Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.

The aimof this work was to develop a liver tissue function index during the transition period of dairy cows managed in low-tropic conditions. In two farms, twenty crossbred and synthetic native cows during the peripartumperiod were selected, and blood samples were taken on days −30 and −15 prepartum...

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Autores:
Rómulo Campos-Gaona
Adriana Correa-Orozco
Arcesio Salamanca-Carreño
Mauricio Vélez-Terranova
Tipo de recurso:
Article of investigation
Fecha de publicación:
2024
Institución:
Universidad Cooperativa de Colombia
Repositorio:
Repositorio UCC
Idioma:
eng
OAI Identifier:
oai:repository.ucc.edu.co:20.500.12494/56903
Acceso en línea:
https://hdl.handle.net/20.500.12494/56903
https://doi.org/10.3390/ani14142056
Palabra clave:
bovine
hepatic function index
metabolism
transition period
Rights
openAccess
License
http://creativecommons.org/licenses/by-nc-nd/4.0/
id COOPER2_29fd57555ef46e02d4884b20bcbc07e9
oai_identifier_str oai:repository.ucc.edu.co:20.500.12494/56903
network_acronym_str COOPER2
network_name_str Repositorio UCC
repository_id_str
dc.title.eng.fl_str_mv Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
title Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
spellingShingle Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
bovine
hepatic function index
metabolism
transition period
title_short Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
title_full Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
title_fullStr Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
title_full_unstemmed Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
title_sort Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.
dc.creator.fl_str_mv Rómulo Campos-Gaona
Adriana Correa-Orozco
Arcesio Salamanca-Carreño
Mauricio Vélez-Terranova
dc.contributor.author.none.fl_str_mv Rómulo Campos-Gaona
Adriana Correa-Orozco
Arcesio Salamanca-Carreño
Mauricio Vélez-Terranova
dc.contributor.researchgroup.none.fl_str_mv Los Araucos
dc.subject.proposal.eng.fl_str_mv bovine
hepatic function index
metabolism
transition period
topic bovine
hepatic function index
metabolism
transition period
description The aimof this work was to develop a liver tissue function index during the transition period of dairy cows managed in low-tropic conditions. In two farms, twenty crossbred and synthetic native cows during the peripartumperiod were selected, and blood samples were taken on days −30 and −15 prepartum, the calving day, and 7, 20, 35, 50, 65, 80 and 105 days postpartumfor serummetabolic tests. On eachmeasurement day, body condition scores (BCS) and parameters on nitrogenmetabolism(total protein—TP, albumin—ALB, globulin—GLOB, urea), adipose tissue metabolism (cholesterol—COL, nonesterified fatty acids—NEFA) and two transaminases (alanine aminotransferase—ALT and aspartate aminotransferase—AST) were evaluated. Data analysis included the Spearman correlation, principal components, multiple linear regression and cluster analysis. Results showed that regarding the days after calving and BCS, a liver tissue function index can be constructed using the TP, urea, COL, ALT and NEFA. The estimated index generated three groupings, both by days after calving and BCS. In the former, the index discriminated the metabolic behavior in the prepartum, parturition and postpartum periods, while in the latter, the index discriminated between extreme (2.25, 2.50 and 4.25), slightly low (2.75 and 3.0) and slightly high (3.25 to 4) conditions. The results allow us to conclude that it is feasible to construct mathematical function indexes for liver function to monitor metabolic changes during highly demanding productive phases in dairy cows under tropical conditions.
publishDate 2024
dc.date.accessioned.none.fl_str_mv 2024-08-13T22:08:23Z
dc.date.available.none.fl_str_mv 2024-08-13T22:08:23Z
dc.date.issued.none.fl_str_mv 2024-07-13
dc.type.none.fl_str_mv Artículo de revista
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dc.identifier.citation.none.fl_str_mv Campos-Gaona, R., Correa-Orozco, A., Salamanca-Carreño, A., Vélez-Terranova, M. 2024. Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions. Animals, 14 (14), 2056: 1-11.
dc.identifier.issn.none.fl_str_mv 2076-2615
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12494/56903
dc.identifier.doi.none.fl_str_mv https://doi.org/10.3390/ani14142056
dc.identifier.eissn.none.fl_str_mv 2076-2615
identifier_str_mv Campos-Gaona, R., Correa-Orozco, A., Salamanca-Carreño, A., Vélez-Terranova, M. 2024. Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions. Animals, 14 (14), 2056: 1-11.
2076-2615
url https://hdl.handle.net/20.500.12494/56903
https://doi.org/10.3390/ani14142056
dc.language.iso.none.fl_str_mv eng
language eng
dc.relation.citationendpage.none.fl_str_mv 11
dc.relation.citationissue.none.fl_str_mv 14
dc.relation.citationstartpage.none.fl_str_mv 1
dc.relation.citationvolume.none.fl_str_mv 14
dc.relation.ispartofjournal.none.fl_str_mv Animals
dc.relation.references.none.fl_str_mv White, H.M. ADSA Foundation Scholar Award: Influencing hepatic metabolism: Can nutrient partitioning be modulated to optimize metabolic health in the transition dairy cow? J. Dairy Sci. 2020, 103, 6741–6750. [CrossRef] [PubMed] 2. McCabe, C.J.; Boerman, J.P. Invited Review: Quantifying protein mobilization in dairy cows during the transition period. Appl. Anim. Sci. 2020, 36, 389–396. [CrossRef] 3. Baldacim, V.A.P.; Madureira, K.M.; Ramos, J.S.; Costa, C.P.; Mori, C.S.; Dias, M.R.B.; Gomes, V. Dynamic of metabolic indicators, insulin like-growth factor I (IGF-I) and cortisol in Holstein cows during the transition period. Acta Sci. Vet. 2018, 46, 8. 4. Schmitt, R.; Pieper, L.; Gonzalez-Grajales, L.A.; Swinkels, J.; Gelfert, C.C.; Staufenbiel, R. Evaluation of different acute-phase proteins for herd health diagnostics in early postpartum Holstein Friesian dairy cows. J. Dairy Res. 2021, 88, 33–37. [CrossRef] [PubMed] 5. Stevenson, J.S.; Banuelos, S.; Mendonça, L.G. Transition dairy cow health is associated with first postpartum ovulation risk, metabolic status, milk production, rumination, and physical activity. J. Dairy Sci. 2020, 103, 9573–9586. [CrossRef] [PubMed] 6. Banuelos, S.; Stevenson, J.S. Transition cow metabolites and physical traits influence days to first postpartum ovulation in dairy cows. Theriogenology 2021, 173, 133–143. [CrossRef] [PubMed] 7. Putman, A.K.; Brown, J.L.; Gandy, J.C.; Wisnieski, L.; Sordillo, L.M. Changes in biomarkers of nutrient metabolism, inflammation. and oxidative stress in dairy cows during the transition into the early dry period. J. Dairy Sci. 2018, 101, 9350–9359. [CrossRef] 8. Andjeli´c, B.; Djokovi´c, R.; Cincovic´, M.; Bogosavljevic´-Boškovic´, S.; Petrovic´, M.; Mladenovic´, J.; Cˇ ukic´, A. Relationships between milk and blood biochemical parameters and metabolic status in dairy cows during lactation. Metabolites 2022, 12, 733. [CrossRef] [PubMed] 9. González, F.D.; Muiño, R.; Pereira, V.; Campos, R.; Benedito, J.L. Relationship among blood indicators of lipomobilization and hepatic function during early lactation in high-yielding dairy cows. J. Vet. Sci. 2011, 12, 251–255. [CrossRef] 10. Stojevi´c, Z.; Piršljin, J.; Milinkovi´c-Tur, S.; Zdelar-Tuk, M.; Beer Ljubi´c, B. Activities of AST, ALT and GGT in clinically healthy dairy cows during lactation and in the dry period. Vet. Arh. 2005, 75, 67–73. 11. Allen, M.S. Control of feed intake by hepatic oxidation in ruminant animals: Integration of homeostasis and homeorhesis. Animals 2020, 14, s55–s64. [CrossRef] [PubMed] 12. Allen, M.S.; Bradford, B.J.; Oba, M. Board-invited review: The hepatic oxidation theory of the control of feed intake and its application to ruminants. J. Anim. Sci. 2009, 87, 3317–3334. [CrossRef] [PubMed] 13. Mordak, R.; Kupczy´ nski, R.; Kuczaj, M.; Ni˙za´ nski, W. Analysis of correlations between selected blood markers of liver function and milk composition in cows during late lactation period. Ann. Anim. Sci. 2020, 20, 871–886. [CrossRef] 14. Arshad, U.; Santos, J.E.P. Hepatic triacylglycerol associations with production and health in dairy cows. J. Dairy Sci. 2022, 105, 5393–5409. [CrossRef] [PubMed] 15. Bertoni, G.; Trevisi, E. Use of the liver activity index and other metabolic variables in the assessment of metabolic health in dairy herds. Vet. Clin. Food Anim. Pract. 2013, 29, 413–431. [CrossRef] [PubMed] 16. Nordlund, K. Transition cow index. In Proceedings of the 39th Proceedings American Association of Bovine Practitioners, St. Paul, MN, USA, 20–24 September 2006; pp. 139–143. 17. Lukas, J.M.; Reneau, J.K.;Wallace, R.L.; De Vries, A. A study of methods for evaluating the success of the transition period in early-lactation dairy cows. J. Dairy Sci. 2015, 98, 250–262. [CrossRef] [PubMed] 18. Soonberg, M.; Kass, M.; Kaart, T.; Barraclough, R.; Haskell, M.J.; Arney, D.R. Effect of grouping on behaviour of dairy heifers and cows in the transition period. J. Dairy Res. 2021, 88, 45–51. [CrossRef] [PubMed] 19. Sammad, A.; Khan, M.Z.; Abbas, Z.; Hu, L.; Ullah, Q.; Wang, Y.; Wang, Y. Major nutritional metabolic alterations influencing the reproductive system of postpartum dairy cows. Metabolites 2022, 12, 60. [CrossRef] [PubMed] 20. Gábor, G.; Balogh, O.G.; Kern, L.; Gábor, P.R.; Fébel, H. Nutrition. Metabolic Status and Reproductive Efficiency in Dairy Herds. Open J. Anim. Sci. 2016, 6, 75–84. [CrossRef] 21. Batista, C.P.; Castro Ruiz, S.M.; Correa Cardona, H.J.; Gonçalves, R.S.; Valle, S.D.F.; Diaz Gonzalez, F.H. Relation between liver lipid content and plasma biochemical indicators in dairy cows. Acta Sci. Vet. 2020, 48, 1–9. [CrossRef] 22. Paiano, R.B.; Birgel, D.B.; Bonilla, J.; Birgel Junior, E.H. Evaluation of biochemical profile of dairy cows with metabolic diseases in tropical conditions. Reprod. Dom. Anim. 2020, 55, 1219–1228. [CrossRef] [PubMed] 23. Holdridge, L.R. Ecología Basada em Zonas de Vida; Instituto Interamericano de Cooperación para la Agricultura: San José de Costa Rica, Costa Rica, 2000; p. 216. 24. Payne, J.M. The Compton metabolic profile test. Proc. R. Soc. Med. 1972, 64, 181–183. [CrossRef] 25. Roche, J.R.; Friggens, N.C.; Kay, J.K.; Fisher, M.W.; Stafford, K.J.; Berry, D.P. Invited review: Body condition score and its association with dairy cow productivity, health, and welfare. J. Dairy Sci. 2009, 92, 5769–5801. [CrossRef] [PubMed] Di Rienzo, J.A.; Casanoves, F.; Balzarini, M.G.; Gonzalez, L.A.; Tablada, E.M. InfoStat, Versión 2020. Universidad Nacional de Córdoba, Argentina. 2024. Available online: http://www.infostat.com.ar/index.php?mod=page&id=34 (accessed on 3 June 2024). 27. R Core Team. R: A Language and Environment for Statistical Computing. 2020. Available online: https://www.R-project.org/ (accessed on 3 June 2024). 28. Štolcová, D.; ˇ Rehák, D.; Barto ˇ n, L.; Rajmon, R. Štolcová. Blood biochemical parameters measured during the periparturient period in cows of Holstein and fleckvieh breeds differing in production purpose. Czech J. Anim. Sci. 2020, 65, 172–181. [CrossRef] 29. Djokovic, R.; Cincovic, M.; Ilic, Z.; Kurcubic, V.; Andjelic, B.; Petrovic, M.; Jasovic, B. Estimation metabolic status in high yielding dairy cows during transition period and full lactation. Acta Sci. Vet. 2019, 47, 1–6. [CrossRef] 30. Puppel, K.; Kuczy ´ nska, B. Metabolic profiles of cow’s blood; a review. J. Sci. Food Agric. 2016, 96, 4321–4328. [CrossRef] [PubMed] 31. Sun, B.F.; Cao, Y.C.; Cai, C.J.; Chao, Y.U.; Li, S.X.; Yao, J.H. Temporal dynamics of nutrient balance, plasma biochemical and immune traits, and liver function in transition dairy cows. J. Integr. Agric. 2020, 19, 820–837. [CrossRef] 32. García-Casillas, A.C.G.; Montiel-Ramos, L.A.M. Integración bioquímica para modelar las respuestas metabólicas en la producción láctea de bovinos lecheros. Soc. Rural. Prod. Medio Ambiente 2014, 12, 71–194. 33. Gerspach, C.; Imhasly, S.; Gubler, M.; Naegeli, H.; Ruetten, M.; Laczkó, E. Altered plasma lipidome profile of dairy cows with fatty liver disease. Res. Vet. Sci. 2017, 110, 47–59. [CrossRef] 34. Batista, C.P.; Gonçalves, R.S.; Contreras, L.V.Q.; de Faria Valle, S.; González, F. Correlation between liver lipidosis, body condition score variation. and hepatic analytes in dairy cows. Braz. J. Vet. Med. 2022, 44, e005121. [CrossRef] 35. Mezzetti, M.; Cattaneo, L.; Passamonti, M.M.; Lopreiato, V.; Minuti, A.; Trevisi, E. The transition period updated: A review of the new insights into the adaptation of dairy cows to the new lactation. Dairy 2021, 2, 617–636. [CrossRef] 36. Caixeta, L.S.; Omontese, B.O. Monitoring and improving the metabolic health of dairy cows during the transition period. Animals 2021, 11, 352. [CrossRef] [PubMed]
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spelling Rómulo Campos-GaonaAdriana Correa-OrozcoArcesio Salamanca-CarreñoMauricio Vélez-TerranovaLos Araucosinternacional, nacional2024-08-13T22:08:23Z2024-08-13T22:08:23Z2024-07-13Campos-Gaona, R., Correa-Orozco, A., Salamanca-Carreño, A., Vélez-Terranova, M. 2024. Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions. Animals, 14 (14), 2056: 1-11.2076-2615https://hdl.handle.net/20.500.12494/56903https://doi.org/10.3390/ani141420562076-2615The aimof this work was to develop a liver tissue function index during the transition period of dairy cows managed in low-tropic conditions. In two farms, twenty crossbred and synthetic native cows during the peripartumperiod were selected, and blood samples were taken on days −30 and −15 prepartum, the calving day, and 7, 20, 35, 50, 65, 80 and 105 days postpartumfor serummetabolic tests. On eachmeasurement day, body condition scores (BCS) and parameters on nitrogenmetabolism(total protein—TP, albumin—ALB, globulin—GLOB, urea), adipose tissue metabolism (cholesterol—COL, nonesterified fatty acids—NEFA) and two transaminases (alanine aminotransferase—ALT and aspartate aminotransferase—AST) were evaluated. Data analysis included the Spearman correlation, principal components, multiple linear regression and cluster analysis. Results showed that regarding the days after calving and BCS, a liver tissue function index can be constructed using the TP, urea, COL, ALT and NEFA. The estimated index generated three groupings, both by days after calving and BCS. In the former, the index discriminated the metabolic behavior in the prepartum, parturition and postpartum periods, while in the latter, the index discriminated between extreme (2.25, 2.50 and 4.25), slightly low (2.75 and 3.0) and slightly high (3.25 to 4) conditions. The results allow us to conclude that it is feasible to construct mathematical function indexes for liver function to monitor metabolic changes during highly demanding productive phases in dairy cows under tropical conditions.1-11application/pdfengMDPI (Suiza)http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessAttribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://purl.org/coar/access_right/c_abf2https://www.mdpi.com/2076-2615/14/14/2056Index Development to Comprehensive Assess Liver Function during the Dairy Cows’ Transition Period in Low-Tropic Conditions.Artículo de revistahttp://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articlehttp://purl.org/redcol/resource_type/ARTinfo:eu-repo/semantics/publishedVersion1114114AnimalsWhite, H.M. ADSA Foundation Scholar Award: Influencing hepatic metabolism: Can nutrient partitioning be modulated to optimize metabolic health in the transition dairy cow? J. Dairy Sci. 2020, 103, 6741–6750. [CrossRef] [PubMed] 2. McCabe, C.J.; Boerman, J.P. Invited Review: Quantifying protein mobilization in dairy cows during the transition period. Appl. Anim. Sci. 2020, 36, 389–396. [CrossRef] 3. Baldacim, V.A.P.; Madureira, K.M.; Ramos, J.S.; Costa, C.P.; Mori, C.S.; Dias, M.R.B.; Gomes, V. Dynamic of metabolic indicators, insulin like-growth factor I (IGF-I) and cortisol in Holstein cows during the transition period. Acta Sci. Vet. 2018, 46, 8. 4. Schmitt, R.; Pieper, L.; Gonzalez-Grajales, L.A.; Swinkels, J.; Gelfert, C.C.; Staufenbiel, R. Evaluation of different acute-phase proteins for herd health diagnostics in early postpartum Holstein Friesian dairy cows. J. Dairy Res. 2021, 88, 33–37. [CrossRef] [PubMed] 5. Stevenson, J.S.; Banuelos, S.; Mendonça, L.G. Transition dairy cow health is associated with first postpartum ovulation risk, metabolic status, milk production, rumination, and physical activity. J. Dairy Sci. 2020, 103, 9573–9586. [CrossRef] [PubMed] 6. Banuelos, S.; Stevenson, J.S. Transition cow metabolites and physical traits influence days to first postpartum ovulation in dairy cows. Theriogenology 2021, 173, 133–143. [CrossRef] [PubMed] 7. Putman, A.K.; Brown, J.L.; Gandy, J.C.; Wisnieski, L.; Sordillo, L.M. Changes in biomarkers of nutrient metabolism, inflammation. and oxidative stress in dairy cows during the transition into the early dry period. J. Dairy Sci. 2018, 101, 9350–9359. [CrossRef] 8. Andjeli´c, B.; Djokovi´c, R.; Cincovic´, M.; Bogosavljevic´-Boškovic´, S.; Petrovic´, M.; Mladenovic´, J.; Cˇ ukic´, A. Relationships between milk and blood biochemical parameters and metabolic status in dairy cows during lactation. Metabolites 2022, 12, 733. [CrossRef] [PubMed] 9. González, F.D.; Muiño, R.; Pereira, V.; Campos, R.; Benedito, J.L. Relationship among blood indicators of lipomobilization and hepatic function during early lactation in high-yielding dairy cows. J. Vet. Sci. 2011, 12, 251–255. [CrossRef] 10. Stojevi´c, Z.; Piršljin, J.; Milinkovi´c-Tur, S.; Zdelar-Tuk, M.; Beer Ljubi´c, B. Activities of AST, ALT and GGT in clinically healthy dairy cows during lactation and in the dry period. Vet. Arh. 2005, 75, 67–73. 11. Allen, M.S. Control of feed intake by hepatic oxidation in ruminant animals: Integration of homeostasis and homeorhesis. Animals 2020, 14, s55–s64. [CrossRef] [PubMed] 12. Allen, M.S.; Bradford, B.J.; Oba, M. Board-invited review: The hepatic oxidation theory of the control of feed intake and its application to ruminants. J. Anim. Sci. 2009, 87, 3317–3334. [CrossRef] [PubMed] 13. Mordak, R.; Kupczy´ nski, R.; Kuczaj, M.; Ni˙za´ nski, W. Analysis of correlations between selected blood markers of liver function and milk composition in cows during late lactation period. Ann. Anim. Sci. 2020, 20, 871–886. [CrossRef] 14. Arshad, U.; Santos, J.E.P. Hepatic triacylglycerol associations with production and health in dairy cows. J. Dairy Sci. 2022, 105, 5393–5409. [CrossRef] [PubMed] 15. Bertoni, G.; Trevisi, E. Use of the liver activity index and other metabolic variables in the assessment of metabolic health in dairy herds. Vet. Clin. Food Anim. Pract. 2013, 29, 413–431. [CrossRef] [PubMed] 16. Nordlund, K. Transition cow index. In Proceedings of the 39th Proceedings American Association of Bovine Practitioners, St. Paul, MN, USA, 20–24 September 2006; pp. 139–143. 17. Lukas, J.M.; Reneau, J.K.;Wallace, R.L.; De Vries, A. A study of methods for evaluating the success of the transition period in early-lactation dairy cows. J. Dairy Sci. 2015, 98, 250–262. [CrossRef] [PubMed] 18. Soonberg, M.; Kass, M.; Kaart, T.; Barraclough, R.; Haskell, M.J.; Arney, D.R. Effect of grouping on behaviour of dairy heifers and cows in the transition period. J. Dairy Res. 2021, 88, 45–51. [CrossRef] [PubMed] 19. Sammad, A.; Khan, M.Z.; Abbas, Z.; Hu, L.; Ullah, Q.; Wang, Y.; Wang, Y. Major nutritional metabolic alterations influencing the reproductive system of postpartum dairy cows. Metabolites 2022, 12, 60. [CrossRef] [PubMed] 20. Gábor, G.; Balogh, O.G.; Kern, L.; Gábor, P.R.; Fébel, H. Nutrition. Metabolic Status and Reproductive Efficiency in Dairy Herds. Open J. Anim. Sci. 2016, 6, 75–84. [CrossRef] 21. Batista, C.P.; Castro Ruiz, S.M.; Correa Cardona, H.J.; Gonçalves, R.S.; Valle, S.D.F.; Diaz Gonzalez, F.H. Relation between liver lipid content and plasma biochemical indicators in dairy cows. Acta Sci. Vet. 2020, 48, 1–9. [CrossRef] 22. Paiano, R.B.; Birgel, D.B.; Bonilla, J.; Birgel Junior, E.H. Evaluation of biochemical profile of dairy cows with metabolic diseases in tropical conditions. Reprod. Dom. Anim. 2020, 55, 1219–1228. [CrossRef] [PubMed] 23. Holdridge, L.R. Ecología Basada em Zonas de Vida; Instituto Interamericano de Cooperación para la Agricultura: San José de Costa Rica, Costa Rica, 2000; p. 216. 24. Payne, J.M. The Compton metabolic profile test. Proc. R. Soc. Med. 1972, 64, 181–183. [CrossRef] 25. Roche, J.R.; Friggens, N.C.; Kay, J.K.; Fisher, M.W.; Stafford, K.J.; Berry, D.P. Invited review: Body condition score and its association with dairy cow productivity, health, and welfare. J. Dairy Sci. 2009, 92, 5769–5801. [CrossRef] [PubMed] Di Rienzo, J.A.; Casanoves, F.; Balzarini, M.G.; Gonzalez, L.A.; Tablada, E.M. InfoStat, Versión 2020. Universidad Nacional de Córdoba, Argentina. 2024. Available online: http://www.infostat.com.ar/index.php?mod=page&id=34 (accessed on 3 June 2024). 27. R Core Team. R: A Language and Environment for Statistical Computing. 2020. 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