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Microbial colonization of the gastrointestinal tract of dairy calves – a review of its importance and relationship to health and performance

Published online by Cambridge University Press:  16 June 2021

Gercino Ferreira Virgínio Júnior Open the ORCID record for Gercino Ferreira Virgínio Júnior [Opens in a new window]  and
Carla Maris Machado Bittar
Gercino Ferreira Virgínio Júnior*
Affiliation:
Department of Animal Science, Luiz de Queiroz College of Agriculture, University of Sao Paulo, Piracicaba, SP, Brazil
Carla Maris Machado Bittar
Affiliation:
Department of Animal Science, Luiz de Queiroz College of Agriculture, University of Sao Paulo, Piracicaba, SP, Brazil
*
Author for correspondence: Gercino Ferreira Virgínio Júnior, Department of Animal Science, Luiz de Queiroz College of Agriculture, University of Sao Paulo, Piracicaba, SP, Brazil. E-mail: [email protected]
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Abstract

This review aims to explain how microbial colonization of the gastrointestinal tract (GIT) in young dairy calves is related to health and, consequently, to the performance of these animals. The review addresses everything from the fundamental aspects of microbial colonization to the current understanding about the microbiota manipulation to improve performance in adult animals. The ruminal microbiota is the most studied, mainly due to the high interest in the fermentative aspects, the production of short-chain fatty acids, and microbial proteins, and its effects on animal production. However, in recent years, the intestinal microbiota has gained space between studies, mainly due to the relationship to the host health and how it affects performance. Understanding how the GIT's microbiota looks like and how it is colonized may allow future studies to predict the best timing for dietary interventions as a way to manipulate it and, consequently, improve the health and performance of young ruminants.

Keywords

Calf nutritiongut healthmicrobiota
Type
Review Article
Information
Animal Health Research Reviews , Volume 22 , Issue 2 , December 2021 , pp. 97 - 108
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abecia, L, Martín-García, AI, Martínez, G, Newbold, CJ and Yáñez-Ruiz, DR (2013) Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning1. Journal of Animal Science 91, 4832–4840.CrossRefGoogle Scholar
Abecia, L, Ramos-Morales, E, Martínez-Fernandez, G, Arco, A, Martín-García, AI, Newbold, CJ and Yáñez-Ruiz, DR (2014) Feeding management in early life influences microbial colonisation and fermentation in the rumen of newborn goat kids. Animal Production Science 54, 1449.CrossRefGoogle Scholar
Abecia, L, Martínez-Fernandez, G, Waddams, K, Martín-García, AI, Pinloche, E, Creevey, CJ, Denman, SE, Newbold, CJ and Yáñez-Ruiz, DR (2018) Analysis of the rumen microbiome and metabolome to study the effect of an antimethanogenic treatment applied in early life of kid goats. Frontiers in Microbiology 9, 1–14.CrossRefGoogle Scholar
Adlerberth, I and Wold, AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatrica 98, 229–238.CrossRefGoogle ScholarPubMed
Alipour, MJ, Jalanka, J, Pessa-Morikawa, T, Kokkonen, T, Satokari, R, Hynönen, U, Iivanainen, A and Niku, M (2018) The composition of the perinatal intestinal microbiota in cattle. Scientific Reports 8, 10437.CrossRefGoogle ScholarPubMed
Allaband, C, McDonald, D, Vázquez-Baeza, Y, Minich, JJ, Tripathi, A, Brenner, DA, Loomba, R, Smarr, L, Sandborn, WJ, Schnabl, B, Dorrestein, P, Zarrinpar, A and Knight, R (2019) Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clinical Gastroenterology and Hepatology 17, 218–230.CrossRefGoogle ScholarPubMed
Araujo, G, Yunta, C, Terré, M, Mereu, A, Ipharraguerre, I and Bach, A (2015) Intestinal permeability and incidence of diarrhea in newborn calves. Journal of Dairy Science 98, 7309–7317.CrossRefGoogle ScholarPubMed
Badman, J, Daly, K, Kelly, J, Moran, AW, Cameron, J, Watson, I, Newbold, J and Shirazi-Beechey, SP (2019) The effect of milk replacer composition on the intestinal microbiota of pre-ruminant dairy calves. Frontiers in Veterinary Science 6, 1–9.CrossRefGoogle ScholarPubMed
Baldwin, RL, McLeod, KR, Klotz, JL and Heitmann, RN (2004) Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. Journal of Dairy Science 87, E55–E65.CrossRefGoogle Scholar
Ballou, MA (2011) Case study: effects of a blend of prebiotics, probiotics, and hyperimmune dried egg protein on the performance, health, and innate immune responses of Holstein calves. The Professional Animal Scientist 27, 262–268.CrossRefGoogle ScholarPubMed
Barden, M, Richards-Rios, P, Ganda, E, Lenzi, L, Eccles, R, Neary, J, Oultram, J and Oikonomou, G (2020) Maternal influences on oral and faecal microbiota maturation in neonatal calves in beef and dairy production systems. Animal Microbiome 2, 31.CrossRefGoogle ScholarPubMed
Bartels, CJM, Holzhauer, M, Jorritsma, R, Swart, WAJM and Lam, TJGM (2010) Prevalence, prediction and risk factors of enteropathogens in normal and non-normal faeces of young Dutch dairy calves. Preventive Veterinary Medicine 93, 162–169.CrossRefGoogle ScholarPubMed
Bezirtzoglou, E (1997) The intestinal Microflora during the first weeks of life. Anaerobe 3, 173–177.CrossRefGoogle ScholarPubMed
Bi, Y, Cox, MS, Zhang, F, Suen, G, Zhang, N, Tu, Y and Diao, Q (2019) Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs. Environmental Microbiology 21, 2333–2346.CrossRefGoogle ScholarPubMed
Bi, Y, Tu, Y, Zhang, N, Wang, S, Zhang, F, Suen, G, Shao, D, Li, S and Diao, Q (2021) Multiomics analysis reveals the presence of a microbiome in the gut of fetal lambs. Gut 70, 853–864.CrossRefGoogle ScholarPubMed
Bittar, CMM, da Silva, JT and Chester-Jones, H (2018) Macronutrient and amino acids composition of milk replacers for dairy calves. Revista Brasileira de Saúde e Produção Animal 19, 47–57.CrossRefGoogle Scholar
Brooks, GF, Carroll, KC, Butel, JS and Morse, SA (2007) Jawetz, Melnick & Adelberg's Medical Microbiology, 24th Edn. Sultan Qaboos University: McGraw-Hill Medical.Google Scholar
Bu, D, Zhang, X, Ma, L, Park, T, Wang, L, Wang, M, Xu, J and Yu, Z (2020) Repeated inoculation of young calves with rumen Microbiota does not significantly modulate the rumen prokaryotic microbiota consistently but decreases diarrhea. Frontiers in Microbiology 11, 1–12.CrossRefGoogle Scholar
Candela, M, Maccaferri, S, Turroni, S, Carnevali, P and Brigidi, P (2010) Functional intestinal microbiome, new frontiers in prebiotic design. International Journal of Food Microbiology 140, 93–101.CrossRefGoogle ScholarPubMed
Cangiano, LR, Yohe, TT, Steele, MA and Renaud, DL (2020) Invited review: strategic use of microbial-based probiotics and prebiotics in dairy calf rearing. Applied Animal Science 36, 630–651.CrossRefGoogle Scholar
Carriço, JA, Rossi, M, Moran-Gilad, J, Van Domselaar, G and Ramirez, M (2018) A primer on microbial bioinformatics for nonbioinformaticians. Clinical Microbiology and Infection 24, 342–349.CrossRefGoogle ScholarPubMed
Castells, L, Bach, A, Aris, A and Terré, M (2013) Effects of forage provision to young calves on rumen fermentation and development of the gastrointestinal tract. Journal of Dairy Science 96, 5226–5236.CrossRefGoogle ScholarPubMed
Castro, JJ, Gomez, A, White, BA, Loften, JR, Drackley, JK and Mangian, HJ (2016) Changes in the intestinal bacterial community, short-chain fatty acid profile, and intestinal development of preweaned Holstein calves. 1. Effects of prebiotic supplementation depend on site and age. Journal of Dairy Science 99, 9703–9715.CrossRefGoogle ScholarPubMed
Chaucheyras-Durand, F and Ossa, F (2014) REVIEW: the rumen microbiome: composition, abundance, diversity, and new investigative tools. The Professional Animal Scientist 30, 1–12.CrossRefGoogle Scholar
Cho, Y-I, Han, J-I, Wang, C, Cooper, V, Schwartz, K, Engelken, T and Yoon, K-J (2013) Case–control study of microbiological etiology associated with calf diarrhea. Veterinary Microbiology 166, 375–385.CrossRefGoogle ScholarPubMed
Clemmons, BA, Voy, BH and Myer, PR (2019) Altering the gut microbiome of cattle: considerations of host-microbiome interactions for persistent microbiome manipulation. Microbial Ecology 77, 523–536.CrossRefGoogle ScholarPubMed
Coelho, MG, Silva, FLM, Silva, MD, da Silva, AP, Cezar, AM, Slanzon, GS, Miqueo, E, de Toledo, AF, Bittar, CMM and De Toledo, A (2020) Acidified milk for feeding dairy calves in tropical raising systems. Journal of Animal and Feed Sciences 29, 215–223.CrossRefGoogle Scholar
Collado, MC, Rautava, S, Aakko, J, Isolauri, E and Salminen, S (2016) Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Scientific Reports 6, 23129.CrossRefGoogle ScholarPubMed
Conroy, ME, Shi, HN and Walker, WA (2009) The long-term health effects of neonatal microbial flora. Current Opinion in Allergy & Clinical Immunology 9, 197–201.CrossRefGoogle ScholarPubMed
Costello, EK, Stagaman, K, Dethlefsen, L, Bohannan, BJM and Relman, DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262.CrossRefGoogle ScholarPubMed
Cruvinel, LB, Ayres, H, Zapa, DMB, Nicaretta, JE, Couto, LFM, Heller, LM, Bastos, TSA, Cruz, BC, Soares, VE, Teixeira, WF, de Oliveira, JS, Fritzen, JT, Alfieri, AA, Freire, RL and Lopes, WDZ (2020) Prevalence and risk factors for agents causing diarrhea (Coronavirus, Rotavirus, Cryptosporidium spp., Eimeria spp., and nematodes helminthes) according to age in dairy calves from Brazil. Tropical Animal Health and Production 52, 777–791.CrossRefGoogle ScholarPubMed
Czarnecki-Maulden, GL (2008) Effect of dietary modulation of intestinal microbiota on reproduction and early growth. Theriogenology 70, 286–290.CrossRefGoogle ScholarPubMed
Daneshvar, D, Khorvash, M, Ghasemi, E, Mahdavi, AH, Moshiri, B, Mirzaei, M, Pezeshki, A and Ghaffari, MH (2015) The effect of restricted milk feeding through conventional or step-down methods with or without forage provision in starter feed on performance of Holstein bull calves1. Journal of Animal Science 93, 3979–3989.CrossRefGoogle ScholarPubMed
Davis, CL and Drackley, JK (1998) The Development, Nutrition, and Management of the Young Calf. (Edn, Ed.). Ames, IA: Iowa State University Press. Available at https://www.cabdirect.org/cabdirect/abstract/19981414219.Google Scholar
de Oliveira, MNV, Jewell, KA, Freitas, FS, Benjamin, LA, Tótola, MR, Borges, AC, Moraes, CA and Suen, G (2013) Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Veterinary Microbiology 164, 307–314.CrossRefGoogle ScholarPubMed
De Simone, C, Ciardi, A, Grassi, A, Gardini, SL, Tzantzoglou, S, Trinchieri, V, Moretti, S and Jirillo, E (1992) Effect of Bifidobacterium bifidum and Lactobacillus acidophilus on gut mucosa and peripheral blood B lymphocytes. Immunopharmacology and Immunotoxicology 14, 331–340.CrossRefGoogle ScholarPubMed
Dehority, BA (1998) Microbial interactions in the rumen. Rev Fac Agron (LUZ) 15, 69–86. Available at https://produccioncientificaluz.org/index.php/agronomia/article/view/26180.Google Scholar
Deng, YF, Wang, YJ, Zou, Y, Azarfar, A, Wei, XL, Ji, SK, Zhang, J, Wu, ZH, Wang, SX, Dong, SZ, Xu, Y, Shao, DF, Xiao, JX, Yang, KL, Cao, ZJ and Li, SL (2017) Influence of dairy by-product waste milk on the microbiomes of different gastrointestinal tract components in pre-weaned dairy calves. Scientific Reports 7, 42689.CrossRefGoogle ScholarPubMed
DePeters, EJ and George, LW (2014) Rumen transfaunation. Immunology Letters 162, 69–76.CrossRefGoogle ScholarPubMed
Deusch, S, Tilocca, B, Camarinha-Silva, A and Seifert, J (2015) News in livestock research – use of omics -technologies to study the microbiota in the gastrointestinal tract of farm animals. Computational and Structural Biotechnology Journal 13, 55–63.CrossRefGoogle Scholar
Dias, J, Marcondes, MI, Noronha, MF, Resende, RT, Machado, FS, Mantovani, HC, Dill-McFarland, KA and Suen, G (2017) Effect of pre-weaning diet on the ruminal archaeal, bacterial, and fungal communities of dairy calves. Frontiers in Microbiology 8, 1–17.CrossRefGoogle ScholarPubMed
Dias, J, Marcondes, MI, de Souza, SM, da Mata e Silva, BC, Noronha, MF, Resende, RT, Machado, FS, Mantovani, HC, Dill-McFarland, KA and Suen, G (2018) Bacterial community dynamics across the gastrointestinal tracts of dairy calves during preweaning development. Applied and Environmental Microbiology 84, e02675–17.CrossRefGoogle ScholarPubMed
Dill-McFarland, KA, Breaker, JD and Suen, G (2017) Microbial succession in the gastrointestinal tract of dairy cows from 2 weeks to first lactation. Scientific Reports 7, 40864.CrossRefGoogle ScholarPubMed
Dill-McFarland, KA, Weimer, PJ, Breaker, JD and Suen, G (2019) Diet influences early Microbiota development in dairy calves without long-term impacts on milk production. Applied and Environmental Microbiology 85, 1–12.CrossRefGoogle ScholarPubMed
Dominguez-Bello, MG, Costello, EK, Contreras, M, Magris, M, Hidalgo, G, Fierer, N and Knight, R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America 107, 11971–11975.CrossRefGoogle ScholarPubMed
dos Santos, G and Bittar, CMM (2015) A survey of dairy calf management practices in some producing regions in Brazil. Revista Brasileira de Zootecnia 44, 361–370.CrossRefGoogle Scholar
Duarte, ER, Abrão, FO, Oliveira Ribeiro, IC, Vieira, EA, Nigri, AC, Silva, KL, Virgínio Júnior, GF, Barreto, SMP and Geraseev, LC (2018) Rumen protozoa of different ages of beef cattle raised in tropical pastures during the dry season. Journal of Applied Animal Research 46, 1457–1461.CrossRefGoogle Scholar
Duffy, LC, Zielezny, MA, Riepenhoff-Talty, M, Dryja, D, Sayahtaheri-Altaie, S, Griffiths, E, Ruffin, D, Barrett, H and Ogra, PL (1994) Reduction of virus shedding by B. bifidum in experimentally induced MRV infection. Digestive Diseases and Sciences 39, 2334–2340.CrossRefGoogle Scholar
Elolimy, A, Alharthi, A, Zeineldin, M, Parys, C, Helmbrecht, A and Loor, JJ (2019) Supply of methionine during late-pregnancy alters fecal microbiota and metabolome in neonatal dairy calves without changes in daily feed intake. Frontiers in Microbiology 10, 1–20.CrossRefGoogle ScholarPubMed
Fischer, AJ, Song, Y, He, Z, Haines, DM, Guan, LL and Steele, MA (2018) Effect of delaying colostrum feeding on passive transfer and intestinal bacterial colonization in neonatal male Holstein calves. Journal of Dairy Science 101, 3099–3109.CrossRefGoogle ScholarPubMed
Fleige, S, Preißinger, W, Meyer, HHD and Pfaffl, MW (2007) Effect of lactulose on growth performance and intestinal morphology of pre-ruminant calves using a milk replacer containing Enterococcus faecium. Animal: An International Journal of Animal Bioscience 1, 367–373.CrossRefGoogle ScholarPubMed
Flint, HJ and Bayer, EA (2008) Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Annals of the New York Academy of Sciences 1125, 280–288.CrossRefGoogle ScholarPubMed
Fonty, G, Gouet, P, Jouany, JP and Senaud, J (1987) Establishment of the microflora and anaerobic fungi in the rumen of lambs. Microbiology (Reading, England) 133, 1835–1843.CrossRefGoogle Scholar
Fonty, G, Senaud, J, Jouany, J-P and Gouet, P (1988) Establishment of ciliate protozoa in the rumen of conventional and conventionalized lambs: influence of diet and management conditions. Canadian Journal of Microbiology 34, 235–241.CrossRefGoogle ScholarPubMed
Fonty, G, Jouany, J, Chavarot, M, Bonnemoy, F and Gouet, P (1991) Development of the rumen digestive functions in lambs placed in a sterile isolator a few days after birth. Reproduction Nutrition Development 31, 521–528.CrossRefGoogle Scholar
Fraser-Liggett, CM (2005) Insights on biology and evolution from microbial genome sequencing. Genome Research 15, 1603–1610.CrossRefGoogle ScholarPubMed
Fruscalso, V, Olmos, G and Hötzel, MJ (2020) Dairy calves’ mortality survey and associated management practices in smallholding, pasture-based herds in southern Brazil. Preventive Veterinary Medicine 175, 104835.CrossRefGoogle ScholarPubMed
Fukushima, Y, Kawata, Y, Hara, H, Terada, A and Mitsuoka, T (1998) Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. International Journal of Food Microbiology 42, 39–44.CrossRefGoogle ScholarPubMed
Gálfi, P, Neogrády, S and Sakata, T (1991) Effects of volatile fatty acids on the epithelial cell proliferation of the digestive tract and its hormonal mediation. In Tsuda T, Sasaki Y and Kawashima R (eds), Physiological Aspects of Digestion and Metabolism in Ruminants. Academic Press, pp. 49–59. Available at https://www.sciencedirect.com/book/9780127022901/physiological-aspects-of-digestion-and-metabolism-in-ruminantsGoogle Scholar
Gibson, GR and Wang, X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. Journal of Applied Bacteriology 77, 412–420.CrossRefGoogle ScholarPubMed
Gill, SR, Pop, M, DeBoy, RT, Eckburg, PB, Turnbaugh, PJ, Samuel, BS, Gordon, JI, Relman, DA, Fraser-Liggett, CM and Nelson, KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359.CrossRefGoogle ScholarPubMed
Godden, SM, Smolenski, DJ, Donahue, M, Oakes, JM, Bey, R, Wells, S, Sreevatsan, S, Stabel, J and Fetrow, J (2012) Heat-treated colostrum and reduced morbidity in preweaned dairy calves: results of a randomized trial and examination of mechanisms of effectiveness. Journal of Dairy Science 95, 4029–4040.CrossRefGoogle ScholarPubMed
Gomez, DE, Arroyo, LG, Costa, MC, Viel, L and Weese, JS (2017) Characterization of the fecal bacterial microbiota of healthy and diarrheic dairy calves. Journal of Veterinary Internal Medicine 31, 928–939.CrossRefGoogle ScholarPubMed
Guilloteau, P, Toullec, R, Grongnet, JF, Patureau-Mirand, P, Prugnaud, J and Sauvant, D (1986) Digestion of milk, fish and soya-bean protein in the preruminant calf: flow of digesta, apparent digestibility at the end of the ileum and amino acid composition of ileal digesta. British Journal of Nutrition 55, 571–592.CrossRefGoogle ScholarPubMed
Gulliksen, SM, Jor, E, Lie, KI, Hamnes, IS, Løken, T, Åkerstedt, J and Østerås, O (2009) Enteropathogens and risk factors for diarrhea in Norwegian dairy calves. Journal of Dairy Science 92, 5057–5066.CrossRefGoogle ScholarPubMed
Guzman, CE, Bereza-Malcolm, LT, De Groef, B and Franks, AE (2015) Presence of selected methanogens, fibrolytic Bacteria, and Proteobacteria in the gastrointestinal tract of neonatal dairy calves from birth to 72 hours. PLoS ONE 10, e0133048.CrossRefGoogle ScholarPubMed
Guzman, CE, Wood, JL, Egidi, E, White-Monsant, AC, Semenec, L, Grommen, SVH, Hill-Yardin, EL, De Groef, B and Franks, AE (2020) A pioneer calf foetus microbiome. Scientific Reports 10, 17712.CrossRefGoogle ScholarPubMed
Hill, TM, Bateman, HG, Aldrich, JM and Schlotterbeck, RL (2010) Effect of milk replacer program on digestion of nutrients in dairy calves. Journal of Dairy Science 93, 1105–1115.CrossRefGoogle ScholarPubMed
Hooper, LV, Bry, L, Falk, PG and Gordon, JI (1998) Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. BioEssays 20, 336–343.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Hornef, M and Penders, J (2017) Does a prenatal bacterial microbiota exist? Mucosal Immunology 10, 598–601.CrossRefGoogle ScholarPubMed
Hungate, RE (1966) The Rumen and its Microbes. New York, NY: Academic Press.Google Scholar
Hungate, RE (1975) The rumen microbial ecosystem. Annual Review of Ecology and Systematics 6, 39–66.CrossRefGoogle Scholar
Izzo, M, Kirkland, P, Mohler, V, Perkins, NR, Gunn, A and House, J (2011) Prevalence of major enteric pathogens in Australian dairy calves with diarrhoea. Australian Veterinary Journal 89, 167–173.CrossRefGoogle ScholarPubMed
Jami, E, Israel, A, Kotser, A and Mizrahi, I (2013) Exploring the bovine rumen bacterial community from birth to adulthood. The ISME Journal 7, 1069–1079.CrossRefGoogle ScholarPubMed
Jiao, J, Lu, Q, Forster, RJ, Zhou, C, Wang, M, Kang, J and Tan, Z (2016) Age and feeding system (supplemental feeding versus grazing) modulates colonic bacterial succession and host mucosal immune maturation in goats1. Journal of Animal Science 94, 2506–2518.CrossRefGoogle Scholar
Kamada, N, Chen, GY, Inohara, N and Núñez, G (2013) Control of pathogens and pathobionts by the gut microbiota. Nature immunology 14, 685–690.CrossRefGoogle ScholarPubMed
Karasov, WH, Martínez del Rio, C and Caviedes-Vidal, E (2011) Ecological physiology of diet and digestive systems. Annual Review of Physiology 73, 69–93.CrossRefGoogle ScholarPubMed
Khan, MA, Lee, HJ, Lee, WS, Kim, HS, Kim, SB, Park, SB, Baek, KS, Ha, JK and Choi, YJ (2008) Starch source evaluation in calf starter: iI. Ruminal parameters, rumen development, nutrient digestibilities, and nitrogen utilization in Holstein calves. Journal of Dairy Science 91, 1140–1149.CrossRefGoogle ScholarPubMed
Khan, MA, Bach, A, Weary, DM and von Keyserlingk, MAG (2016) Invited review: transitioning from milk to solid feed in dairy heifers. Journal of Dairy Science 99, 885–902.CrossRefGoogle ScholarPubMed
Kido, K, Tejima, S, Haramiishi, M, Uyeno, Y, Ide, Y, Kurosu, K and Kushibiki, S (2019) Provision of beta-glucan prebiotics (cellooligosaccharides and kraft pulp) to calves from pre- to post-weaning period on pasture. Animal Science Journal 90, 1537–1543.CrossRefGoogle ScholarPubMed
Kim, HS, Whon, TW, Sung, H, Jeong, Y-S, Jung, ES, Shin, N-R, Hyun, D-W, Kim, PS, Lee, J-Y, Lee, CH and Bae, J-W (2021) Longitudinal evaluation of fecal microbiota transplantation for ameliorating calf diarrhea and improving growth performance. Nature Communications 12, 161.CrossRefGoogle ScholarPubMed
Klein-Jöbstl, D, Schornsteiner, E, Mann, E, Wagner, M, Drillich, M and Schmitz-Esser, S (2014a) Pyrosequencing reveals diverse fecal microbiota in simmental calves during early development. Frontiers in Microbiology 5, 622.Google Scholar
Klein-Jöbstl, D, Iwersen, M and Drillich, M (2014b) Farm characteristics and calf management practices on dairy farms with and without diarrhea: a case-control study to investigate risk factors for calf diarrhea. Journal of Dairy Science 97, 5110–5119.CrossRefGoogle Scholar
Klein-Jöbstl, D, Quijada, NM, Dzieciol, M, Feldbacher, B, Wagner, M, Drillich, M, Schmitz-Esser, S and Mann, E (2019) Microbiota of newborn calves and their mothers reveals possible transfer routes for newborn calves’ gastrointestinal microbiota. PLoS ONE 14, e0220554.CrossRefGoogle ScholarPubMed
Koonin E, V, Makarova, KS and Wolf, YI (2021) Evolution of microbial genomics: conceptual shifts over a quarter century. Trends in Microbiology 1–11 [in press].CrossRefGoogle Scholar
Kouritzin, VA and Guan, LL (2017) The colonization and establishment of the neonatal mammalian microbiome. Fine Focus 3, 89–99.CrossRefGoogle Scholar
Kreikemeier, KK, Harmon, DL, Peters, JP, Gross, KL, Armendariz, CK and Krehbiel, CR (1990) Influence of dietary forage and feed intake on carbohydrase activities and small intestinal morphology of calves. Journal of Animal Science 68, 2916.CrossRefGoogle ScholarPubMed
Lanz Uhde, F, Kaufmann, T, Sager, H, Albini, S, Zanoni, R, Schelling, E and Meylan, M (2008) Prevalence of four enteropathogens in the faeces of young diarrhoeic dairy calves in Switzerland. Veterinary Record 163, 362–366.CrossRefGoogle Scholar
Leahy, SC, Higgins, DG, Fitzgerald, GF and Sinderen, D (2005) Getting better with bifidobacteria. Journal of Applied Microbiology 98, 1303–1315.CrossRefGoogle ScholarPubMed
Ley, RE, Backhed, F, Turnbaugh, PJ, Lozupone, CA, Knight, RD and Gordon, JI (2005) Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences USA 102, 11070–11075.CrossRefGoogle ScholarPubMed
Li, RW, Sparks, M and Connor, EE (2011) Dynamics of the rumen microbiota. In Li, RW (ed.), Metagenomics its Appl. Agric. New York, NY: Nova Science Publishers, pp. 135–164. Available at https://www.ars.usda.gov/research/publications/publication/?seqNo115=248434.Google Scholar
Li, RW, Connor, EE, Li, C, Baldwin VI, RL and Sparks, ME (2012) Characterization of the rumen microbiota of pre-ruminant calves using metagenomic tools. Environmental Microbiology 14, 129–139.CrossRefGoogle ScholarPubMed
Lukens, JR, Gurung, P, Vogel, P, Johnson, GR, Carter, RA, McGoldrick, DJ, Bandi, SR, Calabrese, CR, Walle, LV, Lamkanfi, M and Kanneganti, T-D (2014) Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516, 246–249.CrossRefGoogle ScholarPubMed
Ma, T, Tu, Y, Zhang, N, Guo, J, Deng, K, Zhou, Y, Yun, Q and Diao, Q (2015) Effects of dietary yeast β-glucan on nutrient digestibility and serum profiles in pre-ruminant Holstein calves. Journal of Integrative Agriculture 14, 749–757.CrossRefGoogle Scholar
Ma, T, Villot, C, Renaud, D, Skidmore, A, Chevaux, E, Steele, M and Guan, LL (2020) Linking perturbations to temporal changes in diversity, stability, and compositions of neonatal calf gut microbiota: prediction of diarrhea. The ISME Journal 14, 2223–2235.CrossRefGoogle ScholarPubMed
Mackie, RI, Sghir, A and Gaskins, HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. The American Journal of Clinical Nutrition 69, 1035s–1045s.CrossRefGoogle ScholarPubMed
Malmuthuge, N and Guan, LL (2016) Gut microbiome and omics: a new definition to ruminant production and health. Animal Frontiers 6, 8–12.CrossRefGoogle Scholar
Malmuthuge, N, Griebel, PJ and Guan, LL (2015a) The gut microbiome and Its potential role in the development and function of newborn calf gastrointestinal tract. Frontiers in Veterinary Science 2, 2016.CrossRefGoogle Scholar
Malmuthuge, N, Chen, Y, Liang, G, Goonewardene, LA and Guan, LL (2015b) Heat-treated colostrum feeding promotes beneficial bacteria colonization in the small intestine of neonatal calves. Journal of Dairy Science 98, 8044–8053.CrossRefGoogle Scholar
Malmuthuge, N, Liang, G and Guan, LL (2019) Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes. Genome Biology 20, 172.CrossRefGoogle ScholarPubMed
Maranduba, CdC, De Castro, SBR, De Souza, GT, Rossato, C, da Guia, FC, Valente, MAS, Rettore, JVP, Maranduba, CP, De Souza, CM, Do Carmo, AMR, Macedo, GC and Silva, FDS (2015) Intestinal microbiota as modulators of the immune system and neuroimmune system: impact on the host health and homeostasis. Journal of Immunology Research 2015, 1–14.CrossRefGoogle ScholarPubMed
Maynard, CL, Elson, CO, Hatton, RD and Weaver, CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231–241.CrossRefGoogle ScholarPubMed
Meale, SJ, Li, S, Azevedo, P, Derakhshani, H, Plaizier, JC, Khafipour, E and Steele, MA (2016) Development of ruminal and fecal microbiomes are affected by weaning but not weaning strategy in dairy calves. Frontiers in Microbiology 7, 1–16.CrossRefGoogle Scholar
Meale, SJ, Chaucheyras-Durand, F, Berends, H, Guan, LL and Steele, MA (2017) From pre- to postweaning: transformation of the young calf's gastrointestinal tract. Journal of Dairy Science 100, 5984–5995.CrossRefGoogle Scholar
Minato, H, Otsuka, M, Shirasaka, S, Itabashi, H and Mitsumori, M (1992) Colonization of microorganisms in the rumen of young calves. The Journal of General and Applied Microbiology 38, 447–456.CrossRefGoogle Scholar
Mohammed, SAE-M, Marouf, SAE-M, Erfana, AM, El-Jakee, JKAE-H, Hessain, AM, Dawoud, TM, Kabli, SA and Moussa, IM (2019) Risk factors associated with E. coli causing neonatal calf diarrhea. Saudi Journal of Biological Sciences 26, 1084–1088.CrossRefGoogle Scholar
Mulder, IE, Schmidt, B, Lewis, M, Delday, M, Stokes, CR, Bailey, M, Aminov, RI, Gill, BP, Pluske, JR, Mayer, C-D and Kelly, D (2011) Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS ONE 6, e28279.CrossRefGoogle ScholarPubMed
Myer, PR, Smith, TPL, Wells, JE, Kuehn, LA and Freetly, HC (2015) Rumen microbiome from steers differing in feed efficiency. PLoS ONE 10, e0129174.CrossRefGoogle ScholarPubMed
Nagaraja, TG (2016) Microbiology of the rumen. In Millen D, De Beni AM and Lauritano PR (eds), Rumenology. Cham: Springer International Publishing, pp. 39–61. Available at https://doi.org/10.1007/978-3-319-30533-2_2CrossRefGoogle Scholar
Neish, AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136, 65–80.CrossRefGoogle ScholarPubMed
Newbold, CJ, de la Fuente, G, Belanche, A, Ramos-Morales, E and McEwan, NR (2015) The role of ciliate protozoa in the rumen. Frontiers in Microbiology 6, 1–14.CrossRefGoogle ScholarPubMed
O'Connell Motherway, M, Zomer, A, Leahy, SC, Reunanen, J, Bottacini, F, Claesson, MJ, O'Brien, F, Flynn, K, Casey, PG, Moreno Munoz, JA, Kearney, B, Houston, AM, O'Mahony, C, Higgins, DG, Shanahan, F, Palva, A, de Vos, WM, Fitzgerald, GF, Ventura, M, O'Toole, PW and van Sinderen, D (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proceedings of the National Academy of Sciences USA 108, 11217–11222.CrossRefGoogle ScholarPubMed
O'Hara, E, Kelly, A, McCabe, MS, Kenny, DA, Guan, LL and Waters, SM (2018) Effect of a butyrate-fortified milk replacer on gastrointestinal microbiota and products of fermentation in artificially reared dairy calves at weaning. Scientific Reports 8, 14901.CrossRefGoogle ScholarPubMed
Oikonomou, G, Teixeira, AGV, Foditsch, C, Bicalho, ML, Machado, VS and Bicalho, RC (2013) Fecal microbial diversity in pre-weaned dairy calves as described by pyrosequencing of metagenomic 16S rDNA. Associations of Faecalibacterium species with health and growth. PLoS ONE 8, e63157.CrossRefGoogle Scholar
Pacheco, AR, Barile, D, Underwood, MA and Mills, DA (2015) The impact of the milk glycobiome on the neonate gut microbiota. Annual Review of Animal Biosciences 3, 419–445.CrossRefGoogle ScholarPubMed
Pan, X, Li, Z, Li, B, Zhao, C, Wang, Y, Chen, Y and Jiang, Y (2021) Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats. BMC Genomics 22, 288.CrossRefGoogle ScholarPubMed
Pascale, A, Marchesi, N, Marelli, C, Coppola, A, Luzi, L, Govoni, S, Giustina, A and Gazzaruso, C (2018) Microbiota and metabolic diseases. Endocrine 61, 357–371.CrossRefGoogle ScholarPubMed
Pereira, RVV, Carroll, LM, Lima, S, Foditsch, C, Siler, JD, Bicalho, RC and Warnick, LD (2018) Impacts of feeding preweaned calves milk containing drug residues on the functional profile of the fecal microbiota. Scientific Reports 8, 554.CrossRefGoogle ScholarPubMed
Pitta, DW, Pinchak, WE, Dowd, SE, Osterstock, J, Gontcharova, V, Youn, E, Dorton, K, Yoon, I, Min, BR, Fulford, JD, Wickersham, TA and Malinowski, DP (2010) Rumen bacterial diversity dynamics associated with changing from Bermudagrass hay to grazed winter wheat diets. Microbial Ecology 59, 511–522.CrossRefGoogle ScholarPubMed
Poczynek, M, de Toledo, AF, da Silva, AP, Silva, MD, Oliveira, GB, Coelho, MG, Virgínio Júnior, GF, Polizel, DM, Costa, JHC and Bittar, CMM (2020) Partial corn replacement by soybean hull, or hay supplementation: effects of increased NDF in diet on performance, metabolism and behavior of pre-weaned calves. Livestock Science 231, 103858.CrossRefGoogle Scholar
Pollock, J, Glendinning, L, Wisedchanwet, T and Watson, M (2018) The madness of microbiome: attempting to find consensus “best practice” for 16S microbiome studies. Applied and Environmental Microbiology 84, 1–12.CrossRefGoogle ScholarPubMed
Reis, ME, Toledo, AF, da Silva, AP, Poczynek, M, Fioruci, EA, Cantor, MC, Greco, L and Bittar, CMM (2021) Supplementation of lysolecithin in milk replacer for Holstein dairy calves: effects on growth performance, health, and metabolites. Journal of Dairy Science 104, 5457–5466.CrossRefGoogle ScholarPubMed
Renaud, DL, Kelton, DF, Weese, JS, Noble, C and Duffield, TF (2019) Evaluation of a multispecies probiotic as a supportive treatment for diarrhea in dairy calves: a randomized clinical trial. Journal of Dairy Science 102, 4498–4505.CrossRefGoogle ScholarPubMed
Rey, M, Enjalbert, F, Combes, S, Cauquil, L, Bouchez, O and Monteils, V (2014) Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. Journal of Applied Microbiology 116, 245–257.CrossRefGoogle ScholarPubMed
Russell, JB and Wilson, DB (1996) Why are ruminal cellulolytic bacteria unable to digest cellulose at low pH? Journal of Dairy Science 79, 1503–1509.CrossRefGoogle ScholarPubMed
Russell, SL, Gold, MJ, Hartmann, M, Willing, BP, Thorson, L, Wlodarska, M, Gill, N, Blanchet, M, Mohn, WW, McNagny, KM and Finlay, BB (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Reports 13, 440–447.CrossRefGoogle ScholarPubMed
Saif, LJ and Smith, KL (1985) Enteric viral infections of calves and passive immunity. Journal of Dairy Science 68, 206–228.CrossRefGoogle ScholarPubMed
Sanford, RA, Lloyd, KG, Konstantinidis, KT and Löffler, FE (2021) Microbial taxonomy run amok. Trends in Microbiology 29, 394–404.CrossRefGoogle ScholarPubMed
Sansonetti, PJ and Medzhitov, R (2009) Learning tolerance while fighting ignorance. Cell 138, 416–420.CrossRefGoogle ScholarPubMed
Savage, DC (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology 31, 107–133.CrossRefGoogle ScholarPubMed
Seedorf, H, Kittelmann, S, Henderson, G and Janssen, PH (2014) RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. PeerJ 2, e494.CrossRefGoogle ScholarPubMed
Signorini, ML, Soto, LP, Zbrun, MV, Sequeira, GJ, Rosmini, MR and Frizzo, LS (2012) Impact of probiotic administration on the health and fecal microbiota of young calves: a meta-analysis of randomized controlled trials of lactic acid bacteria. Research in Veterinary Science 93, 250–258.CrossRefGoogle ScholarPubMed
Singh, BB, Sharma, R, Kumar, H, Banga, HS, Aulakh, RS, Gill, JPS and Sharma, JK (2006) Prevalence of Cryptosporidium parvum infection in Punjab (India) and its association with diarrhea in neonatal dairy calves. Veterinary Parasitology 140, 162–165.CrossRefGoogle ScholarPubMed
Slanzon, GS, de Toledo, AF, da Silva, AP, Coelho, MG, da Silva, MD, Cezar, AM and Bittar, CMM (2019) Red propolis as an additive for preweaned dairy calves: effect on growth performance, health, and selected blood parameters. Journal of Dairy Science 102, 8952–8962.CrossRefGoogle ScholarPubMed
Smith, PE, Waters, SM, Gómez Expósito, R, Smidt, H, Carberry, CA and McCabe, MS (2020) Synthetic sequencing standards: a guide to database choice for rumen microbiota amplicon sequencing analysis. Frontiers in Microbiology 11, 1–11.CrossRefGoogle ScholarPubMed
Sommer, F, Ståhlman, M, Ilkayeva, O, Arnemo, JM, Kindberg, J, Josefsson, J, Newgard, CB, Fröbert, O and Bäckhed, F (2016) The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Reports 14, 1655–1661.CrossRefGoogle ScholarPubMed
Steele, MA, Penner, GB, Chaucheyras-Durand, F and Guan, LL (2016) Development and physiology of the rumen and the lower gut: targets for improving gut health. Journal of Dairy Science 99, 4955–4966.CrossRefGoogle ScholarPubMed
Suarez-Mena, FX, Heinrichs, AJ, Jones, CM, Hill, TM and Quigley, JD (2016) Straw particle size in calf starters: effects on digestive system development and rumen fermentation. Journal of Dairy Science 99, 341–353.CrossRefGoogle ScholarPubMed
Sun, D, Mao, S, Zhu, W and Liu, J (2019) Effects of starter feeding on caecal mucosal bacterial composition and expression of genes involved in immune and tight junctions in pre-weaned twin lambs. Anaerobe 59, 167–175.CrossRefGoogle ScholarPubMed
Taschuk, R and Griebel, PJ (2012) Commensal microbiome effects on mucosal immune system development in the ruminant gastrointestinal tract. Animal Health Research Reviews 13, 129–141.CrossRefGoogle ScholarPubMed
Terré, M, Pedrals, E, Dalmau, A and Bach, A (2013) What do preweaned and weaned calves need in the diet: a high fiber content or a forage source? Journal of Dairy Science 96, 5217–5225.CrossRefGoogle ScholarPubMed
Theis, KR, Romero, R, Greenberg, JM, Winters, AD, Garcia-Flores, V, Motomura, K, Ahmad, MM, Galaz, J, Arenas-Hernandez, M and Gomez-Lopez, N (2020) No consistent evidence for microbiota in murine placental and fetal tissues. mSphere 5, 1–18.Google ScholarPubMed
Thomas, M, Webb, M, Ghimire, S, Blair, A, Olson, K, Fenske, GJ, Fonder, AT, Christopher-Hennings, J, Brake, D and Scaria, J (2017) Metagenomic characterization of the effect of feed additives on the gut microbiome and antibiotic resistome of feedlot cattle. Scientific Reports 7, 12257.CrossRefGoogle ScholarPubMed
Toledo, AF, da Silva, AP, Poczynek, M, Coelho, MG, Silva, MD, Polizel, DM, Reis, ME, Virgínio Júnior, GF, Millen, DD and Bittar, CMM (2020) Whole-flint corn grain or tropical grass hay free choice in the diet of dairy calves. Journal of Dairy Science 103, 10083–10098.CrossRefGoogle ScholarPubMed
Uyeno, Y, Sekiguchi, Y and Kamagata, Y (2010) rRNA-based analysis to monitor succession of faecal bacterial communities in Holstein calves. Letters in Applied Microbiology 51, 570–577.CrossRefGoogle ScholarPubMed
Větrovský, T, Morais, D, Kohout, P, Lepinay, C, Algora, C, Awokunle Hollá, S, Bahnmann, BD, Bílohnědá, K, Brabcová, V, D'Alò, F, Human, ZR, Jomura, M, Kolařík, M, Kvasničková, J, Lladó, S, López-Mondéjar, R, Martinović, T, Mašínová, T, Meszárošová, L, Michalčíková, L, Michalová, T, Mundra, S, Navrátilová, D, Odriozola, I, Piché-Choquette, S, Štursová, M, Švec, K, Tláskal, V, Urbanová, M, Vlk, L, Voříšková, J, Žifčáková, L and Baldrian, P (2020) GlobalFungi, a global database of fungal occurrences from high-throughput-sequencing metabarcoding studies. Scientific Data 7, 228.CrossRefGoogle ScholarPubMed
Virgínio Júnior, GF, de Azevedo, RA, Ornelas, LTC, de Oliveira, NJ, Geraseev, LC and Duarte, ER (2016) Physico-chemical and microbiological characterization of ruminal fluid from gastrointestinal contents of Holstein calves in artificial fed milk conventional or fractionated. Acta Veterinaria Brasilica 10, 305–313.Google Scholar
Virgínio Júnior, GF, Coelho, MG, de Toledo, AF, Montenegro, H, Coutinho, LL and Bittar, CMM (2021) The liquid diet composition affects the fecal bacterial community in pre-weaning dairy calves. Frontiers in Animal Science 2, 12.CrossRefGoogle Scholar
Weimer, PJ (2015) Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Frontiers in Microbiology 6, 296.CrossRefGoogle ScholarPubMed
Wickramasinghe, HKJP, Kramer, AJ and Appuhamy, JADRN (2019) Drinking water intake of newborn dairy calves and its effects on feed intake, growth performance, health status, and nutrient digestibility. Journal of Dairy Science 102, 377–387.CrossRefGoogle ScholarPubMed
Wijdeveld, M, Nieuwdorp, M and IJzerman, R (2020) The interaction between microbiome and host central nervous system: the gut-brain axis as a potential new therapeutic target in the treatment of obesity and cardiometabolic disease. Expert Opinion on Therapeutic Targets 24, 639–653.CrossRefGoogle ScholarPubMed
Williams, AG and Coleman, GS (1997) The rumen protozoa. In Hobson PN and Stewart CS (eds), The Rumen Microbial Ecossystem. Dordrecht: Springer. pp 73–139. Available at https://doi.org/10.1007/978-94-009-1453-7_3Google Scholar
Williams, CL, Garcia-Reyero, N, Martyniuk, CJ, Tubbs, CW and Bisesi, JH (2020) Regulation of endocrine systems by the microbiome: perspectives from comparative animal models. General and Comparative Endocrinology 292, 113437.CrossRefGoogle ScholarPubMed
Wood, KM, Palmer, SI, Steele, MA, Metcalf, JA and Penner, GB (2015) The influence of age and weaning on permeability of the gastrointestinal tract in Holstein bull calves. Journal of Dairy Science 98, 7226–7237.CrossRefGoogle ScholarPubMed
Wu, GD, Compher, C, Chen, EZ, Smith, SA, Shah, RD, Bittinger, K, Chehoud, C, Albenberg, LG, Nessel, L, Gilroy, E, Star, J, Weljie, AM, Flint, HJ, Metz, DC, Bennett, MJ, Li, H, Bushman, FD and Lewis, JD (2016) Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut 65, 63–72.CrossRefGoogle ScholarPubMed
Yáñez-Ruiz, DR, Macías, B, Pinloche, E and Newbold, CJ (2010) The persistence of bacterial and methanogenic archaeal communities residing in the rumen of young lambs. FEMS Microbiology Ecology 72, 272–278.CrossRefGoogle ScholarPubMed
Yeoman, CJ and White, BA (2014) Gastrointestinal tract microbiota and probiotics in production animals. Annual Review of Animal Biosciences 2, 469–486.CrossRefGoogle ScholarPubMed
Yeoman, CJ, Ishaq, SL, Bichi, E, Olivo, SK, Lowe, J and Aldridge, BM (2018) Biogeographical differences in the influence of maternal microbial sources on the early successional development of the bovine neonatal gastrointestinal tract. Scientific Reports 8, 3197.CrossRefGoogle ScholarPubMed
Yu, S, Shi, W, Yang, B, Gao, G, Chen, H, Cao, L, Yu, Z and Wang, J (2020) Effects of repeated oral inoculation of artificially fed lambs with lyophilized rumen fluid on growth performance, rumen fermentation, microbial population and organ development. Animal Feed Science and Technology 264, 114465.CrossRefGoogle Scholar
Zeineldin, M, Aldridge, B and Lowe, J (2018) Dysbiosis of the fecal microbiota in feedlot cattle with hemorrhagic diarrhea. Microbial Pathogenesis 115, 123–130.CrossRefGoogle ScholarPubMed
Zhou, M, Chen, Y, Griebel, PJ and Guan, LL (2014) Methanogen prevalence throughout the gastrointestinal tract of pre-weaned dairy calves. Gut Microbes 5, 628–638.CrossRefGoogle ScholarPubMed
Zou, Y, Wang, Y, Deng, Y, Cao, Z, Li, S and Wang, J (2017) Effects of feeding untreated, pasteurized and acidified waste milk and bunk tank milk on the performance, serum metabolic profiles, immunity, and intestinal development in Holstein calves. Journal of Animal Science and Biotechnology 8, 53.CrossRefGoogle ScholarPubMed