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High-grain diet feeding altered the composition and functions of the rumen bacterial community and caused the damage to the laminar tissues of goats

Published online by Cambridge University Press:  19 March 2018

R. Y. Zhang ,
W. Jin ,
P. F. Feng ,
J. H. Liu  and
S. Y. Mao
R. Y. Zhang
Affiliation:
Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang 110866, China
W. Jin
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
P. F. Feng
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
J. H. Liu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
S. Y. Mao*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
*
†E-mail: [email protected]
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Abstract

In the current intensive production system, ruminants are often fed high-grain (HG) diets. However, this feeding pattern often causes rumen metabolic disorders and may further trigger laminitis, the exact mechanism is not clear. This study investigated the effect of HG diet feeding on fermentative and microbial changes in the rumen and on the expression of pro-inflammatory cytokines and matrix metalloproteinases (MMPs) in the lamellar tissue. In all, 12 male goats were fed a hay diet (0% grain; n=6) or an HG diet (56.5% grain; n=6). On day 50 of treatment, samples of blood, rumen content, and lamellar tissue of hooves of goats were collected. The data showed that compared with the hay group, HG-fed goats had lower (P<0.05) rumen pH but higher (P<0.05) total volatile fatty acids and lactate in the rumen and higher (P<0.05) lipopolysaccharide (LPS) levels in the rumen and blood. HG diet feeding altered the composition of rumen bacterial community, and correspondingly, the results suggested that their functions in the HG group were also altered. HG diet feeding increased (P<0.05) the expression of interleukin-1β, interleukin-6, tumour necrosis factor-α and MMP-2 mRNA in the lamellar tissues compared with the hay group. Correlation analysis indicated that the expression of pro-inflammatory cytokines were positively correlated with MMP-2 expression in lamellar tissues. Overall, these results revealed that HG feeding altered the patterns of rumen fermentation and the composition and functions of rumen bacterial community, and lead to higher levels of LPS in the peripheral blood, and further activated the inflammatory response in lamellar tissues, which may progress to the level of laminar damage.

Keywords

rumenlipopolysaccharidelaminitishoovesgoat
Type
Research Article
Information
animal , Volume 12 , Issue 12 , December 2018 , pp. 2511 - 2520
Copyright
© The Animal Consortium 2018 

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References

Bassi, DE, Lopez De Cicco, R, Cenna, J, Litwin, S, Cukierman, E and Klein-Szanto, AJ 2005. PACE4 expression in mouse basal keratinocytes results in basement membrane disruption and acceleration of tumor progression. Cancer Research 65, 7310–7319.Google Scholar
Bicalho, RC, Machado, VS and Caixeta, LS 2009. Lameness in dairy cattle: a debilitating disease or a disease of debilitated cattle? A cross-sectional study of lameness prevalence and thickness of the digital cushion. Journal of Dairy Science 92, 3175–3184.Google Scholar
Clutterbuck, AL, Harris, P, Allaway, D and Mobasheri, A 2010. Matrix metalloproteinases in inflammatory pathologies of the horse. Veterinary Journal 183, 27–38.Google Scholar
Cotta, MA 1988. Amylolytic activity of selected species of ruminal bacterial. Applied and Environmental Microbiology 54, 772–776.Google Scholar
Emmanuel, DG, Dunn, SM and Ametaj, BN 2008. Feeding high proportions of barley grain stimulates an inflammatory response in dairy cows. Journal of Dairy Science 91, 606–614.Google Scholar
Fernando, SC, Purvis, HT, Najar, FZ, Sukharnikov, LO, Krehbiel, CR, Nagaraja, TG, Roe, BA and Desilva, U 2010. Rumen microbial population dynamics during adaptation to a high-grain diet. Applied and Environmental Microbiology 76, 7482–7490.Google Scholar
Greenough, PR, Vermunt, JJ, McKinnon, JJ, Fathy, FA, Berg, PA and Cohen, RD 1990. Laminitis-like changes in the claws of feedlot cattle. Canadian Veterinary Journal 31, 202–208.Google Scholar
Hendry, KA, Knight, CH, Galbraith, H and Wilde, CJ 2003. Basement membrane integrity and keratinization in healthy and ulcerated bovine hoof tissue. Journal of Dairy Research 70, 19–27.Google Scholar
Hua, C, Tian, J, Tian, P, Cong, R, Luo, Y, Geng, Y, Tao, S, Ni, Y and Zhao, R 2017. Feeding a high concentration diet induces unhealthy alterations in the composition and metabolism of ruminal microbiota and host response in a goat model. Frontiers in Microbiology 8, 138.Google Scholar
Johnson, PJ, Kreeger, JM, Keeler, M, Ganjam, VK and Messer, NT 2000. Serum markers of lamellar basement membrane degradation and lamellar histopathological changes in horses affected with laminitis. Equine Veterinary Journal 32, 462–468.Google Scholar
Khafipour, E, Krause, DO and Plaizier, JC 2009a. A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. Journal of Dairy Science 92, 1060–1070.Google Scholar
Khafipour, E, Li, S, Plaizier, JC and Krause, DO 2009b. Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Applied and Environmental Microbiology 75, 7115–7124.Google Scholar
Khafipour, E, Li, S, Tun, HM, Derakshani, H, Moossavi, S and Plaizier, JC 2016. Effects of grain feeding on microbiota in the digestive tract of cattle. Animal Frontiers 6, 13–19.Google Scholar
Klieve, AV, O’Leary, MN, McMillen, L and Ouwerkerk, D 2007. Ruminococcus bromii, identification and isolation as a dominant community member in the rumen of cattle fed a barley diet. Journal of Applied Microbiology 103, 2065–2073.Google Scholar
Kossakowska, AE, Edwards, DR, Prusinkiewicz, C, Zhang, MC, Guo, D, Urbanski, SJ, Grogan, T, Marquez, LA and Janowska-Wieczorek, A 1999. Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin’s lymphomas. Blood 94, 2080–2089.Google Scholar
Kyaw-Tanner, M and Pollitt, CC 2004. Equine laminitis: increased transcription of matrix metalloproteinase-2 (MMP-2) occurs during the developmental phase. Equine Veterinary Journal 36, 221–225.Google Scholar
Leise, BS, Faleiros, RR, Watts, M, Johnson, PJ, Black, SJ and Belknap, JK 2011. Laminar inflammatory gene expression in the carbohydrate overload model of equine laminitis. Equine Veterinary Journal 43, 54–61.Google Scholar
Li, XR, Jiang, RL, Wang, GY, Li, Y, Fan, XJ, Liu, X, Wang, JL, Pan, JL and Gao, L 2015. MMP-2 plays an important role during the early acute developmental phase of oligofructose-induced equine laminitis. Bulletin of the Veterinary Institute in Pulawy 59, 149–153.Google Scholar
Liu, JH, Xu, TT, Liu, YJ, Zhu, WY and Mao, SY 2013. A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 305, R232–R241.Google Scholar
Loftus, JP, Johnson, PJ, Belknap, JK, Pettigrew, A and Black, SJ 2009. Leukocyte-derived and endogenous matrix metalloproteinases in the lamellae of horses with naturally acquired and experimentally induced laminitis. Veterinary Immunology and Immunopathology 129, 221–230.Google Scholar
Manichanh, C, Rigottier-Gois, L, Bonnaud, E, Gloux, K, Pelletier, E, Frangeul, L, Nalin, R, Jarrin, C, Chardon, P, Marteau, P, Roca, J and Dore, J 2006. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55, 205–211.Google Scholar
Nocek, JE 1997. Bovine acidosis: implications on laminitis. Journal of Dairy Science 80, 1005–1028.Google Scholar
Nourian, AR, Asplin, KE, McGowan, CM, Sillence, MN and Pollitt, CC 2009. Equine laminitis: ultrastructural lesions detected in ponies following hyperinsulinaemia. Equine Veterinary Journal 41, 671–677.Google Scholar
Owens, F, Secrist, D, Hill, W and Gill, D 1998. Acidosis in cattle: a review. Journal of Animal Science 76, 275–286.Google Scholar
Plaizier, JC, Khafipour, E, Li, S, Gozho, GN and Krause, DO 2012. Subacute ruminal acidosis (SARA), endotoxins and health consequences. Animal Feed Science and Technology 172, 9–21.Google Scholar
Plaizier, JC, Li, S, Tun, HM and Khafipour, E 2016. Nutritional models of experimentally-induced subacute ruminal acidosis (SARA) differ in their impact on rumen and hindgut bacterial communities in dairy cows. Frontiers in Microbiology 7, 2128.Google Scholar
Pollitt, CC 1996. Basement membrane pathology: a feature of acute equine laminitis. Equine Veterinary Journal 28, 38–46.Google Scholar
Saleem, F, Ametaj, BN, Bouatra, S, Mandal, R, Zebeli, Q, Dunn, SM and Wishart, DS 2012. A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. Journal of Dairy Science 95, 6606–6623.Google Scholar
Sato, H, Takino, T, Kinoshita, T, Imai, K, Okada, Y, Stetler Stevenson, WG and Seiki, M 1996. Cell surface binding and activation of gelatinase A induced by expression of membrane-type-1-matrix metalloproteinase (MT1-MMP). FEBS Letters 385, 238–240.Google Scholar
Steele, MA, Croom, J, Kahler, M, AlZahal, O, Hook, SE, Plaizier, K and McBride, BW 2011. Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. American Journal of Physiology-regulatory Integrative and Comparative Physiology 300, R1515–R1523.Google Scholar
Stevenson, DM and Weimer, PJ 2007. Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Applied Microbiology and Biotechnology 75, 165–174.Google Scholar
van Eps, AW and Pollitt, CC 2004. Equine laminitis: cryotherapy reduces the severity of the acute lesion. Equine Veterinary Journal 36, 255–260.Google Scholar
Webster, AJ, Knott, L and Tarlton, JF 2005. Understanding lameness in the dairy cow. Cattle Practice 13, 93–98.Google Scholar
Zhang, RY, Ye, HM, Liu, JH and Mao, SY 2017. High-grain diets altered rumen fermentation and epithelial bacterial community and resulted in rumen epithelial injuries of goats. Applied Microbiology and Biotechnology 101, 6981–6992.Google Scholar
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