Condition of surplus dairy calves during marketing: A cross-sectional study

In North America, surplus dairy calves are sold soon after birth and often marketed through a third party (e.g., live auction, livestock dealer) before entering veal or dairy beef production. Previous work has demonstrated that a percentage of calves have failed transfer of passive immunity (FTPI) and clinical signs of disease on arrival at calf-raising facilities, but little is known regarding calf condition during marketing. The objectives of this cross-sectional study were to (1) estimate the prevalence of FTPI and poor health outcomes in surplus calves on arrival at livestock dealers, and (2) investigate the association between calf-level variables (body weight, sex, source) and health outcomes. Two livestock dealers in Ohio were visited 2 to 3 times per week, with approximately 28 calves enrolled in the study per visit for a total of 1,119 calves. One blood sample per calf was obtained to evaluate FTPI by measuring serum total protein concentrations (using a cutoff <5.1 g/dL). Calves were clinically evaluated for signs of arthritis, broken ribs or tail, dehydration, depression, diarrhea, fever, navel inflammation, and respiratory disease by 2 observers; health outcomes were dichotomized using clinically relevant cut points. Descriptive statistics were used to estimate the prevalence of calves with poor health outcomes. Multivariable logistic regression models were built to investigate the effect of body weight, sex, and source on health outcomes. Nineteen percent (206/1,091) of calves had FTPI.


INTRODUCTION
Calves born on dairy farms can either be introduced to the milking herd or sold for other purposes, such as red meat production.In North America, calves (mostly males) that are destined for red meat production are predominantly sold from the dairy farm within a week of birth (Shivley et al., 2019;Creutzinger et al., 2021) and commonly referred to as "surplus calves" because these animals exceed the needs of the dairy operation.Surplus calves are typically sold through a third party, such as a live auction, livestock dealer (i.e., a facility where groups of calves are aggregated), or both before entering one of 3 production chains: "bob" veal, "formula-fed" veal, or dairy beef (Creutzinger et al., 2021).
Surplus calf health in the veal and dairy beef industries is directly associated with the quality of neonatal care calves receive on the dairy farm of birth (Creutzinger et al., 2021).For example, colostrum management has been referenced as the most important management practice in determining future calf health and survival (Godden et al., 2019).However, some evidence indicates that colostrum management practices differ for male and female calves, with male calves receiving suboptimal care.For instance, Shively et al. (2019) reported male dairy calves received 4.8 L of colostrum in the first 24 h of life compared with 5.5 L for heifer calves.Negative outcomes associated with inadequate colostrum management and failed transfer of passive immunity (FTPI) include reduced growth (Dewell et al., 2006) and increased preweaning morbidity and mortality (Godden et al., 2019).
Surplus calves have underdeveloped immune systems and are particularly vulnerable to compromised health and welfare (Roadknight et al., 2021).Calves can face several challenges during marketing, including stressors associated with transport, injury, pathogen exposure, hunger and thirst associated with low milk and water allowances, as well as extreme weather conditions (Roadknight et al., 2021), and they often arrive at calf-raising facilitates in poor health (Wilson et al., 2000;Pempek et al., 2017;Renaud et al., 2018).Recent research also suggests most bob veal calves (96%) had at least one poor health metric observed on arrival at a slaughter establishment in the Midwestern United States (England et al., 2023).This study also reported a high prevalence of hypoglycemia (74%), with male calves having 3.1 times greater odds of having hypoglycemia compared with females.
To date, studies on surplus calf welfare have mainly focused on neonatal care practices or calf health on arrival at slaughter establishments or calf-raising facilities.To our knowledge, no studies in the United States have assessed surplus dairy calf condition during marketing on arrival at livestock dealers.By assessing calf condition during marketing, we can identify possible health concerns at this point in the production chain and target interventions to reduce morbidity and mortality before calves enter the veal or dairy beef industries.Thus, the objectives of this cross-sectional study were to (1) estimate the prevalence of FTPI and poor health outcomes in calves on arrival at livestock dealers, and (2) investigate the association between calf-level variables (BW, sex, source) and health outcomes.We anticipated a moderate to high prevalence of navel inflammation, dehydration, depression, and FTPI among surplus calves on arrival at livestock dealers.We also hypothesized that BW, sex, and source would be associated with poor health outcomes.

Animals, Handling, and Facilities
All procedures described herein were in accordance with the guidelines set forth by The Ohio State University's Institutional Animal Care and Use Committee (Animal Use Protocol 2021A00000047), and this study is reported using the Strengthening the Reporting of Observational Studies in Epidemiology Veterinary guideline (O'Connor et al., 2016).
Two livestock dealers (facility 1 and facility 2) responsible for purchasing and selling surplus dairy calves were visited 2 to 3 times per week between May and September 2021.Both facilities were in Ohio, approximately 180 km from The Ohio State University.Individual dairy producers routinely dropped off individuals or small groups of calves daily, and both facilities continuously received new calves throughout the day.Individual calf weights were recorded on electronic scales at the time of purchase by personnel at facility 1. Group calf weights were obtained at facility 2; however, these data were not always routinely recorded by facility personnel.Facility 1 was a naturally ventilated barn with approximately 20 group pens with sawdust bedding, and calves were able to touch calves from other pens through gate partitions.Facility 1 did not provide access to milk or water if calves were purchased and sold the same day; however, although rare, if calves were held at the facility overnight, they were offered milk replacer via nipple buckets twice daily.Facility 2 was also a naturally ventilated barn with straw bedding.Calves were group housed in 2 separate pens, and each pen had one water trough available.Pens were separated by a metal gate with horizontal partitions through which calves could contact other calves in the adjacent pen.Hard copies of written records were obtained from personnel at facilities 1 and 2, which included information on calf source (i.e., the name of dairy farm of birth or the live auction or livestock dealer facility if calves were sourced through a third party), calf identification number, BW, and sex.Calf age was not recorded, as this information was typically not shared between the dairy producer and calf purchaser(s).However, based on the study team's expertise and long-standing experience working within the surplus dairy calf production network, as well as survey-based research conducted in the United States (Shivley et al., 2019), we approximate the age of calves in our study population to be <7 d.

Clinical Health Examination
On arrival at the livestock dealer facilitates, the study team first assessed the total number of calves available for sampling and estimated the number of calf health assessments that could be completed within the time constraints on each day.If possible, all calves were sampled.However, if the number of calves at the livestock dealer facilities exceeded the number of calf health assessments that could be completed, the study team used haphazard selection and sampled an equal proportion of calves per pen to ensure that calves across the facility had an equal chance of being enrolled in the study.Approximately 28 calves were enrolled in the study per day (n = 1,119 calves total).Study personnel (1 postdoctoral scholar, 1 research associate, 1 veterinary student, 1 graduate student, and 2 undergraduate students) with extensive experience handling and assessing calf health performed all aspects of data collection and received 1 wk of training by the lead investigators (1 animal welfare scientist, 1 veterinarian and epidemiologist) before the onset of the study.
Two researchers (1 research associate [author ZE] and 1 experienced veterinary student [MM]) were trained by the lead scientists (1 animal welfare scientist [JP] and 1 veterinary epidemiologist [GH]) before the start of the study, using a standardized health scoring system adapted from previous studies with young calves (Pempek et al., 2017;Garcia et al., 2022); the 2 trained members of the research team (ZE and MM) completed all clinical health examinations.Health examinations included the evaluation of fever (≥39.4°C),depression (4-point scale; Pempek et al., 2019), respiratory dis- ease (4-point scale for ocular and nasal discharge and ear droop; McGuirk and Peek, 2014), broken ribs or tail (2-point scale), arthritis (4-point scale; Garcia et al., 2022), fecal consistency (2-point scale; Renaud et al., 2020), navel inflammation (4-point scale; Pempek et al., 2017), and dehydration (skin tent test, 4-point scale; Garcia et al., 2022).Before the onset of the study, inter-rater reliability was assessed to ensure consistency between ZE and MM by calculating the percent agreement between the examiners after assessing the health of 36 calves; inter-rater reliability was ≥92.8% for the 7 scored health measures (e.g., depression, respiratory disease, broken ribs or tail, arthritis, fecal consistency, navel inflammation, and dehydration).If a calf was severely depressed (depression score = 3), only noninvasive aspects of the health examination were performed; blood samples and rectal temperature were not collected (n = 6 calves).Scoring systems and definitions for each health outcome are described in Table 1.

Blood Collection, Handling, and Processing
Following the health assessment, one blood sample per calf was obtained to evaluate transfer of passive immunity (TPI) by measuring serum total protein (STP) concentrations.Blood samples were collected from the jugular vein into 10-mL vacuum tubes without anticoagulant (BD Vacutainer red top blood collection tubes, Becton Dickinson, Franklin Lakes, NJ).Blood samples were placed into a cooler with ice packs, where they remained during transport to The Ohio State University for STP measurements.Samples were centrifuged at 1,180 × g for 10 min, then transferred via disposable plastic pipettes onto a DD-2 Digital-Dairy Refractometer (MISCO, Solon, OH) to evaluate STP using the following categories: excellent TPI (STP ≥6.2 g/dL), good TPI (STP 5.8-6.1 g/dL), fair TPI (STP 5.1-5.7 g/dL), and poor TPI or FTPI (STP <5.1 g/dL; Lombard et al., 2020).

Sample Size Calculation
The sample size was determined based on a larger project on benchmarking passive TPI and calf health, where the number of surplus calves born on farms designated to receive (intervention) or not receive (control) the benchmarking intervention was considered.Briefly, we anticipated enrolling 900 female and 540 male calves over 9 mo (450 female and 270 male calves per treatment group).The total number of male calves enrolled into the intervention group provided 99% power to detect differences at α = 0.05 in the mean STP concentrations between the intervention and control groups (180 male calves per treatment group) at the 3-mo post intervention follow-up, assuming mean STP concentrations of 5.5 and 6.0 (σ = 0.4) in the control and intervention groups, respectively (Atkinson et al., 2017).The sample size was also inflated for the expected inclusion of random and fixed effects in the model.Likewise, the total of 900 female and 540 male calves, respectively, provided 80% power to identify differences in the prevalence of FTPI between male and female calves, assuming a 12% and 8% respective prevalence, and controlling for important variables in the model.

Statistical Analysis
Calf assessment data were entered into Microsoft Excel (Microsoft Corp., Redmond, WA) and checked for errors and completeness manually.Descriptive statistics were used to determine the prevalence of calves (n = 1,119) with poor health outcomes on arrival at the livestock dealers.All clinical health assessment scores were dichotomized for analysis, and Table 2 summarizes the clinically relevant cutoff values for each variable.Prevalence estimates for poor health outcomes were calculated as the total number of calves having a particular poor health outcome divided by the total number of sampled calves.The SURVEYFREQ procedure of SAS (Version 9.4; SAS Institute Inc., Cary, NC) was used to produce prevalence estimates and 95% confidence intervals (CI), and the EXACT statement was specified when prevalence estimates were <5%.
Complete data were available for 837 calf assessments; calf-level data were either missing or not provided by the livestock dealers for BW (n = 53), sex (n = 56), and source (n = 173).Sex was included in the calf health assessments soon after the onset of the study, once it was realized by the research team that a high proportion of surplus dairy calves were female.Missing data for BW and source were not provided to the study team by the livestock dealers.
Mixed-effect logistic regression models (PROC GLIMMIX, SAS) were built to determine possible associations between independent variables related to calf characteristics and dichotomized dependent clinical health outcome variables.For this study, independent variables related to calf characteristics included BW (as a continuous variable), sex (as a dichotomous variable), and whether calves were purchased directly from a local dairy farm versus indirectly from a third party, such as a live auction or livestock dealer (as a dichotomous variable).Dichotomized dependent clinical health outcome variables included FTPI, diarrhea, navel inflammation, ocular discharge, depression, fever, any dehydration, and moderate to severe dehydration.Because the prevalence of arthritis, broken ribs or tail, ear droop, and nasal discharge were <2.0%(Table 3), these variables were excluded from modelbuilding procedures.Calf-specific source (e.g., the dairy farm of birth) was included as a random effect to account for potential differences in management across locations.
Models were built in multiple steps.First, univariable models were evaluated, and independent variables (e.g., BW, sex, and whether calves were purchased directly from a local dairy farm versus indirectly from a third party) were screened for statistical associations.Independent variables that had moderate statistical associations (defined at a liberal P-value <0.2) were subsequently included in the multivariable analyses.If more than one independent variable was potentially associated with the clinical health outcome of interest (P < 0.2), a manual forward stepwise multivariable logistic regression analysis was used for each model.Variables were retained in the multivariable model if P was <0.05 or if they had a confounding effect on the clinical health outcome of interest.Confounding was assessed by comparisons of the crude and adjusted odds ratios (OR) after a variable was included in the model; a variable was considered a potential confounder if the

DISCUSSION
The objectives of this study were to (1) to estimate the prevalence of FTPI and poor health outcomes in calves on arrival at livestock dealers, and (2) investigate the association between calf-level variables (BW, sex, source) and health outcomes.Nearly one out of every 5 surplus dairy calves had FTPI, with approximately 43% having suboptimal TPI according to recent standards (Lombard et al., 2020).The most common clinical health concerns observed among calves on arrival at the livestock dealer were dehydration (69.2%) and navel inflammation (26.3%).
Neonatal calf care is essential for calf productivity and survival, and one of the most critical aspects is colostrum management (Godden, 2008).Approximately one-fifth of surplus calves (male and female) in our study had FTPI using a STP cut point <5.1 g/dL.The high prevalence of mild dehydration in our study could have inflated STP concentrations and underestimated the true prevalence of FTPI.Compared with our estimate of FTPI, Wilson et al. ( 2023) evaluated STP concentrations in 1,433 surplus dairy calves at an assembly facility in British Columbia, Canada, and documented a 24% FTPI prevalence when using an STP cut point <5.1 g/dL.Other FTPI estimates observed in surplus dairy calf populations range from 12% (Wilson et al., 2020a) to 43% (Wilson et al., 2000).In comparison, Shively et al. ( 2018) reported a 12.1% FTPI prevalence in heifer calves (n = 1,972 calves).Our estimate of FTPI prevalence, particularly for male calves, is approximately double the current recommendations for FTPI in calf populations (i.e., 10% of calves with STP values <5.1 g/dL; Lombard et al., 2020).Therefore, we encourage continued efforts to improve colostrum management for surplus calves, and strategies to strengthen the relationship between dairy producers and those purchasing calves (e.g., live auction or livestock dealer personnel, calf raisers) should be explored in future research (Creutzinger et al., 2022).
A lower BW was associated with FTPI in our study.Cuttance et al. (2018) reported an association between FTPI (STP <5.2 g/dL) and calf BW at weaning, 6, 9, and 12 mo of age; calves with FTPI were 0.9 kg lighter at weaning and 3.3 kg lighter at 12 mo of age compared with calves with successful TPI.Windeyer et  (Winder et al., 2016;Creutzinger et al., 2021).It is possible that dairy producers prioritized allocating high-quality resources, such as colostrum, to heavier calves that may be more apt to enter formula-fed veal or dairy beef production, compared with smaller calves that may enter bob veal production; however, this requires further exploration.
Most calves were at least mildly dehydrated on arrival at the livestock dealers in this study.We chose to estimate any level of dehydration prevalence because calves experiencing mild, moderate, or severe dehydration likely feel thirsty and experience a negative affective state before the onset of more severe clinical signs of dehydration.Any level of dehydration has also been associated with a greater risk of early mortality in formula-fed veal production (Renaud et al., 2018).Comparable to our results, Marcato et al. (2020) reported that 70% of surplus calves were dehydrated (skin tent >1 s) during marketing in the Netherlands, and Pempek et al. (2017) reported 35.1% of formula-fed veal calves (n = 400) were moderately to severely dehydrated (skin tent >4 s) on arrival at calf-raising facilities.Our comparable estimate for moderate to severe dehydration using a skin tent test ≥4 s was significantly lower in this study (2.60%).In the current study, calf health was assessed earlier in the production chain, upon arrival at livestock dealers.We suspect that because calves are not typically provided milk or water during marketing unless they are retained overnight, the prevalence of dehydration would most likely increase as calves continue to move throughout the production chain.
Approximately one-quarter of calves (26%) had navel inflammation in our study.Comparatively, others previously reported 12% (Wilson et al., 2020b) and 20% (Marquou et al., 2019) of surplus dairy calves had navel inflammation at live auctions in British Columbia and Québec, Canada, respectively.Additionally, males had nearly twice the odds of having navel inflammation compared with females.Von Konigslow et al. ( 2022) reported improved umbilical healing in females compared with males, suggesting the existence of some physiological differences based on sex.Our findings might suggest differences in the cleanliness or type of housing used for female and male calves, as they are sometimes housed in separate locations on the dairy farm after birth (Wilson et al., 2020a).Navel inflammation is considered painful, and calves with this disease change their behavior and spend less time lying compared with healthy calves (Studds et al., 2018).Thus, guaranteeing successful TPI and cleanliness of environments on the dairy farm of birth (e.g., calving pen, calf housing area), as well as during transport and marketing for all calves, is critical to reduce the likelihood of navel inflammation.
Source was associated with diarrhea and depression.Calves purchased via a third party had lower odds of depression and diarrhea compared with calves purchased directly from the dairy farm of birth.Although we did not anticipate this finding, it is possible that calf haulers assessed calf fitness before transport from a third party and agreed only to transport calves without signs of disease.Renaud et al. (2018) also found that droverderived calves (i.e., calves transported from multiple dairy farms to a calf-raising facility by a third party) had reduced mortality in veal production compared with calves transported directly from the dairy farm of birth.Additionally, a slaughter establishment that harvests large numbers of bob veal calves was located within the same county as the 2 livestock dealers in this study; it is possible that this facility may have accepted all surplus calves from local dairy farms, regardless of their condition.Further, Goetz et al. (2023) reported a lower incidence of diarrhea in calves that were older (15-19 d of age) at the time of transport compared with calves that were 2 to 6 d of age.It is plausible that age played a role in the association between source and the incidence of diarrhea and depression, with calves sourced from a third party being older than calves from a local dairy farm.
A possible limitation of this study is the lack of detailed information on calf age, breed, and source.Crossbred surplus calves might produce a greater economic return for dairy producers compared with purebreds (Buczinski et al., 2021), and thus, dairy producers may prioritize allocating higher quality resources, such as colostrum, to crossbred calves; future research is needed to investigate possible differences in calf care practices due to breed.Additionally, the type of source (local dairy farm versus third party) was available, but because addresses were not disclosed, we were unable to estimate the total distance or time calves were transported.Lastly, measures to elucidate calves' affective state were not included in this study.Investigating the mental and emotional state of the animal would lead to a more holistic assessment of surplus dairy calf welfare, particularly considering calf hunger and thirst during fasting, and should be explored in future research.

CONCLUSIONS
To our knowledge, this study is the first to describe surplus dairy calf health on arrival at livestock dealers in the United States.Approximately 1 out of every 5 surplus dairy calves had FTPI, with 40% having suboptimal TPI.This finding highlights the opportunity for continued improvements in colostrum management for female and male surplus dairy calves.Dehydration (69.2%) and navel inflammation (26.2%) were the most prevalent health concerns, and male calves had greater odds of having navel inflammation.This finding may suggest differences in housing, navel care practices, or calf age at sale for female and male surplus dairy calves.We encourage more research to better understand neonatal care on the dairy farm of birth, as well as strategies to implement best management practices for predominantly male surplus dairy calves.Lastly, considering the high prevalence of dehydration, we encourage the provision of milk, oral electrolyte solutions, or water on the dairy farm of birth and during marketing.

Figure 1 .
Figure 1.Proportion of male and female surplus calves (a) and calves from different sources (b) with excellent (≥6.2 g/dL), good (5.8-6.1 g/dL), fair (5.1-5.7 g/dL), and poor (<5.1 g/dL) serum total protein values, in reference to consensus serum total protein and percentage of calves recommended in each transfer of passive immunity (TPI) category.
Maggard et al.: SURPLUS DAIRY CALF HEALTH DURING MARKETING

Table 1 .
Maggard et al.:SURPLUS DAIRY CALF HEALTH DURING MARKETING Description of scoring criteria used to evaluate calves for clinical signs of respiratory inflammation (as indicated by ocular and nasal discharge and ear droop), broken tail or ribs, arthritis (joint inflammation), diarrhea, navel inflammation, dehydration, and depression on arrival at 2 livestock dealers in Ohio Health outcome

Table 2 .
Maggard et al.: SURPLUS DAIRY CALF HEALTH DURING MARKETING Clinically relevant cut points for health measures assessed in calves on arrival at 2 livestock dealers in Ohio

Table 3 .
Maggard et al.: SURPLUS DAIRY CALF HEALTH DURING MARKETING Number and percentage of female and male surplus dairy calves with poor health outcomes at 2 livestock dealers in Ohio

Table 4 .
Maggard et al.: SURPLUS DAIRY CALF HEALTH DURING MARKETING Univariable logistic regression models for poor health outcomes in 837 surplus dairy calves on arrival at 2 livestock dealers in Ohio

Table 5 .
Results from final multivariable logistic regression models evaluating the effect of BW, sex, and source on failed transfer of passive immunity, navel inflammation, diarrhea, and depression in 837 surplus dairy calves on arrival at 2 livestock dealers in Ohio