Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático

La hipercetonemia o cetosis bovina es un desorden metabólico, que se caracteriza por el incremento patológico de cuerpos cetónicos (beta-hidroxibutirato (βHB), Acetoacetato (AcAc) y acetona) y ocurre en el periparto de vacas de leche. El origen primario de la enfermedad es el balance energético negativo (BEN), que puede ser desencadenado por el incremento excesivo de los requerimientos energéticos o la presentación de enfermedades posparto, resultando en la presentación de signos clínicos o disminución de la producción de leche. El objetivo de esta revisión consiste en describir, mediante un modelo, los procesos bioquímicos del rumen y los mecanismos fisiopatológicos, involucrados con incremento excesivo de los cuerpos cetónicos. En resumen... Ver más

Guardado en:

0123-4226

2619-2551

23

2020-06-30

http://purl.org/coar/access_right/c_abf2

info:eu-repo/semantics/openAccess

Oscar Felípe Huertas Molina, Daniela Londoño Vásquez, Martha Olivera Angel - 2020

id 6db59c87499b6c92ea2856c1f228019d
record_format ojs
spelling Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
MANN, S.; YEPES, F.A.L.; BEHLING-KELLY, E.; MCART, J.A.A. 2017. The effect of different treatments for early-lactation hyperketonemia on blood β-hydroxybutyrate, plasma nonesterified fatty acids, glucose, insulin, and glucagon in dairy cattle. J. Dairy Science (Estados Unidos), 100(8):6470-6482. https://doi.org/10.3168/jds.2016-12532
PRATTI DANIEL, J.L.; RESENDE JÚNIOR, J.C. 2012. Absorção e metabolismo de ácidos graxos voláteis pelo rúmen e omaso. Ciencia E Agrotecnologia (Brasil). 36(1):93-99. https://doi.org/10.1590/S1413-70542012000100012
PRATAMA, R.; ARTIKA, I.M.; CHAIDAMSARI, T.; SUGIARTI, H.; PUTRA, S.M. 2014. Isolation and molecular cloning of cellulase gene from bovine rumen bacteria. Current Biochemistry (Indonesia). 1(1):29-36. https://doi.org/10.29244/cb.1.1.29-36
PABON, M. 2004. Notas de clase. Bioquímica ruminal. Ed. Universidad Nacional de Colombia (Bogotá D.C). 50p.
NOCEK, J.E.; HERBEIN, J.H.; POLAN, C.E. 1980. Influence of ration physical form, ruminal degradable nitrogen and age on rumen epithelial propionate and acetate transport and some enzymatic activities. The J. Nutrition (Inglaterra). 110(12):2355-2364. https://doi.org/10.1093/jn/110.12.2355
NIELSEN, L.; GONZALEZ-GARCIA, R.; MARCELLIN, E.; NAVONE, L.; STOWERS, C.; MCCUBBIN, T. 2017. Microbial propionic acid production. Fermentation (Estados Unidos). 3(2):21. https://doi.org/10.3390/fermentation3020021
NAKAMURA, S.; HAGA, S.; KIMURA, K.; MATSUYAMA, S. 2018. Propionate and butyrate induce gene expression of monocarboxylate transporter 4 and cluster of differentiation 147 in cultured rumen epithelial cells derived from preweaning dairy calves. Journal of Animal Science (Inglaterra). 96(11):4902-4911. https://doi.org/10.1093/jas/sky334
MURRAY, R.; BENDER, D.; BOTHAM, K.L.; KENNELLY, P.J.; RODWELL, V.W.; WEIL P.A. 2012. Bioquímica ilustrada harper. Ed. McGrawHill (Estados Unidos). 480p.
MILLEN, D.D.; ARRIGONI, M.D.B.; DIAS, R. 2016. Rumenology. Ed. Springer L. (Brasil). 314p.
MIAO, L.; YANG, Y.; LIU, Y.; LAI, L.; WANG, L.; ZHAN, Y.; YIN, R.; YU, M.; LI, CH.; YANG, X.; GE, C. 2019. Glycerol kinase interacts with nuclear receptor nr4a1 and regulates glucose metabolism in the liver. FASEB J.Official Publication of the Federation of American Societies for Experimental Biology (Estados Unidos). 33(6):6736-6747. https://doi.org/10.1096/fj.201800945RR
MATSUMOTO, H.; SASAKI, K.; BESSHO, T.; KOBAYASHI, E.; ABE, T.; SASAZAKI, S.; OYAMA, K.; MANNEN, H. 2012. The snps in the acaca gene are effective on fatty acid composition in Holstein milk. Molecular Biology Reports (Suiza). 39(9):8637-8644. https://doi.org/10.1007/s11033-012-1718-5
MADRESEH-GHAHFAROKHI, S.; DEHGHANI-SAMANI, A.; DEHGHANI-SAMANI, A. 2018. Ketosis (acetonaemia) in dairy cattle farms: practical guide based on importance, diagnosis, prevention and treatments. J. Dairy, Veterinary & Animal Research (Hungría), 7(6):299-302. doi.org/10.15406/jdvar.2018.07.00230
RATANAKHANOKCHAI, K.; WAEONUKUL, R.; PASON, P.; TACHAAPAIKOON, C.; KYU, K.L.; SAKKA, K.; KOSUGI, A.; MORI, Y. 2013. Paenibacillus curdlanolyticus strain b-6 multienzyme complex: a novel system for biomass utilization. En: Matovic, M.D (ed.). Biomass Now - Cultivation and Utilization. IntechOpen https://doi.org/10.5772/51820
MAAS, L.K.; GLASS, T.L. 1991. Celobiose uptake by the cellulolytic ruminal anaerobe Fibrobacter (Bacteroides) succinogenes. Can. J. Microbiol. (Canadá). 37(1):141-147. https://doi.org/10.1139/m91-021
LIU, L.; ZHUGE, X.; SHIN, H.D.; CHEN, R.R.; LI, J.; DU, G.; CHEN, J. 2015. Improved production of propionic acid in Propionibacterium jensenii via combinational overexpression of glycerol dehydrogenase and malate dehydrogenase from klebsiella pneumoniae. Applied and Environmental Microbiology (Estados Unidos). 81(7):2256-2264. https://doi.org/10.1128/AEM.03572-14
LEIGHTON, B.; NICHOLAS, A.R.; POGSON, C.I. 1983. The pathway of ketogenesis in rumen epithelium of the sheep. The Biochemical J. (Inglaterra). 216(3):769-772. https://doi.org/10.1042/bj2160769
LANGIN, D. 2006. Control of fatty acid and glycerol release in adipose tissue lipolysis. Comptes Rendus - Biologies (Francia). 329(8):598-607. https://doi.org/10.1016/j.crvi.2005.10.008
KRISTENSEN, N.B.; HUNTINGTON, G.B.; HARMON, D.L. 2005. Splanchnic carbohydrate and energy metabolism in growing ruminants. In: Burrin D.G.; Mersman H.J. (eds.). Biology of Growing Animals p.405-432. Boston. https://doi.org/10.1016/S1877-1823(09)70024-4
KOHO, N.; MAIJALA, V.; NORBERG, H.; NIEMINEN, M.; PÖSÖ, A.R. 2005. Expression of mct1, mct2 and mct4 in the rumen, small intestine and liver of reindeer (Rangifer tarandus tarandus L.). Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology (Holanda). 141(1):29-34. https://doi.org/10.1016/j.cbpb.2005.03.003
KIRAT, D.; MATSUDA, Y.; YAMASHIKI, N.; HAYASHI, H.; KATO, S. 2007. Expression, cellular localization, and functional role of monocarboxylate transporter 4 (mct4) in the gastrointestinal tract of ruminants. Gene (Holanda). 391(1-2):140-149. https://doi.org/10.1016/j.gene.2006.12.020
KIRAT, D.; MASUOKA, J.; HAYASHI, H.; IWANO, H.; YOKOTA, H.; TANIYAMA, H.; KATO, S. 2006. Monocarboxylate transporter 1 (mct1) plays a direct role in short-chain fatty acids absorption in caprine rumen. J. Physiology (Estados Unidos). 576(2):635-647. https://doi.org/10.1113/jphysiol.2006.115931
KATO, D.; SUZUKI, Y.; SATOSHI, H.; HAGA, S.; SO, K.; YAMAUCHI, E.; NAKANO, M; ISHIZAKI, H.; CHOI, K.; KATOH, K., ROH, S. 2015. Utilization of digital differential display to identify differentially expressed genes related to rumen development. Animal Science Journal. 87(4):584-590. https://doi.org/10.1111/asj.12448
JIANG, W.; PINDER, R.S.; PATTERSON, J.A.; RICKE, S.C. 2014. Sugar phosphorylation activity in ruminal acetogens. J. Environmental Science and Health (Estados Unidos). 18(25):37-41. https://doi.org/10.1080/10934529.2012.664998
HERDT, T.H. 2000. Ruminant adaptation to negative energy balance. Veterinary Clinics of North America: Food Animal Practice (Estados Unidos). 16(2):215–230. https://doi.org/10.1016/s0749-0720(15)30102-x
PRATTI DANIEL, J.L.; RESENDE JÚNIOR, J.C.; CRUZ, F.J. 2006. Participação do ruminoretículo e omaso na superfície absortiva total do proventrículo de bovinos. Brazilian J. Veterinary Research and Animal Science (Brasil). 43(5):688-694. https://doi.org/10.11606/issn.1678-4456.bjvras.2006.26579
SANGALLI, J.; SAMPAIO, R.V.; DEL COLLADO, J.; COELHO DA SILVEIRA, J.; CAMARA DE BEM, T.H.; PERECIN, F.; SMITH, L.C.; VIEIRA MEIRELLES, F. 2018. Metabolic gene expression and epigenetic effects of the ketone body β-hydroxybutyrate on h3k9ac in bovine cells, oocytes and embryos. Scientific Reports (Estados Unidos). 8(1):1-18. https://doi.org/10.1038/s41598-018-31822-7
HACKMANN, T.J.; NGUGI, D.K.; FIRKINS, J.L.; TAO, J. 2017. Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short- chain fatty acids Tim. Environmental Microbiology (Estados Unidos), 19(11):4670-4683. https://doi.org/10.1111/1462-2920.13929
XIANG, E.; HUTTON ODDY, V.; ARCHIBALD, A.L.; VERCOE, P.E.; DALRYMPLE, B.P. 2016. Epithelial, metabolic and innate immunity transcriptomic signatures differentiating the rumen from other sheep and mammalian gastrointestinal tract tissues. PeerJ (Estados Unidos). 4:e1762. https://doi.org/10.7717/peerj.1762
Text
http://purl.org/coar/access_right/c_abf2
info:eu-repo/semantics/openAccess
http://purl.org/coar/version/c_970fb48d4fbd8a85
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_1843
http://purl.org/coar/resource_type/c_6501
info:eu-repo/semantics/article
ZHANG, J.; TAN, J.; ZHANG, C.; WANG, Y.; CHEN, X.; LEI, C.; CHEN, H.; FANG, X. 2019. Research on associations between variants and haplotypes of aquaporin 9 (aqp9) gene with growth traits in three cattle breeds. Animal Biotechnology (Inglaterra). https://doi.org/10.1080/10495398.2019.1675681
XU, W.; VERVOORT, J.; SACCENTI, E.; VAN HOEIJ, R.; KEMP, B.; VAN KNEGSEL, A. 2018. Milk metabolomics data reveal the energy balance of individual dairy cows in early lactation. Scientific Reports (Estados Unidos). 8(1):1-11. https://doi.org/10.1038/s41598-018-34190-4
XU, S.; WU, Z.; ZOU, Y.; LI, S.; CAO, Z. 2017. Evaluation of a hand-held meter to detect subclinical ketosis in dairy cows. Advances in Dairy Research (Estados Unidos). 5(2):2-5. https://doi.org/10.4172/2329-888x.1000173
WONGKITTICHOTE, P.; MEW, N.A.; CHAPMAN, K.A. 2017. Propionyl-CoA carboxylase–a review. Molecular genetics and metabolism. 122(4):145-152. https://doi.org/10.1016/j.ymgme.2017.10.002
SMITH, B.P. 2013. Large animal internal medicine. Eds. Elsevier (Estados Unidos). 1661p.
WHITE, H.M.; KOSER, S.L.; DONKIN, S.S. 2012. Gluconeogenic enzymes are differentially regulated by fatty acid cocktails in madin-darby bovine kidney cells 1. J. Dairy Science (Estados Unidos). 95(3):1249-1256. https://doi.org/10.3168/jds.2011-4644
WHITE, D.; DRUMMOND, J.; FUQUA, C. 2012. The physiology and biochemistry of prokaryotes. Eds. Oxford University Press (Estados Unidos). 632p.
WEIGAND, E.; YOUNG, J.W.; MCGILLIARD, A.D. 1975. Volatile fatty acid metabolism by rumen mucosa from cattle fed hay or grain. J. Dairy Science (Estados Unidos). 58(9):1294-1300. https://doi.org/10.3168/jds.s0022-0302(75)84709-6
WEI, Y.; LI, X.; ZHANG, D.; YONGFENG, L. 2019. Comparison of protein differences between high- and low-quality goat and bovine parts based on iTRAQ technology. Food Chemistry (Holanda). 289(3):240-249. https://doi.org/10.1016/j.foodchem.2019.03.052
WEBSTER, L.T.; GEROWIN, J.L.; RAKITA, L. 1965. Purification and characteristics of a butyryl coenzime a synthetase from bovine heart mitocondria. The Journal of Biological Chemistry (Estados Unidos). 240(1):29-33.
WATFORD, M.; HOD, Y.; CHIAO, Y.; UTTER, F.; HANSON, R.W. 1981. The unique role of the kidney in gluconeogenesis in the chicken. The J. Biological Chemistry (Estados Unidos). 256(19):10023-10027. Disponible desde Internet en: https://www.jbc.org/content/256/19/10023.long
WANG, L.; ZHANG, G.; LI, Y.; ZHANG, Y. 2020. Effects of high forage/concentrate diet on volatile fatty acid production and the microorganisms involved in vfa production in cow rumen. Animals (Inglaterra), 10(2):223. https://doi.org/10.3390/ani10020223
VITAL, M.; CHUANG HOWE, A.; TIEDJE, J.M. 2014. Revealing the bacterial butyrate synthesis pathways by analyzing (Meta) Genomic Data. American Society for Microbiology (Estados Unidos). 5(2):1-11. https://doi.org/10.1128/mBio.00889-14
VAN LINGEN, H.J.; PLUGGE, C.M.; FADEL, J.G.; KEBREAB, E. 2016. Thermodynamic driving force of hydrogen on rumen microbial metabolism: a theoretical investigation. PLoS ONE (Estados Unidos). 11(10):1-18. https://doi.org/10.1371/journal.pone.0161362
VAIDYA, J.D.; HORNUNG, B.V.H.; SMIDT, H.; EDWARDS, J.E.; PLUGGE, C.M. 2019. Propionibacterium ruminifibrarum sp. nov., isolated from cow rumen fibrous content. Internal J. Systematic and Evolutionary Microbiology (Inglaterra). 69(8):2584-2590. https://doi.org/https://doi.org/10.1099/ijsem.0.003544
STORM, A.C.; KRISTENSEN, N.B.; HANIGAN, M.D. 2012. A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating holstein cows. J. Dairy Science (Estados Unidos). 95(6):2919-2934. https://doi.org/10.3168/jds.2011-4239
HEITMANN, R.N.; DAWES, D.J.; SENSENIG, S.C. 1987. Hepatic ketogenesis and peripheral ketone body utilization in the ruminant. The Journal of Nutrition (Inglaterra). 117(6):1174-1180. https://doi.org/10.1093/jn/117.6.1174
HARFOOT, C.G. 1981. Lipid metabolism in the rumen. En: Lipid metabolism in ruminant animals. Pergamon. p. 21-55.
HACKMANN, T.J.; FIRKINS, J.L. 2015. Electron transport phosphorylation in rumen butyrivibrios: unprecedented atp yield for glucose fermentation to butyrate. Frontiers in Microbiology (Estados Unidos). 6(1):1-11. https://doi.org/10.3389/fmicb.2015.00622
1
https://revistas.udca.edu.co/index.php/ruadc/article/view/1304
Revista U.D.C.A Actualidad & Divulgación Científica
Universidad de Ciencias Aplicadas y Ambientales U.D.C.A
application/pdf
application/xml
Artículo de revista
Núm. 1 , Año 2020 :Revista U.D.C.A Actualidad & Divulgación Científica. Enero-Junio
23
https://creativecommons.org/licenses/by-nc-sa/4.0/
vaca lechera
cuerpos cetónicos
cetosis
balance energético negativo
Olivera-Angel, Martha
Londoño-Vásquez, Daniela
Huertas-Molina, Oscar Felípe
La hipercetonemia o cetosis bovina es un desorden metabólico, que se caracteriza por el incremento patológico de cuerpos cetónicos (beta-hidroxibutirato (βHB), Acetoacetato (AcAc) y acetona) y ocurre en el periparto de vacas de leche. El origen primario de la enfermedad es el balance energético negativo (BEN), que puede ser desencadenado por el incremento excesivo de los requerimientos energéticos o la presentación de enfermedades posparto, resultando en la presentación de signos clínicos o disminución de la producción de leche. El objetivo de esta revisión consiste en describir, mediante un modelo, los procesos bioquímicos del rumen y los mecanismos fisiopatológicos, involucrados con incremento excesivo de los cuerpos cetónicos. En resumen, se realizó un modelo fisiológico uniendo literatura fragmentada, sobre la relación entre la función ruminal, hepática y la inducción de lipolisis e incremento de la actividad de Carnitil-Palmitoil transferasa-1 (CPT-1), cuyo resultado puede ser la producción excesiva de Acetil-CoA que, junto con la falta de propionato y oxalacetato (precursores de gluconeogénesis y ciclo de Krebs), dan lugar a la producción patológica de acetoacetato y beta-hidroxibutirato.
Español
Publication
Oscar Felípe Huertas Molina, Daniela Londoño Vásquez, Martha Olivera Angel - 2020
BRUSS, M.L. 2008. Lipids and ketones. En: Kaneko, J.; Harvey, J.; Bruss, M.L. (eds). Clinical Biochemistry of Domestic Animals. Ed. ElSEVIER (Estados unidos). p.81–115. https://doi.org/10.1016/B978-0-12-370491-7.00004-0
GARZÓN-AUDOR, A.M.; OLIVER-ESPINOSA, O.J. 2018. Incidencia y prevalencia de cetosis clínica y subclínica en ganado en pastoreo en el altiplano cundiboyacense, Colombia. CES Medicina Veterinaria Y Zootecnia (Colombia). 13(2):121-136. https://doi.org/10.21615/cesmvz.13.2.3
FRIGGENS, N.C.; BERG, P.; THEILGAARD, P.; KORSGAARD, I.R.; INGVARTSEN, K.L; LØVENDAHL, P.; JENSEN, J. 2007. Breed and parity effects on energy balance profiles through lactation: evidence of genetically driven body energy change. J. Dairy Science (Estados Unidos). 90(11):5291-5305. https://doi.org/10.3168/jds.2007-0173
FRANKLUNDT, C.V.; GLASS, T.L. 1987. Glucose uptake by the cellulolytic ruminal anaerobe bacteroides succinogenes. J. Bacteriology (Estados Unidos). 169(2):500-506.
ENGELKING, L.R. 2015. Textbook of veterinary physiological chemistry. Ed. Elsevier (Estados Unidos). 786p.
EMMANUEL, B.; MILLIGAN, L.P. 1983. Butyrate: acetoacetyl-coa transferase activity in bovine rumen epithelium. Canadian J. Animal Science. 63(1):355-360. https://doi.org/10.4141/cjas83-043
EMMANUEL, B. 1981. Further metabolic studies in the rumen epithelium of camel (camelus dromedarius) and sheep (ovis aries). Comparative Biochemistry and Physiology Part B: Comparative Biochemistry. 68(1):155-158. https://doi.org/10.1016/0305-0491(81)90196-6
EMMANUEL, B. 1980. Oxidation of butyrate to ketone bodies and CO2 in the rumen epithelium, liver, kidney, heart and lung of camel (camelus dromedarius), sheep (ovis aries) and goat (carpa hircus). Comparative Biochemistry and Physiology -- Part B: Biochemistry and molecular biology (Holanda), 65(4):699-704. https://doi.org/10.1016/0305-0491(80)90182-0
DUFFIELD, T.F.; LISSEMORE, K.D.; MCBRIDE, B.W.; LESLIE, K.E. 2009. Impact of hyperketonemia in early lactation dairy cows on health and production. Journal of Dairy Science (Estados Unidos). 92(2):571-580. https://doi.org/10.3168/jds.2008-1507
DIJKSTRA, J.; ELLIS, J.L.; KEBREAB, E.; STRATHE, A.B.; LÓPEZ, S.; FRANCE, J.; BANNINK, A. 2012. Ruminal ph regulation and nutritional consequences of low pH. Animal Feed Science and Technology (Estados Unidos). 172(1-2):22-33. https://doi.org/10.1016/j.anifeedsci.2011.12.005
ALUWONG, T.; KOBO, P.I.; ABDULLAHI, A. 2010. Volatile fatty acids production in ruminants and the role of monocarboxylate transporters: a review. African Journal of Biotechnology. 9(38):6229-6232.
CHANDLER, T.L.; PRALLE, R.S.; DÓREA, J.R.R.; POOCK, S.E.; OETZEL, G.R.; FOURDRAINE, R.H.; WHITE, H.M. 2017. Predicting hyperketonemia by logistic and linear regression using test-day milk and performance variables in early-lactation holstein and jersey cows. J. Dairy Science (Estados Unidos). 101(3):2476-2491. https://doi.org/10.3168/jds.2017-13209
CHURCH, D.C. 1993. El rumiante: Fisiología Digestiva Y Nutrición. Ed. Acribia S.A (España). 652p.
ASCHENBACH, J.R.; KRISTENSEN, N.B.; DONKIN, S.S.; HAMMON, H.M.; PENNER, G.B. 2010. Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life (Estados Unidos). 62(12):869-877. https://doi.org/10.1002/iub.400
ANTANAITIS, R.; JUOZAITIEN, V.; TELEVI, M.; MALAŠAUSKIEN, D. 2018. Changes in the real-time registration of milk β -hydroxybutyrate according to stage and lactation number, milk yield, and status of reproduction in dairy cows. Polish J. Veterinary Sciences (Polonia). 21(4):763-768. https://doi.org/10.24425/pjvs.2018.125589
BALDWIN, R.L.; JESSE, B.W. 1996. Propionate modulation of ruminal ketogenesis. J. Animal Science. 74(7):1694-1700. https://doi.org/10.2527/1996.7471694x
BALDWIN, R.L.; JESSE, B.W. 1991. Technical note: isolation and characterization of sheep ruminal epithelial cells. J. Animal Science (Inglaterra), 69(9):3603-3609. https://doi.org/10.2527/1991.6993603x
BALDWIN, R.L.; CONNOR, E.E. 2017. Rumen function and development. Veterinary Clinics of North America - Food Animal Practice (Norte América). 33(3):427-439. https://doi.org/10.1016/j.cvfa.2017.06.001
BALDWIN, R.L. 1998. Use of isolated ruminal epithelial cells in the study of rumen metabolism. The Journal of Nutrition (Inglaterra), 128:293S-296S. https://doi.org/10.1093/jn/128.2.293s
Bovine hyperketonemia or ketosis is a metabolic disorder characterized by high levels of ketone bodies (beta-hydroxybutyrate (βHB), Acetoacetate (AcAc), and acetone) in periparturient dairy cows. A Negative Energy Balance (NEB) is identified as the primary cause of the disease, which is triggered by the excessive increase of energy requirements or the presence of postpartum diseases, resulting in the appearance of clinical signs or decreased milk production. The purpose of this review is to describe the rumen’s biochemical Process and the physiopathological mechanisms involved in the excessive production of ketone bodies. After conducting a literature review, a physiological model was carried out in order to understand the relationship between the rumen and liver functions with lipolysis induction and increased CPT-1 activity. The above may result in the overproduction of Acetyl-CoA, which together, with the lack of propionate and oxaloacetate (gluconeogenesis and Krebs cycle precursors), leads to the pathological production of acetoacetate and beta-hydroxybutyrate.
dairy cattle
ketone bodies
ketosis
negative energy balance
Journal article
Hyperketonemia: Biochemistry of volatile fatty acid production and its hepatic metabolism
2020-06-30T00:00:00Z
https://doi.org/10.31910/rudca.v23.n1.2020.1304
10.31910/rudca.v23.n1.2020.1304
https://revistas.udca.edu.co/index.php/ruadc/article/download/1304/1923
2619-2551
https://revistas.udca.edu.co/index.php/ruadc/article/download/1304/1929
2020-06-30
2020-06-30T00:00:00Z
0123-4226
institution UNIVERSIDAD DE CIENCIAS APLICADAS Y AMBIENTALES
thumbnail https://nuevo.metarevistas.org/UNIVERSIDADDECIENCIASAPLICADASYAMBIENTALES/logo.png
country_str Colombia
collection Revista U.D.C.A Actualidad & Divulgación Científica
title Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
spellingShingle Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
Olivera-Angel, Martha
Londoño-Vásquez, Daniela
Huertas-Molina, Oscar Felípe
vaca lechera
cuerpos cetónicos
cetosis
balance energético negativo
dairy cattle
ketone bodies
ketosis
negative energy balance
title_short Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
title_full Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
title_fullStr Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
title_full_unstemmed Hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
title_sort hipercetonemia: bioquímica de la producción de ácidos grasos volátiles y su metabolismo hepático
title_eng Hyperketonemia: Biochemistry of volatile fatty acid production and its hepatic metabolism
description La hipercetonemia o cetosis bovina es un desorden metabólico, que se caracteriza por el incremento patológico de cuerpos cetónicos (beta-hidroxibutirato (βHB), Acetoacetato (AcAc) y acetona) y ocurre en el periparto de vacas de leche. El origen primario de la enfermedad es el balance energético negativo (BEN), que puede ser desencadenado por el incremento excesivo de los requerimientos energéticos o la presentación de enfermedades posparto, resultando en la presentación de signos clínicos o disminución de la producción de leche. El objetivo de esta revisión consiste en describir, mediante un modelo, los procesos bioquímicos del rumen y los mecanismos fisiopatológicos, involucrados con incremento excesivo de los cuerpos cetónicos. En resumen, se realizó un modelo fisiológico uniendo literatura fragmentada, sobre la relación entre la función ruminal, hepática y la inducción de lipolisis e incremento de la actividad de Carnitil-Palmitoil transferasa-1 (CPT-1), cuyo resultado puede ser la producción excesiva de Acetil-CoA que, junto con la falta de propionato y oxalacetato (precursores de gluconeogénesis y ciclo de Krebs), dan lugar a la producción patológica de acetoacetato y beta-hidroxibutirato.
description_eng Bovine hyperketonemia or ketosis is a metabolic disorder characterized by high levels of ketone bodies (beta-hydroxybutyrate (βHB), Acetoacetate (AcAc), and acetone) in periparturient dairy cows. A Negative Energy Balance (NEB) is identified as the primary cause of the disease, which is triggered by the excessive increase of energy requirements or the presence of postpartum diseases, resulting in the appearance of clinical signs or decreased milk production. The purpose of this review is to describe the rumen’s biochemical Process and the physiopathological mechanisms involved in the excessive production of ketone bodies. After conducting a literature review, a physiological model was carried out in order to understand the relationship between the rumen and liver functions with lipolysis induction and increased CPT-1 activity. The above may result in the overproduction of Acetyl-CoA, which together, with the lack of propionate and oxaloacetate (gluconeogenesis and Krebs cycle precursors), leads to the pathological production of acetoacetate and beta-hydroxybutyrate.
author Olivera-Angel, Martha
Londoño-Vásquez, Daniela
Huertas-Molina, Oscar Felípe
author_facet Olivera-Angel, Martha
Londoño-Vásquez, Daniela
Huertas-Molina, Oscar Felípe
topicspa_str_mv vaca lechera
cuerpos cetónicos
cetosis
balance energético negativo
topic vaca lechera
cuerpos cetónicos
cetosis
balance energético negativo
dairy cattle
ketone bodies
ketosis
negative energy balance
topic_facet vaca lechera
cuerpos cetónicos
cetosis
balance energético negativo
dairy cattle
ketone bodies
ketosis
negative energy balance
citationvolume 23
citationissue 1
citationedition Núm. 1 , Año 2020 :Revista U.D.C.A Actualidad & Divulgación Científica. Enero-Junio
publisher Universidad de Ciencias Aplicadas y Ambientales U.D.C.A
ispartofjournal Revista U.D.C.A Actualidad & Divulgación Científica
source https://revistas.udca.edu.co/index.php/ruadc/article/view/1304
language Español
format Article
rights http://purl.org/coar/access_right/c_abf2
info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/4.0/
Oscar Felípe Huertas Molina, Daniela Londoño Vásquez, Martha Olivera Angel - 2020
references MANN, S.; YEPES, F.A.L.; BEHLING-KELLY, E.; MCART, J.A.A. 2017. The effect of different treatments for early-lactation hyperketonemia on blood β-hydroxybutyrate, plasma nonesterified fatty acids, glucose, insulin, and glucagon in dairy cattle. J. Dairy Science (Estados Unidos), 100(8):6470-6482. https://doi.org/10.3168/jds.2016-12532
PRATTI DANIEL, J.L.; RESENDE JÚNIOR, J.C. 2012. Absorção e metabolismo de ácidos graxos voláteis pelo rúmen e omaso. Ciencia E Agrotecnologia (Brasil). 36(1):93-99. https://doi.org/10.1590/S1413-70542012000100012
PRATAMA, R.; ARTIKA, I.M.; CHAIDAMSARI, T.; SUGIARTI, H.; PUTRA, S.M. 2014. Isolation and molecular cloning of cellulase gene from bovine rumen bacteria. Current Biochemistry (Indonesia). 1(1):29-36. https://doi.org/10.29244/cb.1.1.29-36
PABON, M. 2004. Notas de clase. Bioquímica ruminal. Ed. Universidad Nacional de Colombia (Bogotá D.C). 50p.
NOCEK, J.E.; HERBEIN, J.H.; POLAN, C.E. 1980. Influence of ration physical form, ruminal degradable nitrogen and age on rumen epithelial propionate and acetate transport and some enzymatic activities. The J. Nutrition (Inglaterra). 110(12):2355-2364. https://doi.org/10.1093/jn/110.12.2355
NIELSEN, L.; GONZALEZ-GARCIA, R.; MARCELLIN, E.; NAVONE, L.; STOWERS, C.; MCCUBBIN, T. 2017. Microbial propionic acid production. Fermentation (Estados Unidos). 3(2):21. https://doi.org/10.3390/fermentation3020021
NAKAMURA, S.; HAGA, S.; KIMURA, K.; MATSUYAMA, S. 2018. Propionate and butyrate induce gene expression of monocarboxylate transporter 4 and cluster of differentiation 147 in cultured rumen epithelial cells derived from preweaning dairy calves. Journal of Animal Science (Inglaterra). 96(11):4902-4911. https://doi.org/10.1093/jas/sky334
MURRAY, R.; BENDER, D.; BOTHAM, K.L.; KENNELLY, P.J.; RODWELL, V.W.; WEIL P.A. 2012. Bioquímica ilustrada harper. Ed. McGrawHill (Estados Unidos). 480p.
MILLEN, D.D.; ARRIGONI, M.D.B.; DIAS, R. 2016. Rumenology. Ed. Springer L. (Brasil). 314p.
MIAO, L.; YANG, Y.; LIU, Y.; LAI, L.; WANG, L.; ZHAN, Y.; YIN, R.; YU, M.; LI, CH.; YANG, X.; GE, C. 2019. Glycerol kinase interacts with nuclear receptor nr4a1 and regulates glucose metabolism in the liver. FASEB J.Official Publication of the Federation of American Societies for Experimental Biology (Estados Unidos). 33(6):6736-6747. https://doi.org/10.1096/fj.201800945RR
MATSUMOTO, H.; SASAKI, K.; BESSHO, T.; KOBAYASHI, E.; ABE, T.; SASAZAKI, S.; OYAMA, K.; MANNEN, H. 2012. The snps in the acaca gene are effective on fatty acid composition in Holstein milk. Molecular Biology Reports (Suiza). 39(9):8637-8644. https://doi.org/10.1007/s11033-012-1718-5
MADRESEH-GHAHFAROKHI, S.; DEHGHANI-SAMANI, A.; DEHGHANI-SAMANI, A. 2018. Ketosis (acetonaemia) in dairy cattle farms: practical guide based on importance, diagnosis, prevention and treatments. J. Dairy, Veterinary & Animal Research (Hungría), 7(6):299-302. doi.org/10.15406/jdvar.2018.07.00230
RATANAKHANOKCHAI, K.; WAEONUKUL, R.; PASON, P.; TACHAAPAIKOON, C.; KYU, K.L.; SAKKA, K.; KOSUGI, A.; MORI, Y. 2013. Paenibacillus curdlanolyticus strain b-6 multienzyme complex: a novel system for biomass utilization. En: Matovic, M.D (ed.). Biomass Now - Cultivation and Utilization. IntechOpen https://doi.org/10.5772/51820
MAAS, L.K.; GLASS, T.L. 1991. Celobiose uptake by the cellulolytic ruminal anaerobe Fibrobacter (Bacteroides) succinogenes. Can. J. Microbiol. (Canadá). 37(1):141-147. https://doi.org/10.1139/m91-021
LIU, L.; ZHUGE, X.; SHIN, H.D.; CHEN, R.R.; LI, J.; DU, G.; CHEN, J. 2015. Improved production of propionic acid in Propionibacterium jensenii via combinational overexpression of glycerol dehydrogenase and malate dehydrogenase from klebsiella pneumoniae. Applied and Environmental Microbiology (Estados Unidos). 81(7):2256-2264. https://doi.org/10.1128/AEM.03572-14
LEIGHTON, B.; NICHOLAS, A.R.; POGSON, C.I. 1983. The pathway of ketogenesis in rumen epithelium of the sheep. The Biochemical J. (Inglaterra). 216(3):769-772. https://doi.org/10.1042/bj2160769
LANGIN, D. 2006. Control of fatty acid and glycerol release in adipose tissue lipolysis. Comptes Rendus - Biologies (Francia). 329(8):598-607. https://doi.org/10.1016/j.crvi.2005.10.008
KRISTENSEN, N.B.; HUNTINGTON, G.B.; HARMON, D.L. 2005. Splanchnic carbohydrate and energy metabolism in growing ruminants. In: Burrin D.G.; Mersman H.J. (eds.). Biology of Growing Animals p.405-432. Boston. https://doi.org/10.1016/S1877-1823(09)70024-4
KOHO, N.; MAIJALA, V.; NORBERG, H.; NIEMINEN, M.; PÖSÖ, A.R. 2005. Expression of mct1, mct2 and mct4 in the rumen, small intestine and liver of reindeer (Rangifer tarandus tarandus L.). Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology (Holanda). 141(1):29-34. https://doi.org/10.1016/j.cbpb.2005.03.003
KIRAT, D.; MATSUDA, Y.; YAMASHIKI, N.; HAYASHI, H.; KATO, S. 2007. Expression, cellular localization, and functional role of monocarboxylate transporter 4 (mct4) in the gastrointestinal tract of ruminants. Gene (Holanda). 391(1-2):140-149. https://doi.org/10.1016/j.gene.2006.12.020
KIRAT, D.; MASUOKA, J.; HAYASHI, H.; IWANO, H.; YOKOTA, H.; TANIYAMA, H.; KATO, S. 2006. Monocarboxylate transporter 1 (mct1) plays a direct role in short-chain fatty acids absorption in caprine rumen. J. Physiology (Estados Unidos). 576(2):635-647. https://doi.org/10.1113/jphysiol.2006.115931
KATO, D.; SUZUKI, Y.; SATOSHI, H.; HAGA, S.; SO, K.; YAMAUCHI, E.; NAKANO, M; ISHIZAKI, H.; CHOI, K.; KATOH, K., ROH, S. 2015. Utilization of digital differential display to identify differentially expressed genes related to rumen development. Animal Science Journal. 87(4):584-590. https://doi.org/10.1111/asj.12448
JIANG, W.; PINDER, R.S.; PATTERSON, J.A.; RICKE, S.C. 2014. Sugar phosphorylation activity in ruminal acetogens. J. Environmental Science and Health (Estados Unidos). 18(25):37-41. https://doi.org/10.1080/10934529.2012.664998
HERDT, T.H. 2000. Ruminant adaptation to negative energy balance. Veterinary Clinics of North America: Food Animal Practice (Estados Unidos). 16(2):215–230. https://doi.org/10.1016/s0749-0720(15)30102-x
PRATTI DANIEL, J.L.; RESENDE JÚNIOR, J.C.; CRUZ, F.J. 2006. Participação do ruminoretículo e omaso na superfície absortiva total do proventrículo de bovinos. Brazilian J. Veterinary Research and Animal Science (Brasil). 43(5):688-694. https://doi.org/10.11606/issn.1678-4456.bjvras.2006.26579
SANGALLI, J.; SAMPAIO, R.V.; DEL COLLADO, J.; COELHO DA SILVEIRA, J.; CAMARA DE BEM, T.H.; PERECIN, F.; SMITH, L.C.; VIEIRA MEIRELLES, F. 2018. Metabolic gene expression and epigenetic effects of the ketone body β-hydroxybutyrate on h3k9ac in bovine cells, oocytes and embryos. Scientific Reports (Estados Unidos). 8(1):1-18. https://doi.org/10.1038/s41598-018-31822-7
HACKMANN, T.J.; NGUGI, D.K.; FIRKINS, J.L.; TAO, J. 2017. Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short- chain fatty acids Tim. Environmental Microbiology (Estados Unidos), 19(11):4670-4683. https://doi.org/10.1111/1462-2920.13929
XIANG, E.; HUTTON ODDY, V.; ARCHIBALD, A.L.; VERCOE, P.E.; DALRYMPLE, B.P. 2016. Epithelial, metabolic and innate immunity transcriptomic signatures differentiating the rumen from other sheep and mammalian gastrointestinal tract tissues. PeerJ (Estados Unidos). 4:e1762. https://doi.org/10.7717/peerj.1762
ZHANG, J.; TAN, J.; ZHANG, C.; WANG, Y.; CHEN, X.; LEI, C.; CHEN, H.; FANG, X. 2019. Research on associations between variants and haplotypes of aquaporin 9 (aqp9) gene with growth traits in three cattle breeds. Animal Biotechnology (Inglaterra). https://doi.org/10.1080/10495398.2019.1675681
XU, W.; VERVOORT, J.; SACCENTI, E.; VAN HOEIJ, R.; KEMP, B.; VAN KNEGSEL, A. 2018. Milk metabolomics data reveal the energy balance of individual dairy cows in early lactation. Scientific Reports (Estados Unidos). 8(1):1-11. https://doi.org/10.1038/s41598-018-34190-4
XU, S.; WU, Z.; ZOU, Y.; LI, S.; CAO, Z. 2017. Evaluation of a hand-held meter to detect subclinical ketosis in dairy cows. Advances in Dairy Research (Estados Unidos). 5(2):2-5. https://doi.org/10.4172/2329-888x.1000173
WONGKITTICHOTE, P.; MEW, N.A.; CHAPMAN, K.A. 2017. Propionyl-CoA carboxylase–a review. Molecular genetics and metabolism. 122(4):145-152. https://doi.org/10.1016/j.ymgme.2017.10.002
SMITH, B.P. 2013. Large animal internal medicine. Eds. Elsevier (Estados Unidos). 1661p.
WHITE, H.M.; KOSER, S.L.; DONKIN, S.S. 2012. Gluconeogenic enzymes are differentially regulated by fatty acid cocktails in madin-darby bovine kidney cells 1. J. Dairy Science (Estados Unidos). 95(3):1249-1256. https://doi.org/10.3168/jds.2011-4644
WHITE, D.; DRUMMOND, J.; FUQUA, C. 2012. The physiology and biochemistry of prokaryotes. Eds. Oxford University Press (Estados Unidos). 632p.
WEIGAND, E.; YOUNG, J.W.; MCGILLIARD, A.D. 1975. Volatile fatty acid metabolism by rumen mucosa from cattle fed hay or grain. J. Dairy Science (Estados Unidos). 58(9):1294-1300. https://doi.org/10.3168/jds.s0022-0302(75)84709-6
WEI, Y.; LI, X.; ZHANG, D.; YONGFENG, L. 2019. Comparison of protein differences between high- and low-quality goat and bovine parts based on iTRAQ technology. Food Chemistry (Holanda). 289(3):240-249. https://doi.org/10.1016/j.foodchem.2019.03.052
WEBSTER, L.T.; GEROWIN, J.L.; RAKITA, L. 1965. Purification and characteristics of a butyryl coenzime a synthetase from bovine heart mitocondria. The Journal of Biological Chemistry (Estados Unidos). 240(1):29-33.
WATFORD, M.; HOD, Y.; CHIAO, Y.; UTTER, F.; HANSON, R.W. 1981. The unique role of the kidney in gluconeogenesis in the chicken. The J. Biological Chemistry (Estados Unidos). 256(19):10023-10027. Disponible desde Internet en: https://www.jbc.org/content/256/19/10023.long
WANG, L.; ZHANG, G.; LI, Y.; ZHANG, Y. 2020. Effects of high forage/concentrate diet on volatile fatty acid production and the microorganisms involved in vfa production in cow rumen. Animals (Inglaterra), 10(2):223. https://doi.org/10.3390/ani10020223
VITAL, M.; CHUANG HOWE, A.; TIEDJE, J.M. 2014. Revealing the bacterial butyrate synthesis pathways by analyzing (Meta) Genomic Data. American Society for Microbiology (Estados Unidos). 5(2):1-11. https://doi.org/10.1128/mBio.00889-14
VAN LINGEN, H.J.; PLUGGE, C.M.; FADEL, J.G.; KEBREAB, E. 2016. Thermodynamic driving force of hydrogen on rumen microbial metabolism: a theoretical investigation. PLoS ONE (Estados Unidos). 11(10):1-18. https://doi.org/10.1371/journal.pone.0161362
VAIDYA, J.D.; HORNUNG, B.V.H.; SMIDT, H.; EDWARDS, J.E.; PLUGGE, C.M. 2019. Propionibacterium ruminifibrarum sp. nov., isolated from cow rumen fibrous content. Internal J. Systematic and Evolutionary Microbiology (Inglaterra). 69(8):2584-2590. https://doi.org/https://doi.org/10.1099/ijsem.0.003544
STORM, A.C.; KRISTENSEN, N.B.; HANIGAN, M.D. 2012. A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating holstein cows. J. Dairy Science (Estados Unidos). 95(6):2919-2934. https://doi.org/10.3168/jds.2011-4239
HEITMANN, R.N.; DAWES, D.J.; SENSENIG, S.C. 1987. Hepatic ketogenesis and peripheral ketone body utilization in the ruminant. The Journal of Nutrition (Inglaterra). 117(6):1174-1180. https://doi.org/10.1093/jn/117.6.1174
HARFOOT, C.G. 1981. Lipid metabolism in the rumen. En: Lipid metabolism in ruminant animals. Pergamon. p. 21-55.
HACKMANN, T.J.; FIRKINS, J.L. 2015. Electron transport phosphorylation in rumen butyrivibrios: unprecedented atp yield for glucose fermentation to butyrate. Frontiers in Microbiology (Estados Unidos). 6(1):1-11. https://doi.org/10.3389/fmicb.2015.00622
BRUSS, M.L. 2008. Lipids and ketones. En: Kaneko, J.; Harvey, J.; Bruss, M.L. (eds). Clinical Biochemistry of Domestic Animals. Ed. ElSEVIER (Estados unidos). p.81–115. https://doi.org/10.1016/B978-0-12-370491-7.00004-0
GARZÓN-AUDOR, A.M.; OLIVER-ESPINOSA, O.J. 2018. Incidencia y prevalencia de cetosis clínica y subclínica en ganado en pastoreo en el altiplano cundiboyacense, Colombia. CES Medicina Veterinaria Y Zootecnia (Colombia). 13(2):121-136. https://doi.org/10.21615/cesmvz.13.2.3
FRIGGENS, N.C.; BERG, P.; THEILGAARD, P.; KORSGAARD, I.R.; INGVARTSEN, K.L; LØVENDAHL, P.; JENSEN, J. 2007. Breed and parity effects on energy balance profiles through lactation: evidence of genetically driven body energy change. J. Dairy Science (Estados Unidos). 90(11):5291-5305. https://doi.org/10.3168/jds.2007-0173
FRANKLUNDT, C.V.; GLASS, T.L. 1987. Glucose uptake by the cellulolytic ruminal anaerobe bacteroides succinogenes. J. Bacteriology (Estados Unidos). 169(2):500-506.
ENGELKING, L.R. 2015. Textbook of veterinary physiological chemistry. Ed. Elsevier (Estados Unidos). 786p.
EMMANUEL, B.; MILLIGAN, L.P. 1983. Butyrate: acetoacetyl-coa transferase activity in bovine rumen epithelium. Canadian J. Animal Science. 63(1):355-360. https://doi.org/10.4141/cjas83-043
EMMANUEL, B. 1981. Further metabolic studies in the rumen epithelium of camel (camelus dromedarius) and sheep (ovis aries). Comparative Biochemistry and Physiology Part B: Comparative Biochemistry. 68(1):155-158. https://doi.org/10.1016/0305-0491(81)90196-6
EMMANUEL, B. 1980. Oxidation of butyrate to ketone bodies and CO2 in the rumen epithelium, liver, kidney, heart and lung of camel (camelus dromedarius), sheep (ovis aries) and goat (carpa hircus). Comparative Biochemistry and Physiology -- Part B: Biochemistry and molecular biology (Holanda), 65(4):699-704. https://doi.org/10.1016/0305-0491(80)90182-0
DUFFIELD, T.F.; LISSEMORE, K.D.; MCBRIDE, B.W.; LESLIE, K.E. 2009. Impact of hyperketonemia in early lactation dairy cows on health and production. Journal of Dairy Science (Estados Unidos). 92(2):571-580. https://doi.org/10.3168/jds.2008-1507
DIJKSTRA, J.; ELLIS, J.L.; KEBREAB, E.; STRATHE, A.B.; LÓPEZ, S.; FRANCE, J.; BANNINK, A. 2012. Ruminal ph regulation and nutritional consequences of low pH. Animal Feed Science and Technology (Estados Unidos). 172(1-2):22-33. https://doi.org/10.1016/j.anifeedsci.2011.12.005
ALUWONG, T.; KOBO, P.I.; ABDULLAHI, A. 2010. Volatile fatty acids production in ruminants and the role of monocarboxylate transporters: a review. African Journal of Biotechnology. 9(38):6229-6232.
CHANDLER, T.L.; PRALLE, R.S.; DÓREA, J.R.R.; POOCK, S.E.; OETZEL, G.R.; FOURDRAINE, R.H.; WHITE, H.M. 2017. Predicting hyperketonemia by logistic and linear regression using test-day milk and performance variables in early-lactation holstein and jersey cows. J. Dairy Science (Estados Unidos). 101(3):2476-2491. https://doi.org/10.3168/jds.2017-13209
CHURCH, D.C. 1993. El rumiante: Fisiología Digestiva Y Nutrición. Ed. Acribia S.A (España). 652p.
ASCHENBACH, J.R.; KRISTENSEN, N.B.; DONKIN, S.S.; HAMMON, H.M.; PENNER, G.B. 2010. Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life (Estados Unidos). 62(12):869-877. https://doi.org/10.1002/iub.400
ANTANAITIS, R.; JUOZAITIEN, V.; TELEVI, M.; MALAŠAUSKIEN, D. 2018. Changes in the real-time registration of milk β -hydroxybutyrate according to stage and lactation number, milk yield, and status of reproduction in dairy cows. Polish J. Veterinary Sciences (Polonia). 21(4):763-768. https://doi.org/10.24425/pjvs.2018.125589
BALDWIN, R.L.; JESSE, B.W. 1996. Propionate modulation of ruminal ketogenesis. J. Animal Science. 74(7):1694-1700. https://doi.org/10.2527/1996.7471694x
BALDWIN, R.L.; JESSE, B.W. 1991. Technical note: isolation and characterization of sheep ruminal epithelial cells. J. Animal Science (Inglaterra), 69(9):3603-3609. https://doi.org/10.2527/1991.6993603x
BALDWIN, R.L.; CONNOR, E.E. 2017. Rumen function and development. Veterinary Clinics of North America - Food Animal Practice (Norte América). 33(3):427-439. https://doi.org/10.1016/j.cvfa.2017.06.001
BALDWIN, R.L. 1998. Use of isolated ruminal epithelial cells in the study of rumen metabolism. The Journal of Nutrition (Inglaterra), 128:293S-296S. https://doi.org/10.1093/jn/128.2.293s
type_driver info:eu-repo/semantics/article
type_coar http://purl.org/coar/resource_type/c_1843
type_version info:eu-repo/semantics/publishedVersion
type_coarversion http://purl.org/coar/version/c_970fb48d4fbd8a85
type_content Text
publishDate 2020-06-30
date_accessioned 2020-06-30T00:00:00Z
date_available 2020-06-30T00:00:00Z
url https://revistas.udca.edu.co/index.php/ruadc/article/view/1304
url_doi https://doi.org/10.31910/rudca.v23.n1.2020.1304
issn 0123-4226
eissn 2619-2551
doi 10.31910/rudca.v23.n1.2020.1304
url4_str_mv https://revistas.udca.edu.co/index.php/ruadc/article/download/1304/1923
url2_str_mv https://revistas.udca.edu.co/index.php/ruadc/article/download/1304/1929
_version_ 1797159747751772160