Abstract

Résumé

Introduction

Disease and mortality in male calves remain important topics for research in animal welfare and calf production. Recent studies in Belgium and the Netherlands reported that 25% of white veal calves developed at least 1 disease during their lifetime (1) and that 15% and 61% developed diarrhea and bovine respiratory disease (BRD), respectively (2). Other studies have reported 4% to 10% total mortality throughout the feeding period for veal calves in eastern Canada and Switzerland (3,4). Such health challenges have resulted in high levels of antimicrobial use in the male calf industry contributing to the emergence of antimicrobial resistance (4,5).

The care of calves at the dairy farm of origin may influence subsequent health. Relevant factors include the quality and quantity of colostrum provided, the type and cleanliness of housing, and exposure to adverse events such as dystocia (4,6–8). Additionally, calves that are marketed at a young age may be vulnerable to health challenges as low body weight has been associated with higher mortality in calves arriving at veal facilities (8). Better management at the dairy farm and improved marketing practices could increase male calf health and welfare (9).

Long-distance transportation can also affect calf health (10). Transportation of young calves has been associated with dehydration, weight loss, and mobilization of body reserves as identified by increased serum glucose and cortisol levels (11,12). Additionally, a North American survey found 4% of male dairy calves became compromised (dead or non-ambulatory) after transportation, compared to 0.045% in other classes of cattle (13). Due to Canada’s large geography, many young dairy calves are transported long distances between dairy farms and calf-rearing facilities, but the effects of long-distance transportation have not been systemically evaluated (14).

Because calf age and health are considered important for good transportation outcomes, many countries have specific requirements for calf condition before transportation. For example, New Zealand (15) and the European Union (16) require calves to have healthy navels, and be a minimum age of 4 and 14 d before transportation, respectively. Recently, Canada introduced regulations to limit transportation time for unweaned calves to 12 h, prohibit transport of calves with unhealed or infected navels, and require that transport of calves less than 9 d of age be limited to movements directly to the final destination (14). However, there has been little research to inform these policies, and no studies have followed calves from dairy farms to relate pre-transport health to subsequent morbidity and mortality at calf rearing facilities.

This prospective single-cohort study was designed to i) describe the condition and management of male calves at the dairy farm of origin before transportation; ii) evaluate risk factors associated with immediate deterioration of calf condition after long-distance transportation; and iii) determine how calf condition before transport related to subsequent morbidity and mortality.

Materials and methods

Statistical analyses

Due to logistical constraints in following calves throughout the study, each analysis used a different subset of calves (Figure 1).

Open in a separate window

Figure 1

Flowchart showing the number of calves for the various statistical analyses.

BRD – Bovine respiratory disease; STP – Serum total protein.

Pre-transport descriptive data

Only calves with complete health scores that were confirmed to be transported to the calf grower or auction (n = 623) were included to ensure that evaluations reflected calf condition within 24 h of transport. Microsoft Excel (Microsoft Corporation, Redmond, Washington, USA) was used to tabulate descriptive data. Median and mean measures of central tendency are reported depending on the data distribution. Health score deterioration was evaluated using RStudio version 1.2.1335 as an indication of decline in condition; all other data analysis was performed using SAS University Edition (SAS Institute, Cary, North Carolina, USA).

Health deterioration after transport

Calves (n = 161) were evaluated for changes in health score. The correlation between STP measured before versus after transportation was based on 81 calves because 80 calves were missing an STP measurement due to a malfunctioning refractometer or were > 9 d at the time of the second sample. A McNemar test with Durkalski’s adjustment for the effect of farm was used to evaluate changes (26), using the “clust.bin.pair” package of R package version 0.1.2 (27). A paired t-test and Pearson correlation (r) were used to compare STP levels before and after transportation (Proc Univariate). The assumption of normality was confirmed with data visualization and a Shapiro-Wilk test for normality.

For modelling purposes, for each health category (attitude, pyrexia, BRD, fecal, navel), calves were scored 1 if they had deteriorated after transport and 0 if condition was unchanged or improved. Logistic mixed-effect models were then used to test the effect of age, HG, and FTPI on heath deterioration, with dairy farm of origin included as a random effect to account for variation in management, including the differences in transportation. Model building was completed using Proc glimmix with a binary distribution and logit link function. Pearson correlations between explanatory variables were calculated to assess collinearity, with none showing a coefficient > 0.6. Univariable regression models were used to determine if age, HG or FTPI was associated with health deterioration. Only FTPI was associated with health score deterioration, so multivariable modelling was not pursued.

Morbidity and mortality

Similar model-building was used for morbidity and mortality at the calf grower using Proc glimmix. Three models were created with calves scoring 1 if they were treated for diarrhea in the first 2 wk (model 1), treated for BRD in the first 2 wk (model 2), or died during these 2 wk (model 3). In each model, calves were scored 0 if they remained untreated in the 2 wk (models 1 and 2) or survived the 2 wk (model 3). Initially, univariable logistic mixed-effect models were used to test for associations between these outcomes and age, HG, FTPI, and the dichotomized health scores taken on the dairy farm of origin (Table 2). Dairy farm within calf grower was considered a random effect. Factors liberally associated in univariable modelling (P < 0.2) were offered to the multivariable model using backwards elimination. Six calves were confirmed arrived but were lost to follow-up and did not have treatment or mortality records. The 6 calves that died before the end of week 2 without being treated for diarrhea or BRD were not included in morbidity regression analysis. A further 38 calves that were lost to follow-up and could not be confirmed alive after 2 wk were not included in mortality analysis.

Table 2

Univariable model for morbidity (diarrhea, bovine respiratory disease) and mortality outcomes for male dairy calves in the first 2 weeks after arrival at a calf grower, including variables associated at P < 0.2.

Health outcome	N	Variablea	n	OR	95% CI	P-value
Diarrhea	370	FTPI
		Fail	50	2.0	1.0 to 4.2	0.067
		Pass	300	Referent
		HG
		Every 1 cm increase	364	0.9	0.8 to 1.0	0.009
		Navel
		Abnormal	39	2.2	1.0 to 4.9	0.046
		Normal	329
		Pyrexia
		Abnormal	17	3.5	1.2 to 10.9	0.024
		Normal	350	Referent
BRD	370	BRD
		Abnormal	7	6.5	0.8 to 52.3	0.080
		Normal	355	Referent
		HG
		Every 1 cm increase	364	1.1	1.0 to 1.2	0.068
Mortality	338	Attitude
		Abnormal	11	11.7	2.7 to 51.4	0.001
		Normal	324	Referent
		BRD
		Abnormal	7	4.3	0.5 to 39.0	0.190
		Normal	323	Referent
		Fecal
		Abnormal	64	3.9	1.3 to 12.1	0.020
		Normal	272	Referent
		HG
		Every 1 cm increase	329	0.9	0.8 to 1.0	0.050

Open in a separate window

^aVariables as recorded on the dairy farm of origin.

FTPI — Failure of transfer of passive immunity, defined as serum total protein < 5.2 g/dL; HG — Heart girth circumference (cm); BRD — Bovine respiratory disease; OR — Odds ratio; CI — Confidence interval; N — Total number.

Intra-observer agreement

To verify intra-observer agreement for health measures in the standardized examination, 25 calves at the University of British Columbia’s Dairy Education and Research Centre were assessed twice on 1 d, approximately 3 h apart. Weighted (for measures with multiple levels) and unweighted (for binary measures) kappa coefficients were used to determine agreement (Proc Freq). Cicchetti-Allison (linear) weight type was used for the weighted kappa calculation. Intraobserver agreement for HG was calculated by a concordance correlation for 106 calves that were assessed within 1 h before transportation (as part of this study) and again approximately 3 h later at an auction market.

Results

For the 25 calves assessed for intra-observer agreement, the percent agreement ranged from 36% to 100% using the 4-point health scale. With health scores converted to dichotomized scores (0 for normal and 1 for abnormal), percent agreement ranged from 88% to 100% (Table 3). For HG measured on 106 calves, the correlation coefficient for intra-observer agreement was 0.95.

Health management at the farm of origin

The median dairy herd size was 290 milking cows (IQR: 205 to 401), and a median of 30 (IQR: 21 to 49) calves were transported per farm. Calves received a median of 6 L (range: 4 to 8 L) of milk per day provided as 2 daily meals. Three farms did not feed calves on the day they were transported. Farms fed calves unpasteurized waste milk (9 farms), milk replacer (6 farms), pasteurized waste milk (1 farm), or both unpasteurized waste milk and milk replacer (1 farm). Male calves were raised in a different area or type of housing than female calves on 12 farms, while 5 farms used similar housing for both sexes. Individual hutches or pens were used for male calves on 10 farms, while 7 used a group pen or a mix of individual and group or pair housing.

The prevalence of disease and disease symptoms in male calves varied widely among the different dairy farms (Figure 2; Table A1). The median (IQR) level of FTPI was 12% (range: 4% to 19%), with 2 farms showing no cases of FTPI. At least 1 health abnormality was identified in 233/623 calves (37%) in their pre-transportation assessment, but this ranged from 3/20 calves (15%) on 1 farm to 14/21 calves (67%) on another. From graphical evaluation, the variation did not appear related to the farm-level variables such as type of milk fed, herd size, or housing type.

Open in a separate window

Figure 2

Box and whisker plot of the prevalence of disease and disease symptoms (n = 623) and failure of transfer of passive immunity (n = 567) in male dairy calves assessed ≤ 24 h before transportation from 17 BC dairy farms. Boxes show medians with upper and lower quartiles; whiskers indicate range. BRD — Bovine respiratory disease; FTPI — Failure of transfer of passive immunity, defined as serum total protein < 5.2 g/dL.

The median age of calves at transportation was 5 d (IQR: 3 to 7 d), ranging from 1 to 54 d for the 428 calves of known age (Figure 3). Mean ± SD heart girth of calves was 82 ± 4 cm, which corresponds to 44 kg body weight (BW) (25), with calves ranging from 67 cm (~27 kg) to 98 cm (~77 kg).

Open in a separate window

Figure 3

Distribution of ages of 428 male dairy calves transported to calf grower operations from 17 dairy farms in British Columbia.

Morbidity and mortality

During the first 2 wk after transportation, complete morbidity and mortality records were available for 370 and 338 of the calves, respectively. During these 2 wk, 86/370 calves (23%) were treated for diarrhea, 164/370 calves (44%) were treated for BRD, and 13/338 (4%) died. A larger proportion of calves was treated for disease at CG2 compared to CG1 [75/189 (40%) versus 11/181 (6%) for diarrhea, 147/189 (78%) versus 17/181 (9%) for BRD], but similar mortality was observed at both locations [7/185 (3.8%) versus 6/153 (3.9%)]. In the final logistic regression model, smaller HG and abnormal navel score were associated with increased diarrhea treatment in the first 2 wk (Table 5). However, an interaction was found between navel score and HG, such that calves with a small heart girth that had navel disease had increased odds of being treated for diarrhea. In addition, calves with a depressed attitude at the dairy farm had increased odds of dying in the first 2 wk at the calf grower (Table 5). No factors measured at the dairy farm were associated with BRD treatment at the calf grower.

Table 5

Logistic mixed regression models of associated risk factors for male dairy calves being treated for diarrhea or dying in the first 2 weeks at a calf grower.

Outcome	Variable	Estimate	SE	t	P-value	OR	95% CI
Diarrhea	Intercept	5.5	3.5	1.57	0.14	—	—
	Abnormal navel	23.2	10.6	2.18	0.03	2.8	1.2–6.7
	Normal navel	Reference	—	—	—	—
	HGa (cm)	−0.09	0.04	−2.05	0.04	0.9	0.8–1.0
	HGa navel interaction
	HG with abnormal navelb	−0.3	0.13	−2.09	0.04	0.7	0.5–0.9
	HG with normal navelb	Reference	—	—	—	—
Mortality	Abnormal attitude	2.5	0.75	3.29	0.001	11.8	2.7–51.4
	Normal attitude	Reference

Open in a separate window

^aHG — Heart girth (cm).

^bBased on 1 cm offset from the mean heart girth (81.1 cm).

SE — Standard error; t — calculated difference; OR — Odds ratio; CI — Confidence interval.

Discussion

Of the 640 calves that were assessed before transportation, many had an identifiable health abnormality and the prevalence of these abnormalities varied widely, depending on the dairy farm of origin. Calf disease on dairy and veal farms is a considerable challenge, and has been linked to provision of colostrum, cleanliness of housing, and body weight upon arrival (4,8). The importance of reducing calf disease has been emphasized because of the negative welfare implications and to minimize the use of antimicrobials in food animals (4). However, the use of good calf management practices is inconsistent among farms (28), so the variability in calf condition seen in our study is not surprising.

Some calves in this study were transported at a very young age and light weight. However, age itself was not a predictor of immediate health deterioration, morbidity or mortality, and age was not highly correlated with HG in this data set. While weight of calves entering veal facilities is an important risk factor for mortality (8), the optimal age and weight for transport of dairy calves has not been well-established. Regulations in New Zealand, the EU, and Canada have considered age an important criterion for calves to be considered fit for transportation, but it remains unclear whether transporting older calves will improve their welfare. The effect of age may also interact with the time and conditions of transport, for example, with younger calves being more susceptible to extreme weather or lengthy transport. Further research using a wider range of ages and transportation conditions is warranted to determine if there is an optimal age to transport young calves.

Interpretation of herd-level factors is limited because of the small number of farms used in the current study. Similar to our findings, other work has shown that male calves were more likely than female calves to be housed individually (3), perhaps because farmers wanted to keep male calves healthy before transport. Regarding feeding practices, calves were provided a smaller quantity of milk than is currently recommended, and some were provided unpasteurized waste milk, which has been associated with reduced immunity and productivity (29).

Levels of FTPI in this study were comparable to levels seen in some recent studies (3), but lower than those reported in earlier survey results (30). This could be due to sampling bias as well-managed farms may have been more willing to participate, or it could reflect improved colostrum management in recent years. In a 2017 Canadian survey, 91% of farmers reported always feeding colostrum to male calves (28), as is consistent with our observations of FTPI. The variation between farms was notable, however, with 2 farms having no calves with FPTI and others having a very high rate of failure. This finding, together with the observed differences in the environmental and nutritional management, underlines the inconsistency observed in care of male calves on dairy farms (9).

Of the 161 calves that were assessed before and after transportation, the percentage with diarrhea was lower at the calf grower than at the farm of origin. This may reflect dehydration as calves did not receive milk or water for an estimated 24 to 36 h before and during transport, and/or the use of oral meloxicam. Indeed, better gastrointestinal health has been observed when meloxicam was given before long distance (8.5 h) transportation of Jersey calves (31). More calves had pyrexia after transportation which could reflect an inability of young calves to closely regulate their body temperature during transportation as seen in previous studies (11). As this study took place during the winter months, it is unlikely that high environmental temperature or humidity played a role in pyrexia.

Calf STP concentrations were similar and highly correlated before and after transport. This supports the results of previous work which compared calves transported up to 12 h to control calves that remained on their home farm (32). Serum total protein taken from male dairy calves upon arrival at rearing facilities has been used as an indication of FTPI and has been predictive of respiratory disease and mortality (2). Our results support that STP measured upon arrival at calf-rearing facilities reflects FTPI accurately.

Calves with FTPI were more likely to develop a depressed attitude after transportation. While “depressed attitude” is not a clinical diagnosis, it can be a symptom of septicemia, fatigue, and dehydration (33), and may indicate an inability of the calf to cope with external conditions. Calf “attitude,” although not specific to any one disease condition, may be predictive of poor health outcomes and be useful for assessing fitness for transport.

In this study, calves with swollen navels and small HG were especially likely to be treated for diarrhea. Previous work has identified weight and navel disease (6,8) as important risk factors for disease and mortality in veal calves. Navel disease did not increase the probability of being treated for diarrhea for calves with larger HG, which may have been more resistant to developing illness due to age (34) or a higher plane of nutrition (35). Other unmeasured factors may also have been important in this finding including poor environmental cleanliness and lack of preventative measures such as navel dipping that may have resulted in both poor growth and navel infection.

In the first 2 wk at the calf grower, 44% of calves were treated for BRD; this is comparable to previous work which found a 60% cumulative incidence of BRD over the first 18 d after arrival at a veal facility (2). Interestingly, none of the calf conditions measured at the dairy farm of origin predicted BRD outcomes at the calf grower. Perhaps environmental and management factors (air quality, nutrition, mingling of animals) had a greater influence on the development of BRD.

This study builds on previous research which suggests the quality of care of male dairy calves can predispose them to poor health outcomes at calf-rearing facilities. However, the study was limited by an inability to follow all the calves to the calf grower, resulting in smaller sample size which might have affected the findings related to morbidity and mortality. In future studies, improved data collection at the calf grower could increase the sample size and might reveal further calf-level risk factors.

In summary, some calves in this study were transported at a young age and light weight, and some displayed disease symptoms that should preclude transport. These factors varied widely depending on the farm of origin. Calves transported at a light weight with navel disease, and those with a depressed attitude, were more likely to experience poor health outcomes during the first 2 wk at calf-grower facilities. These findings indicate a need to improve the health of male dairy calves before they are transported. Further clarification on the optimum age and weight, and other criteria for transport of calves are necessary to inform policy and protect male dairy calf health and welfare.

Acknowledgments

Appendix

Footnotes

References