Identification of biomarkers measured upon arrival associated with morbidity, mortality, and average daily gain in grain-fed veal calves
Open accessAbstract
There is a strong need for management strategies that help reduce the incidence of disease and subsequent antimicrobial use in the veal industry. Biomarkers could serve as useful tools that allow producers to take preventative measures before clinical problems occur. The objective of this prospective cohort study was to identify biomarkers measured upon arrival associated with morbidity, mortality, and average daily gain (ADG) in grain-fed veal calves. Upon arrival at a grain-fed veal facility in Ontario, Canada, calves were weighed and health-scored using a standardized health-scoring system. Several metabolites were measured including creatine kinase (CK), cholesterol, haptoglobin, manganese, serum total protein, iron, cobalt, zinc, selenium, molybdenum, and IgG. Farm personnel treated calves according to their farm protocol and weighed them at 78 d after arrival. Performance, treatment, and mortality records from the facility were used for analysis. Multivariable Cox proportional hazard models were created to evaluate metabolic biomarkers associated with morbidity and mortality. A mixed linear regression model was created to determine biomarkers associated with ADG. A total of 992 male dairy calves were evaluated at arrival from January to December 2017. Of the calves evaluated, 74 calves (7.5%) died and 877 (88.4%) were treated for illness over the 11-wk period under observation. Higher levels of haptoglobin and molybdenum were associated with a greater hazard of morbidity, whereas higher weight upon arrival and higher levels of both CK and IgG were associated with a reduced hazard of morbidity. For mortality, higher weight upon arrival and higher levels of cholesterol and IgG were associated with a lower hazard of mortality occurring over the 78-d period of observation. Higher weight, cholesterol, copper, CK, iron, and IgG were associated with increased ADG, whereas increased zinc and haptoglobin were negatively associated with ADG. These results demonstrate that certain biomarkers could be used to identify high-risk calves when measured upon arrival at a veal facility. Future research should focus on determining the utility of these biomarkers to selectively target intervention strategies to improve ADG and reduce morbidity and mortality.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The impact of altered physiological status and health of calves during and after transport is triggered by a combination of factors including reduced feed and water intake, increased physiological and physical stressors, muscle fatigue and immunosuppression.
“The impact of altered physiological status and health of calves during and after transport has been well documented and has been shown to be triggered by a combination of factors including a reduction in feed and water intake, and increased physiological and physical stressors, muscle fatigue and immunosuppression [3–9].”
From Observational study: effect of varying transport durations and feed withdrawal on the physiological status and health of dairy calves (2025) · cites this paper as [7]
Calves arriving with elevated haptoglobin had a greater hazard of morbidity, whereas calves with higher levels of cholesterol and IgG had a lower hazard of mortality.
“Specifically, calves arriving with elevated haptoglobin had a greater hazard of morbidity, whereas calves with higher levels of cholesterol and IgG had a lower hazard of mortality”
From A randomized controlled trial investigating the effect of transport duration and age at transport on surplus dairy calves: Part II. Impact on hematological variables. (2023) · cites this paper as Goetz et al., 2021
Higher cholesterol, IgG, and CK on arrival to a veal facility have been associated with increased average daily gain compared with calves arriving with lower cholesterol, IgG, and CK.
“Higher cholesterol, IgG, and CK on arrival to a veal facility have also been associated with increased ADG compared with calves arriving with lower cholesterol, IgG, and CK”
From A randomized controlled trial investigating the effect of transport duration and age at transport on surplus dairy calves: Part II. Impact on hematological variables. (2023) · cites this paper as Goetz et al., 2021
Measures such as creatine kinase, haptoglobin, IgG, and cholesterol have been associated with future morbidity, mortality, and average daily gain in veal calves.
“Measures such as creatine kinase (CK), haptoglobin, IgG, and cholesterol have been associated with future morbidity, mortality, and ADG in veal calves”
From A randomized controlled trial investigating the effect of transport duration and age at transport on surplus dairy calves: Part II. Impact on hematological variables. (2023) · cites this paper as Goetz et al., 2021
Previous studies have found that calves arriving to a veal facility with higher levels of cholesterol experience increased ADG and decreased hazard of mortality during the growing period.
“Previous studies have found that calves arriving to a veal facility with higher levels of cholesterol experience increased ADG and decreased hazard of mortality during the growing period”
From A randomized controlled trial investigating the effect of transport duration and age at transport on surplus dairy calves: Part II. Impact on hematological variables. (2023) · cites this paper as Goetz et al., 2021
Elevated concentration of acute phase proteins has been associated with reduced ADG and in surplus calves, increased haptoglobin upon arrival has been associated with a higher hazard of morbidity in calves at a calf-raising facility.
“Elevated concentration of acute phase proteins has been associated with reduced ADG and in surplus calves, increased haptoglobin upon arrival has been associated with a higher hazard of morbidity in calves at a calf-raising facility (Pardon et al., 2015; Goetz et al., 2021).”
From A randomized controlled trial evaluating the effect of providing a rest period during long-distance transportation of surplus dairy calves: Part II. Effect on hematological variables (2024) · cites this paper as Goetz et al., 2021
A previous study found that increased levels of CK were associated with increased ADG and decreased hazard of morbidity.
“A previous study also found that increased levels of CK were associated with increased ADG and decreased hazard of morbidity”
From A randomized controlled trial investigating the effect of transport duration and age at transport on surplus dairy calves: Part II. Impact on hematological variables. (2023) · cites this paper as Goetz et al., 2021
Higher BW at arrival is associated with decreased mortality and infection risk, as well as higher growth rates.
“Higher BW is associated with decreased mortality [48, 49] and infection risk [25, 50, 51], as well as higher growth rates [52, 53].”
From Effects of age and feeding protocols on the metabolic and physiological condition of unweaned calves during and after long-distance transport (2026) · cites this paper as [53]
Cites
Colostrum Management for Dairy Calves
Godden, S., Lombard, J. E., & Woolums, A. R. (2019) · Veterinary Clinics of North America Food Animal Practice · doi:10.1016/j.cvfa.2019.07.005 · Cited by 982 · see citing works
Passive Transfer of Colostral Immunoglobulins in Calves
Weaver, D. M., Tyler, J. W., VanMetre, D. C., Hostetler, D. E., & Barrington, G. M. (2000) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.2000.tb02278.x · Cited by 829 · see citing works
Colostrum Management for Dairy Calves
Godden, S. (2008) · Veterinary Clinics of North America Food Animal Practice · doi:10.1016/j.cvfa.2007.10.005 · Cited by 697 · see citing works
Svensson, C., Lundborg, K., Emanuelson, U., & Olsson, S.-O. (2003) · Preventive Veterinary Medicine · doi:10.1016/s0167-5877(03)00046-1 · Cited by 404 · see citing works
Léger, B., Cartoni, R., Praz, M., Lamon, S., Dériaz, O., Crettenand, A., Gobelet, C., Rohmer, P., Konzelmann, M., Lüthi, F., et al. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.116715 · Cited by 381 · see citing works
Stress, immunity, and the management of calves
Hulbert, L. E., & Moisá, S. J. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10198 · Cited by 370 · see citing works
Lombard, J. E., Urie, N. J., Garry, F. B., Godden, S., Quigley, J. D., Earleywine, T. J., McGuirk, S. M., Moore, D. A., Branan, M., Chamorro, M. F., et al. (2020) · Journal of Dairy Science · doi:10.3168/jds.2019-17955 · Cited by 359 · see citing works
Bovine haptoglobin response in clinically defined field conditions
Skinner, J., Brown, R., & Roberts, L. (1991) · Veterinary Record · doi:10.1136/vr.128.7.147 · Cited by 278 · see citing works
Micronutrients and immune function in cattle
Spears, J. W. (2000) · Proceedings of The Nutrition Society · doi:10.1017/s0029665100000835 · Cited by 255 · see citing works
Raboisson, D., Trillat, P., & Cahuzac, C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150452 · Cited by 206 · see citing works
The mechanisms relating to increases in plasma enzymes and isoenzymes in diseases of animals
Boyd, J. W. (1983) · Veterinary Clinical Pathology · doi:10.1111/j.1939-165x.1983.tb00609.x · Cited by 184 · see citing works
Virtala, A.-M. K., Mechor, G. D., Gröhn, Y. T., & Erb, H. N. (1996) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(96)76457-3 · Cited by 182 · see citing works
Longitudinal study on morbidity and mortality in white veal calves in Belgium
Pardon, B., Bleecker, K. D., Hostens, M., Callens, J., Dewulf, J., & Deprez, P. R. (2012) · BMC Veterinary Research · doi:10.1186/1746-6148-8-26 · Cited by 170 · see citing works
Enjalbert, F., Lebreton, P., & Salát, O. (2006) · Journal of animal physiology and animal nutrition · doi:10.1111/j.1439-0396.2006.00627.x · Cited by 164 · see citing works
Gånheim, C., Hultén, C., Carlsson, U., Kindahl, H., Niskanen, R., & Waller, K. P. (2003) · Journal of Veterinary Medicine Series B · doi:10.1046/j.1439-0450.2003.00658.x · Cited by 162 · see citing works
Acute phase proteins in cattle after exposure to complex stress
Lomborg, S. R., Nielsen, L. R., Heegaard, P. M. H., & Jacobsen, S. (2008) · Veterinary Research Communications · doi:10.1007/s11259-008-9057-7 · Cited by 159 · see citing works
Thompson, P. N., Stone, A., & Schultheiss, W. A. (2006) · Journal of Animal Science · doi:10.2527/2006.842488x · Cited by 157 · see citing works
Evaluating the Clinical Utility of a Biomarker
Pletcher, M. J., & Pignone, M. P. (2011) · Circulation · doi:10.1161/circulationaha.110.943860 · Cited by 154 · see citing works
Zinc Nutrition of Cattle: A Review
Miller, W. J. (1970) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(70)86355-x · Cited by 145 · see citing works
Effects of transport and lairage time on some blood constituents of Friesian-cross steers in Chile
Tadich, N., Gallo, C., Bustamante, H., Schwerter, M., & van Schaik, G. (2005) · Livestock Production Science · doi:10.1016/j.livprodsci.2004.10.004 · Cited by 142 · see citing works
Urie, N. J., Lombard, J. E., Shivley, C. B., et al. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-14010 · Cited by 140 · see citing works
Kim, M.-H., Yang, J.-Y., Upadhaya, S. D., Lee, H., Yun, C., & Ha, J. K. (2011) · Journal of Veterinary Science · doi:10.4142/jvs.2011.12.2.151 · Cited by 122 · see citing works
Pardon, B., Alliët, J., Boone, R., Roelandt, S., Valgaeren, B., & Deprez, P. (2015) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2015.04.009 · Cited by 116 · see citing works
Chelack, B. J., Morley, P. S., & Haines, D. M. (1993) · PubMed · Cited by 114 · see citing works
Prevalence of respiratory disorders in veal calves and potential risk factors
Brscic, M., Leruste, H., Heutinck, L. F. M., Bokkers, E. A. M., Wolthuis-Fillerup, M., Stockhofe, N., Gottardo, F., Lensink, B. J., Cozzi, G., & Van Reenen, C. G. (2012) · Journal of Dairy Science · doi:10.3168/jds.2011-4699 · Cited by 114 · see citing works
Virtala, A., Mechor, G. D., Grohn, Y. T., & Erb, H. N. (1996) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1996.208.12.2043 · Cited by 108 · see citing works
Monitoring of physiological and blood parameters during perinatal and neonatal period in calves
Piccione, G., Casella, S., Pennisi, P., Giannetto, C., Costa, A., & Caola, G. (2010) · Arquivo Brasileiro de Medicina Veterinária e Zootecnia · doi:10.1590/s0102-09352010000100001 · Cited by 102 · see citing works
de Water, G. V., Verjans, F., & Geers, R. (2003) · Livestock Production Science · doi:10.1016/s0301-6226(03)00010-1 · Cited by 98 · see citing works
Knowles, T. G., Warriss, P. D., Brown, S. N., Edwards, J. E., Watkins, P. E., & Phillips, A. J. (1997) · Veterinary Record · doi:10.1136/vr.140.5.116 · Cited by 93 · see citing works
Teixeira, A. G. V., de Lima, F. S., Bicalho, M. L. S., et al. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7625 · Cited by 91 · see citing works
Management practices for male calves on Canadian dairy farms
Renaud, D. L., Duffield, T. F., LeBlanc, S. J., Haley, D. B., & Kelton, D. F. (2017) · Journal of Dairy Science · doi:10.3168/jds.2017-12750 · Cited by 89 · see citing works
Self-citationO'Connor, A. M. C., Sargeant, J. M., Dohoo, I. R., Erb, H. N., Cevallos, M., Egger, M., Ersbøll, A. K., Martin, S. W., Nielsen, L. R., Pearl, D. L., et al. (2016) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.14592 · Cited by 87 · see citing works
Bacterial contamination of colostrum fed to newborn calves in Québec dairy herds.
Fecteau, G., Baillargeon, P., Higgins, R., Paré, J., & Fortin, M. (2002) · PubMed Central · Cited by 82 · see citing works
Orro, T., Pohjanvirta, T., Rikula, U., Huovilainen, A., Alasuutari, S., Sihvonen, L. H., Pelkonen, S., & Soveri, T. (2009) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2009.10.005 · Cited by 82 · see citing works
Mortality risk factors for calves entering a multi-location white veal farm in Ontario, Canada
Winder, C. B., Kelton, D. F., & Duffield, T. F. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-11345 · Cited by 79 · see citing works
Self-citationEvaluating potential biomarkers of health and performance in veal calves
Marcato, F., van den Brand, H., Kemp, B., & van Reenen, K. (2018) · Frontiers in Veterinary Science · doi:10.3389/fvets.2018.00133 · Cited by 76 · see citing works
An evaluation of antimicrobial therapy for undifferentiated bovine respiratory disease.
Bateman, K. G., Martin, S. W., Shewen, P. E., & MENZIES, P. I. (1990) · PubMed Central · Cited by 73 · see citing works
Renaud, D. L., Duffield, T. F., LeBlanc, S. J., Haley, D. B., & Kelton, D. F. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-14042 · Cited by 70 · see citing works
Self-citationOntsouka, E. C., Albrecht, C., & Bruckmaier, R. M. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-9741 · Cited by 69 · see citing works
Management of preweaned bull calves on dairy operations in the United States
Shivley, C. B., Lombard, J. E., Urie, N. J., Weary, D. M., & von Keyserlingk, M. A. G. (2019) · Journal of Dairy Science · doi:10.3168/jds.2018-15100 · Cited by 69 · see citing works
(1993) · Europe PMC (PubMed Central) · Cited by 60 · see citing works
A review of post transport mortality among younger calves
Knowles, T. (1995) · Veterinary Record · doi:10.1136/vr.137.16.406 · Cited by 59 · see citing works
Bernardini, D., Gerardi, G., Peli, A., Nanni Costa, L., Amadori, M., & Segato, S. (2012) · Journal of Animal Science · doi:10.2527/jas.2011-4113 · Cited by 53 · see citing works
Kipp, S., Segelke, D., Schierenbeck, S., Reinhardt, F., Reents, R., Wurmser, C., Pausch, H., Fries, R., Thaller, G. E., Tetens, J., et al. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-11118 · Cited by 52 · see citing works
Scott, K., Kelton, D. F., Duffield, T. F., & Renaud, D. L. (2019) · Journal of Dairy Science · doi:10.3168/jds.2019-16829 · Cited by 52 · see citing works
Self-citationMurray, C. F., Windeyer, M. C., Duffield, T. F., Haley, D. B., Pearl, D. L., Waalderbos, K. M., & Leslie, K. E. (2014) · Journal of Dairy Science · doi:10.3168/jds.2014-8465 · Cited by 44 · see citing works
Renaud, D. L., Waalderbos, K. M., Beavers, L., Duffield, T. F., Leslie, K. E., & Windeyer, M. C. (2020) · Journal of Dairy Science · doi:10.3168/jds.2019-17397 · Cited by 42 · see citing works
Self-citationMontgomery, S. P., Sindt, J. J., Greenquist, M. A., Miller, W. F., Pike, J. N., Loe, E. R., Sulpizio, M. J., & Drouillard, J. S. (2008) · Journal of Animal Science · doi:10.2527/jas.2008-0969 · Cited by 40 · see citing works
Jongman, E., & Butler, K. (2014) · Animals · doi:10.3390/ani4020184 · Cited by 37 · see citing works
Stress, acute phase proteins and immune modulation in calves
Yun, C., WYNN, P. C., & Ha, J. K. (2014) · Animal Production Science · doi:10.1071/an14441 · Cited by 37 · see citing works
Buczinski, S., Rademacher, R. D., Tripp, H. M., Edmonds, M. D., Johnson, E. G., & Dufour, S. (2014) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2014.12.003 · Cited by 32 · see citing works
(2012) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 21 · see citing works
Taggart, D. P., Fraser, W. D., Shenkin, A., et al. (1990) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/1010-7940(90)90017-t · Cited by 18 · see citing works
van Ravenswaay, R. O., Henry, P. R., & Ammerman, C. B. (2001) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(01)00208-5 · Cited by 14 · see citing works
Cui, K., Tu, Y., Wang, Y. C., et al. (2016) · Animal Production Science · doi:10.1071/an15388 · Cited by 5 · see citing works
Blood cholesterol concentrations in dairy calves
Otter, A., & Hateley, G. (2017) · Veterinary Record · doi:10.1136/vr.j122 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Preparing Male Dairy Calves for the Veal and Dairy Beef Industry
Renaud, D., & Pardon, B. (2022) · Veterinary Clinics of North America: Food Animal Practice · doi:10.1016/j.cvfa.2021.11.006 · Cited by 45 · see citing works
Self-citationMarcato, F., van den Brand, H., Kemp, B., Engel, B., Schnabel, S. K., Hoorweg, F. A., Wolthuis-Fillerup, M., & van Reenen, K. (2022) · Journal of Dairy Science · doi:10.3168/jds.2021-20637 · Cited by 35 · see citing works
Characterizing the literature surrounding transportation of young dairy calves: A scoping review
Goetz, H. M., Winder, C. B., Costa, J. H. C., Creutzinger, K. C., Uyama, T., Kelton, D. F., Dunn, J., & Renaud, D. L. (2022) · Journal of Dairy Science · doi:10.3168/jds.2021-21211 · Cited by 32 · see citing works
Self-citationMarcato, F., van den Brand, H., Kemp, B., Engel, B., Schnabel, S. K., Jansen, C. A., Rutten, V. P. M. G., Koets, A. P., Hoorweg, F. A., de Vries-Reilingh, G., et al. (2022) · Journal of Dairy Science · doi:10.3168/jds.2021-20636 · Cited by 24 · see citing works
Rot, C., Creutzinger, K., Goetz, H., Winder, C., Morrison, J., Conboy, M., Bajus, A., & Renaud, D. L. (2022) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2022.105630 · Cited by 21 · see citing works
Self-citationGoetz, H. M., Creutzinger, K. C., Kelton, D. F., Costa, J. H. C., Winder, C. B., Gomez, D. E., & Renaud, D. L. (2023) · Journal of Dairy Science · doi:10.3168/jds.2022-22367 · Cited by 20 · see citing works
Self-citationAntimicrobial Use and Resistance in Surplus Dairy Calf Production Systems
Vinayamohan, P. G., Locke, S. R., Portillo-Gonzalez, R., Renaud, D. L., & Habing, G. G. (2022) · Microorganisms · doi:10.3390/microorganisms10081652 · Cited by 14 · see citing works
Self-citationGoetz, H. M., & Renaud, D. L. (2024) · Journal of Dairy Science · doi:10.3168/jds.2024-25012 · Cited by 2 · see citing works
Self-citationvan Dijk, L. L., Siegmann, S., Field, N. L., Sugrue, K., van Reenen, C. G., Bokkers, E. A. M., Conneely, M., & Sayers, G. (2025) · Irish Veterinary Journal · doi:10.1186/s13620-025-00287-2 · Cited by 4 · see citing works
Siegmann, S., van Dijk, L. L., Field, N. L., Sayers, G., Sugrue, K., van Reenen, C. G., Bokkers, E. A. M., & Conneely, M. (2026) · Irish Veterinary Journal · doi:10.1186/s13620-026-00340-8 · Cited by 2 · see citing works
“Higher BW is associated with decreased mortality [48, 49] and infection risk [25, 50, 51], as well as higher growth rates [52, 53].”
- Authors
- Goetz, H. M., Kelton, D. F., Costa, J. H. C., Winder, C. B., & Renaud, D. L.
- Affiliations
- University of Guelph (CA)
- University of Kentucky (US)
- Corresponding author
- Renaud, D.L.
- Venue
- Journal of Dairy Science
- Publisher
- American Dairy Science Association
- Published
- 2021-01
- Volume
- 104
- Issue
- 1
- Pages
- 874-885
- ISSN
- 0022-0302 (ISSN-L)
- OpenAlex
- W3095453680
- Cited by
- 37
- References
- 57
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 8 · 2023: 6 · 2022: 10 · 2021: 5
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Dairy Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ontario Ministry of Agriculture, Food and Rural Affairs
- Topics
- Health Sciences › Veterinary › Small Animals › Animal health and immunology
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Effects of Environmental Stressors on Livestock
- Keywords
- veal calves, biomarkers, calf morbidity, calf mortality, average daily gain, creatine kinase, haptoglobin, molybdenum, cholesterol, IgG, trace elements, antimicrobial use reduction
- MeSH terms
- Farms, Animals, Animal Feed, Anti-Bacterial Agents, Cattle, Cattle Diseases, Health Status, Male, Morbidity, Ontario, Prospective Studies, Risk Factors, Cohort Studies, Biomarkers, Weight Gain
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review