Factors influencing the composition and balance of foals’ microbiota
DOI:
https://doi.org/10.33448/rsd-v10i9.17778Keywords:
Immune system; Gut microbiota; gut microbiota; Intestinal flora; intestinal flora; Equine microbiota. ; equine microbiotaAbstract
Horses are extremely dependent on the correct functioning of the digestive system for energy production and the performance of their physiological functions. The intestinal microbiota plays a key role in maintaining health, being related to the modulation of the immune system, protection against pathogenic microorganisms and also for obtaining nutrients. Due to the importance of the microbiota in maintaining health from the beginning of life, this review aims to address the early composition, development and factors that influence the intestinal microbiota in foals. A qualitative review was carried out in the main research databases. Data referring to the early microbial colonization suggest that it occurs since intrauterine life, despite the fact that at birth, the foals acquire a large part of the microorganisms that will form its microbiota. The main phyla involved in this process are Proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes, which are aquired from a combination of bacteria present in the feces, vagina and other maternal environments. From birth until the first weeks of life, the microbiota gradually changes due to several factors, which include the composition of food, coprophagy, exposure to different environments and medications. The foal's microbiota becomes more stable in the first and second months of life. It is suggested that changes in the composition (dysbiosis) and diversity of the different phyla are a risk factor for the development of diseases, since the microbiota directly influences the immune system. From advances in sequencing technologies it was possible to investigate the components and factors associated with early colonization of microbiota in horses as well as factors related to the development of dysbiosis and disease. Nevertheless, many facts are still unclear and should be adressed in the future.
References
Aagaard, K., Ganu, R., Ma, J., Hu, M., Miller, L., Jobe, A., Kallapur, S. & Chougnet, C. (2013). Intraamniotic interleukin-1 (IL1β) induces histologic chorioamnionitis and alters the microbiome in a primate model of inflammatory preterm birth. American Journal of Obstetrics and Gynecology 208: S218.
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.
Alarcón, P., González, M. & Castro, É. (2016). Rol de la microbiota gastrointestinal en la regulación de la respuesta inmune. Revista médica de Chile, 144(7), 910-916.
Backhed, F. R., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F. & Gordon, J. I. (2004). The gut microbiota as an environmental factor tha regulates fat storage. Proceedings of the National Academy of Sciences, 101(44):15718-23.
Bäckhed, F. R., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kobatcheva-Datchary, P., Li, Y. Xia, Y., Xie, H., Zhong, H., Tanweer, K., Zhang, J., Li, J., Xiao, L., Al-Aama, J., Zhang, D., Lee, Y. S., Kotowska, D., Colding, C., Tremarolli, V., Yin, Y., Bergman, S., Xu, X., Madsen, L., Kristiansen, K., Dahlgren, J. & Wang, J. (2015).. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 17(6): 852.
Bordin, A. I., Suchodolski, J. S., Markel, M. E., Weaver, K. B., Steiner, J. M., Dowd, S. E., Pillai, S. & Cohen, N. D. (2013). Effects of Administration of Live or Inactivated Virulent Rhodococccus equi and Age on the Fecal Microbiome of Neonatal Foals. Plos One. 8(6):e66640.
Costa, M. C., Stämpfli, H. R., Allen‐Vercoe, E. & Weese, J. S. (2016). Development of the faecal microbiota in foals. Equine veterinary journal, 48(6), 681-688.
Costa, M. C., Stämpfli, H. R., Arroyo, L. G., Allen- Vercoe, E., Gomes, R. G. & Weese, J. S. (2015). Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs. BMC Veterinary Research, 11:19.
Costa, M. C. & Weese, J. S. (2012). The equine intestinal microbiome. Animal Health Research Reviews, 13(1); 121–128.
Cobb, C. M., Kelly, P. J., Williams, K. B., Babbar, S., Angolkar, M. & Derman, R. J. (2017). The oral microbiome and adverse pregnancy outcomes. International Journal of Women's Health, 9: 551–559.
Crowell-Davis, S. L., Caudle, A. B. (1989). Coprophagy by foals: recognition of maternal feces. Applied Animal Behaviour Science. 24(3): 267-272.
Crowell-Davis, S. L. & Houpt, K. A. (1985). Coprophagy by foals: effect of age and possible functions. Equine Veterinary Journal. 17: 17–19.
De La Torre, U., Henderson, J. D., Furtado, K. L., Pedroja, M., Elenamarie, O., Mora, A., Pechanec, M. Y., Maga, E. A & Mienaltowski, M. J. (2019). Utilizing the fecal microbiota to understand foal gut transitions from birth to weaning. Plos One, 14(4): e0216211.
Earing, J. E., Durig, A. C., Gellin, G. L., Lawrence, L. M. & Flythe, M. D. (2012). Bacterial Colonization of the Equine Gut; Comparison of Mare and Foal Pairs by PCR-DGGE*. Advances in Microbiology, 2: 79-86.
Fanaro, S., Chierici, R., Guerrini, P., & Vigi, V. (2003). Intestinal microflora in early infancy: composition and development. Acta paediatrica, 92, 48-55.
Faubladier, C., Julliand, V., Danel, J., Philippeau, C. (2013). Bacterial carbohydrate-degrading capacity in foal faeces: changes from birth to pre-weaning and the impact of maternal supplementation with fermented feed products. British Journal of Nutrition, 110: 1040–1052
Fernandes, K. A., Kittelmann, S., Rogers, C. W., Gee E. K, Bolwell, C. F., Bermingham E. N. & Thomas, D. G. (2014). Faecal Microbiota of Forage-Fed Horses in New Zealand and the Population Dynamics of Microbial Communities following Dietary Change. PLoS ONE, 9(11): e112846.
Flemer, B., Gaci, N., Borrel, G., Sanderson, I. R., Chaudhary, P. P., Tottey, W., O’Toole, P. W. & Brugère, J-F. (2017). Fecal microbiota variation across the lifespan of the healthy laboratory rat. Gut Microbes, 8(5):428-439.
Garber, A., Hastie, P., Murray, J-A. (2020). Factors Influencing Equine Gut Microbiota: Current Knowledge. Journal of Equine veterinary Science. 88: 102943.
Giguère, S. & Polkes, A. C. (2005). Immunologic Disorders in Neonatal Foals. Veterinary Clinics: Equine Practice, 21: 241–272.
Gosalbes, M. J., Llop, S., Vallès, Y., Moya, A., Ballester, F. & Francino M. P. (2013). Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clinical & Experimental Allergy, (43): 198–211.
Gronlund, M. M., Salminen, S., Mykkanen, H., Kero, P., Lehtonen, O. P. Development of intestinal bacterial enzymes in infants- relationship tom ode of delivery and type of feeding. APMIS, 107(7):655-60.
Gustafsson, A. (2004). Antibiotic Associated Diarrhea in Horses, with special reference to Clostridium difficile. Doctoral thesis. Swedish University of Agricultural Sciences, Uppsala.
Harlow, B. E., Lawrence, L. M. & Flythe, M. D. (2013). Diarrhea-associated pathogens, lactobacilli and cellulolytic bacteria in equine feces: responses to antibiotic challenge. Veterinary Microbiology. 166, 225-232.
Hemberg, E., Einarsson, S., Kútvölgyi, G., Lundeheim, N., Bagge, E., Båverud, V., Jones, B. & Morrell, J. M. (2015). Occurrence of bacteria and polymorphonuclear leukocytes in fetal compartments at parturition; relationships with foal and mare health in the peripartum period. Theriogenology, 84(1): 163-169.
Husso, A., Jalanka, J., Alipour, M. J., Huhti, P., Kareskoski, M., Pessa-Morikawa, T., Livanainen A & Niku, M. (2020). The composition of the perinatal intestinal microbiota in horse. Scientific Reports, 10(1), 1-12.
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(2):33.
Jeffcott, L. B. (1975). The transfer of passive immunity to the foal and its relation to immune status after birth. Journal of reproduction and fertility, 23(23):727-33.
Johnston, R. H., Kamstra, L. D. & Kohler, P. H. (1970). Mares’ Milk Composition as Related to “Foal Heat” Scours. Journal of Animal Science, 31(3), 549–553.
Kuhl, J., Winterhoff, N., Wulf, M., Schweigert, F. J., Schwendenwein, I., Bruckmaie,r R. M., Aurich, J., Kutzer, P. & Aurich, C. (2011). Changes in faecal bacteria and metabolic parameters in foals during the first six weeks of life. Veterinary Microbiology, 151(3-4): 321-328.
Lindenberg, F., Krych, L., Kot, W., Fielden, J., Frøkiær, H., van Galen, G., Nielsen, D. S. & Hansen, A.K. (2019). Development of the equine gut microbiota. Scientific reports, 9(1), 1-9.
Liu, Y., Bailey, K. E., Dyall- Smith, M., Marenda, M. S., Hardefeldt, L. Y., Browning, G. F., Gilkerson, J. R. & Billman-Jacobe, H. Faecal microbiota and antimicrobial resistance gene profiles of healthy foals (2020). Equine Veterinary Journal, 00:1–11.
Magdesian, K. G. (2015). Neonatal foal diarrhea. Veterinary Clinics: Equine Practice, 21, 295–312
Mols, K. L., Boe-Hansen, G. B., Mikkelsen, D., Bryden, W. L., Cawdell- Smith, A. J. (2020). Prenatal establishment of the foal gut microbiota: a critique of the in utero colonisation hypothesis. Animal Production Science, 60: 2080–2092.
Moreau, M. M., Eades, S. C., Reinemeyer, C. R., Fugaro, M. N. and Onishi, J. C. (2014). Illumina sequencing of the V4 hypervariable region 16S rRNA gene reveals extensive changes in bacterial communities in the cecum following carbohydrate oral infusion and development of early-stage acute laminitis in the horse. Veterinary Microbiology, 168, 436-441.
Pereira, A. S., Shitsuka, D. M., Parreira, F. J. & Shutsuka, R. (2018). Metodologia da pesquisa científica, 1º Edição UBA/NTE/UFSM, Universidade Federal de Santa Maria.
Prince, A. L., Chu, D. M., Seferovic, D. M., Antony, K. M., Ma, J. & Aagaard, K. M. (2015). The perinatal microbiome and pregnancy: Moving beyond the vaginal microbiome. 5(6): a023051.
Purchiaroni, F., Tortora, A., Gabrielli, M., Gabrielli, M., Bertucci, F., Gigante, G., Ianiro, G., Ojetti, V., Scarpellini, E. & Gasbarrin, A. (2013). The role of intestinal microbiota and the immune system. European Review for medical and Pharmacological Sciences, 17: 323-333.
Pyles, M. B., Hayes, S., Crum, A., Kunes, M., Radomski, E., Flythe, M. & Lawrence, L. (2020). Detecting coprophagy in foals and its relationship with foal gut helth. Journal of Animal Science, 98(4): 91–92.
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, 1(2):231-237.
Russell, S. L., Gold, M. J., Willing, B. P., Thorson, L., McNagny, K. M. and Finlay, B. B. (2013). Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes, 4: 158-164.
Saad, S. M. I. (2006). Probióticos e prebióticos: o estado da arte. Revista Brasileira de Ciências Farmacêuticas, 42(1), 1-16.
Schoster, A., Staempfli, H. R., Guardabassi, L. G., Jalali, M. & Weese, J. S. (2017). Comparison of the fecal bacterial microbiota of healthy and diarrheic foals at two and four weeks of life. BMC Veterinary Research, 13: 144.
Steel, J. H., Malatos, S., Kennea, N., Edwards, A. D., Miles, L., Duggan, P., Reynolds, P. R., Feldman, R. G. & Sullivan, M. H. F. (2005). Bacteria and Inflammatory Cells in Fetal Membranes Do Not Always Cause Preterm Labor. Pediatric Research, 57(3): 404–411.
Steelman, S. M., Chowdharu, B. P., Dowd, S., Suchodolski, J. & Janecka, J. (2012). Pyrosequencing of 16S rRNA genes in fecal samples reveals high diversity of hindgut microflora in horses and potential links to chronic laminitis, BMC Veterinary Research, 8:231.
Taschuk, R. & Griebel, P. J. (2012). Commensal microbiome effects on mucosal immune system development in the ruminant gastrointestinal tract. Animal Health Research Reviews, 13(1); 129–141.
Tavanner, M. K., McDonnell, S. M. & Biddle, A. S. (2020). Development of the equine hindgut microbiome in semi-feral and domestic conventionally-managed foals. Animal Microbiome, 2:43.
Toh, M. C. & Allen-Vercoe E. (2015). The human gut microbiota with reference to autism spectrum disorder: considering the whole as more than a sum of its parts. Microbial Ecology in Health and Disease, 26:26309.
Tonini, I. G. O., Vaz, D. S. S. & Mazur, C. E. (2020). Gut-brain axis: relationship between intestinal microbiota and mental disorders. Research, Society and Development, 9(7), e499974303.
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., Egholm, M., Henrissat, B., Heath, A. C., Knight, R. and Gordon, J. I. (2009) A core gut microbiome in obese and lean twins. Nature, 457, 480-484.
Weese, J. S., Holcombe, S. J., Embertson R. M., Kurtz, K. A., Roessner, H. A., Jalali, M. & Wismer, S. E. (2015). Changes in the faecal microbiota of mares precede the development of post partum colic. Equine Veterinary Journal, 47: 641–649.
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Copyright (c) 2021 Mariana Andrade Mousquer; Tatiane Leite Almeida; Rafaela Pinto de Souza; Vitória Müller; Eliza Moreira Piemolini; Bruna da Rosa Curcio; Carlos Eduardo Wayne Nogueira
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