monitoring fetal exposure to toxic substances: recent trends and perspectives. Trends in Analytical Chemistry 109, 124–141.

Zhuang L, Chen H, Zhang S, Zhuang J, Li Q, Feng Z (2019) Intestinal microbiota in early life and its implications on childhood health. Genomics, Proteomics and Bioinformatics 17, 13–25.
Intestinal microbiota in early life and its implications on childhood health.Crossref | GoogleScholarGoogle Scholar | 30986482PubMed |