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Can Vet J. Mar 2009; 50(3): 275–281.
PMCID: PMC2643452

Language: English | French

Factors associated with serum immunoglobulin levels in beef calves from Alberta and Saskatchewan and association between passive transfer and health outcomes

Abstract

Inadequate consumption of colostrum can negatively affect calf health and survival. The serum immunoglobulin G (IgG) concentrations of 935 beef calves from 152 herds in Alberta and Saskatchewan have been described, using radial immunodiffusion. The determinants and health effects of serum IgG concentrations were studied in 601 calves sampled between 2 and 8 days of age. Of these calves, 6% had failure of passive transfer and an additional 10% had marginal passive transfer. Serum IgG concentrations were lower in calves born to a heifer, as a twin, or experiencing dystocia. The odds of both calf death and treatment were increased in calves with serum IgG concentrations below 24 g/L; a threshold notably higher than the 16 g/L usually considered as providing adequate passive transfer. The finding of 1/3 of calves with serum IgG concentrations less than 24 g/L suggests that calfhood treatments and mortality could be decreased by ensuring that high risk calves consume colostrum.

Résumé

Facteurs associés avec des taux d’immunoglobuline sérique chez des veaux de boucherie de l’Alberta et de la Saskatchewan et l’association entre le transfert passif et les résultats de santé. Une consommation inadéquate de colostrum peut influencer négativement la santé et la survie des veaux. Les concentrations d’immunoglobuline sérique G (IgG) de 935 veaux de boucherie provenant de 152 troupeaux en Alberta et en Saskatchewan ont été décrites, en utilisant une immunodiffusion radiale. Les déterminants et les effets sur la santé des concentrations sériques d’IgG ont été étudiés chez 601 veaux sélectionnés âgés entre 2 et 8 jours. Parmi ces veaux, 6 % ont présenté un échec du transfert passif et 10 % avaient un transfert passif négligeable. Les concentrations sériques d’IgG étaient inférieures chez les veaux nés d’une taure donnant naissance à des jumeaux ou qui présentait de la dystocie. Les risques de mortalité du veau et de traitement étaient accrus chez les veaux avec des concentrations sériques d’IgG inférieures à 24 g/L; un seuil considérablement supérieur aux 16 g/L habituellement considérés comme fournissant un transfert passif adéquat. La constatation que le tiers des veaux avaient des concentrations sériques d’IgG de moins de 24 g/L suggère que les traitements et la mortalité des veaux pourraient être réduits en veillant à ce que les veaux à risque élevé consomment du colostrum.

(Traduit par Isabelle Vallières)

Introduction

The syndesmochorial placenta of cattle prevents the bovine fetus from receiving immunoglobulins in utero; therefore, calves are born essentially agammaglobulinemic (1). Calves acquire passive immunity by consuming colostrum in the first 24 to 36 h of life (1,2). Inadequate colostrum consumption leads to failure of passive transfer (FPT), which has detrimental effects on calf health and survival. As many as 40% of dairy calves experience FPT (3,4). However, beef and dairy calf management is considerably different, as beef calves generally remain with the cow post-calving and nurse ad libitum, while dairy producers often separate calves from their dams and then provide the colostrum. Hence, the prevalence of and risk factors for FPT in beef calves may vary substantially from those in reports describing dairy calves.

Inadequate passive transfer is associated with increased morbidity and mortality before weaning (5,6). Negative health effects can continue into the feeding period (5). Thus, identifying risk factors for FPT in calves could have substantial implications for the Canadian beef industry. One Canadian study, which described predictors of serum IgG concentrations in beef calves in Quebec, found that calves born in stanchions were at increased risk for FPT (7). While this study provided useful regional information, risk factors for FPT, such as calving management, are different in other areas of Canada. For example, most beef calves in western Canada are born outside (8). Understanding the frequency of and risk factors for FPT in western Canada is important, because almost 70% of Canada’s 5 million beef cows are located in Alberta and Saskatchewan. Feedlots in Alberta produce 67% of the 3.4 million head of finished cattle in Canada and 80% of Canada’s fed cattle production occurs in Alberta and Saskatchewan (9,10). The objectives of this study were to describe the prevalence of, and predictors for, serum immunoglobulin (Ig) G concentrations in beef calves from Alberta and Saskatchewan, and to investigate the relationship between serum IgG concentrations and health events in the first 3 mo of life.

Materials and methods

Herd and sample selection

The calves described in this survey were a convenience sample from a subset of 203 beef herds that participated in a multifaceted survey of risk factors affecting the productivity and health of cow-calf herds in western Canada (11). Private veterinary clinics across Alberta, Saskatchewan, and northeastern British Columbia were asked to participate. Within each practice, herds were enrolled, based on selection criteria that considered herd size, completeness of animal identification, existing calving records, presence of animal handling facilities, and a relationship with a local veterinary clinic. Herds of fewer than 50 animals were not included. Only herds using a winter/spring calving season were enrolled in the study. One of 6 project veterinarians regularly visited each herd to collect samples and data, and to monitor the quality and consistency of on-farm records.

Samples were collected, during a single herd visit from February 1 to June 30, 2002, from the initial, individually identified calves that were successfully restrained in the calving and nursery areas. The number of calf samples collected per herd was determined by the number of accessible animals and was limited by the budget available and the willingness of the producer to participate. Blood samples were collected by jugular venipuncture, using 10-mL vacuum tubes (BD Vacutainer tubes; Becton Dickinson, Franklin Lakes, New Jersey, USA). All samples were transported on ice to the laboratory (Prairie Diagnostic Laboratories, Saskatoon, Saskatchewan).

Radial immunodiffusion for serum antibody determination

Serum IgG concentrations were assessed to measure the success of passive transfer in each calf. A 1% agarose (SeaKem ME; Lonza Group, Basel, Switzerland) solution was prepared by adding 1 g of agarose to 100 mL of phosphate buffered saline (pH 7.4) and heating the mixture to boiling point to dissolve the agarose. The agarose solution was cooled for 15 to 20 min by immersing it in a water bath set at 56°C. Rabbit anti-bovine IgG (Jackson Laboratories, West Grove, Pennsylvania, USA) was added to give a final concentration of 3%. After thorough mixing, 15 mL of the solution was poured onto leveled clear plastic plates (10 × 8.5 cm) and allowed to gel at room temperature for 15 min. Circles were punched in the gel and the encircled gel was aspirated, creating a series of 2.5-mm wells. Four microliters of standard bovine antiserum (Bethyl Laboratories, Montgomery, Texas, USA) containing 28 g/L of IgG was added to the wells; 5 two-fold dilutions were used, beginning at a 1:4 dilution (7 g/L). Test sera were diluted 1:10, providing an effective range of 4.73–70 g/L. The gel plates were incubated at room temperature in a humidified chamber for 16 to 18 h. The diameters of the resulting immunoprecipitation rings were measured. A linear regression equation, developed previously in the laboratory, related zone diameters to the log concentration of known serial dilutions. This equation was used to interpolate the test sera IgG concentrations with an R2 ≥ 0.98 (Prairie Diagnostic Laboratories, Saskatoon, Saskatchewan).

Risk factors, herd management, and reproduction data

All data for this investigation were collected between April 1, 2001 and June 30, 2002. Following their enrollment, producers used standard forms to prospectively maintain records on animal inventory and health. These data were provided to the veterinarians involved in the project during herd visits in the fall of 2001, before the calving season in 2002, and during the calving season in 2002. During these visits, additional data were collected on herd-level and cow-level risk factors that potentially were associated with calf serum IgG concentrations, using standard forms.

Project veterinarians established the initial inventory of study herds in the fall of 2001. By using records provided by each herd owner, the veterinarian recorded the individual identification of each cow, along with her age and breed, whether she was born on the farm or purchased, and the date of purchase. Throughout the study, animals removed from the herd were recorded, along with the date and reasons for their removal. The accuracy of inventory records was verified during on-farm visits.

Project veterinarians conducted herd visits during the fall of 2001 to pregnancy test and record a body condition score (BCS) (using a 9-point scale) for all cows in the study herds (12). Before the calving season in 2002, the veterinarians visited each herd to record each cow’s BCS, and to collect data on feeding management, using a standard questionnaire. A 3rd visit occurred during the calving season to collect blood samples from the calves and, using a standard form, data on risk factors for calf mortality and disease and postcalving feeding management. Detailed calving records that had been prospectively maintained by herd owners were provided to the project veterinarians. For each cow that calved during the study period, the cow identification, date of calving, single or twin birth, calf sex, degree of assistance provided to the cow, and description of any calving problems were recorded. Owners also recorded the dates of all calf losses. Calf mortality was defined as a calf that died more than 1 h after birth and before the earlier of 3 mo of age or June 30.

Treatment information was based on records provided by the herd owner and was defined as any pharmaceutical, other than vaccines, given to a calf for therapeutic or prophylactic indications. Again, the period of interest was from 1 h after birth to the earlier of 3 mo of age or June 30; this cutoff date minimized data inaccuracies and incomplete records that occurred after calves were on summer pasture. The risk of treatment for any reason, diarrhea (scours/enteritis/colitis), pneumonia, and omphalitis (navel ill), was also determined, based on herd owner records of reason for treatment.

Meteorological data

All winter housing and calving areas were plotted on an electronic map of western Canada (ArcView GIS 3.2; ESRI, Redlands, California, USA). The locations of stations providing daily temperature data were obtained from Environment Canada and added to the GIS database. Average daily temperatures were determined for the meteorological station closest to each full-term calf born from December 1, 2001 to June 30, 2002.

Data comparisons and statistical analysis

Calf- and herd-level factors were summarized, using commercially available software (Microsoft Excel; Microsoft Corporation, Redmond, Washington, USA). Generalized linear mixed models were used to estimate the association between potentially related factors and the outcomes of interest (PROC MIXED; SAS version 9.1.3, SAS Institute, Cary, North Carolina, USA). Predictors of serum IgG concentrations were examined, using a normal distribution, and models were adjusted for clustering by including a random intercept for each herd. Factors examined included calf gender, calf age at sampling, twin birth, history of assistance at birth, perinatal cow health problems, birth month, average ambient temperature on the calving date, BCS of cow at pregnancy detection, cow breed, and cow age. Management factors (dichotomized as yes/no) considered as potential predictors of serum IgG concentrations included the following: separation of cows close to parturition from rest of herd, separation of pregnant and postpartum cows, calving heifers before the cow herd, the presence of handling facilities for dystocia, the presence of lights in the calving pens for night-checking, and adequate bedding in the calving area. Finally, 3 colostrum management practices were considered; namely, ensuring calves receive colostrum within 12 h of birth, storage of frozen colostrum from cows in own herd, and purchasing frozen colostrum from a neighboring dairy farm.

The following 5 calf health outcomes were examined for their relationship with serum IgG concentrations: calf death, calf treatment for any reason, and treatment for diarrhea, pneumonia, or navel ill. Models had a binomial distribution and logit link function and used generalized estimating equations (PROC GENMOD; SAS Institute) to adjust for clustering by herd. The relationship between serum IgG concentrations and health events was the primary interest; thus, serum IgG concentration was forced into all models either as a continuous variable or as 1 of 3 dichotomous variables: failure of passive transfer (IgG concentrations ≤ 8 g/L), inadequate passive transfer (IgG concentrations ≤ 16 g/L), or optimal passive transfer (IgG concentrations > 24 g/L) (5,6). Other factors considered in the models of health outcomes included cow age and breed, calf age at sampling, calf gender, calving month, and history of assistance at calving. Herd-level factors considered included colostrum management, use of vitamin E/selenium injections in calves, the use of bedding and shelters in the calving facility, removal of calves from calving facility to nursery pasture within 48 h of birth, the purchase of foster calves, and the precalving use of Escherichia coli, rotavirus, and coronavirus vaccines in cows and heifers.

For all models, variables unconditionally associated with the outcome at P < 0.2 were considered further. For continuous predictors and outcomes, each predictor was plotted against its studentized residuals. Variables without substantial fanning were maintained as continuous variables, while those with fanning were categorized. For continuous predictors and dichotomous outcomes, the effect estimate of each quartile was graphed against the log odds of the outcome to assess the relationship for linearity. Nonlinear associations were addressed by categorizing the variable, and the resultant categorical variable was considered further if significant at P < 0.2. All potential risk factors with an unconditional P < 0.2 were included in the full model. Manual stepwise backward selection was used to develop a main effects model, retaining only variables significant at P < 0.05. Those removed from the full model were reintroduced into the main effects model, separately, to ensure that confounding had not caused inappropriate removal. Biologically reasonable first-order interactions were considered and retained in the final model, along with the main effects, if P < 0.05. Residuals of the final models were examined visually for outliers. The association between each variable of interest and dichotomous outcomes were reported as an odds ratio (OR = expβ) with 95% confidence intervals (CI) (13).

Results

A maximum of 20 calves per herd [median = 6 calves, inter-quartile range (IQR) = 5 to 7 calves] were sampled from 152 herds. Participating herds began calving from January 1 to April 30 of 2002, and calves were sampled from February 1 to June 30. The 935 calves were born to 747 cows and 169 heifers, which were predominantly continental and British breeds and crosses (Table 1). Most cows were in good body condition at pregnancy detection, did not require assistance at calving, and were not diagnosed with postcalving health problems, such as uterine prolapse, retained placenta, or metritis (Table 1).

Table 1
Characteristics of all calves (N = 935) sampled, and of calves sampled between 2 and 8 d of age (n = 601), and unconditional associations between these characteristics and serum IgG concentrations in calves sampled between 2 and 8 d (n = 601)

All calves studied were born to a cow from the study herds; no calves were purchased. Seventy-six of the selected calves had a twin, and both calves were sampled from 21 sets of twins. On the day of birth, the average ambient temperature ranged from + 13°C to −32°C with a mean of −9.3°C (s = 9.0). Most calves were healthy for the first 3 mo of life; however, 166 (18%) of the calves were treated by the herd owner with prophylactic or therapeutic pharmaceuticals. The most common conditions requiring treatment were diarrhea (75 calves), pneumonia (27 calves), and omphalitis (31 calves); 46 calves received treatment for other conditions. Thirteen calves were treated for > 1 condition. Twenty-nine calves (3.1%) died prior to 3 mo of age; 18 of these had received treatment prior to death.

At sampling, the calves ranged from < 1 d to 94 d of age (median = 6 d; IQR = 4 to 10 d). Serum IgG concentrations were associated with the calf age at sampling. Calves sampled before 2 d of age had a predicted mean serum IgG concentration of 29.3 g/L (95% CI, 24.1 to 34.5 g/L), those sampled between 2 and 8 d old had predicted mean serum IgG concentration of 30.4 g/L (95% CI, 29.0 to 31.7 g/L), and calves > 8 d old had a predicted mean of 22.7 g/L (95% CI, 21.0 to 24.5 g/L). The serum IgG concentrations of calves sampled at > 8 d old were significantly different from those sampled between 2 and 8 d old (P ≤ 0.0001) and from those samples at < 2 d old (P = 0.02). From 2 to 8 d of age, serum IgG concentrations declined by 1.6 g/L/d (95% CI, 1.0 to 2.2 g/L/d). The rate of decline decreased to 0.24 g/L/d between 9 and 45 d of age (95% CI, 0.14 to 0.34 g/L/d), following which IgG levels plateaued. Subsequent models evaluating factors associated with serum IgG concentrations and the relationship between serum IgG concentrations and health outcomes were restricted to the 601 calves sampled between 2 and 8 d of age. Confounding by age was further addressed by controlling for the age of the calf at sampling.

Of the 601 calves sampled between 2 and 8 d of age, 35 (5.8%) had serum IgG concentrations < 8 g/L, 62 (10.3%) had concentrations between 8 and 16 g/L, 100 (16.6%) were between 16 and 24 g/L, and 404 (67.2%) were > 24 g/L. Data were not collected on how, or if, each calf received colostrum. However, 124 of 152 producers reported that they routinely ensured that calves received colostrum at a volume equal to 10% of their body weight within 12 h of birth. In 74 herds, frozen colostrum was stored from cows in the herd; in 36 herds, frozen colostrum was purchased from a neighboring dairy. These herd management practices were not associated with serum IgG concentrations (P > 0.35).

In a series of unconditional models adjusting only for herd effects, serum IgG concentrations were lower in calves that were twins, required assistance during calving, were born to a heifer, were born to a thin cow (BCS < 5 at pregnancy detection), or were born to a cow with perinatal health problems (Table 1). When considered in a multivariable model, birth to a heifer, twinning, and assistance at parturition remained significant, after adjusting for the decline in serum IgG concentration with each day of age (Table 2).

Table 2
Final model of the associations between calf characteristics and serum IgG concentrations for calves sampled between 2 and 8 d of age (n = 601)

Serum IgG concentrations were not associated with specific treatment for the 3 most common disease conditions in these calves: diarrhea, pneumonia, and omphalitis (Figure 1). However, the odds of treatment for any reason and the odds of death decreased as serum IgG concentrations increased, when evaluated unconditionally (P = 0.03 and 0.03, respectively) (Figure 1). The final models describing the odds of treatment and death included this relationship while identifying higher odds of death and treatment for calves of herd owners not routinely using selenium and vitamin E injections at birth (Table 3). Producers in 84 of the 152 participating herds reported that they routinely administered vitamin E and selenium to calves.

Figure 1
Mean serum IgG concentrations and standard deviation (error bars) in calves sampled between 2 and 8 d of age (n = 601) by adverse health outcomes.
Table 3
Final models of the association between death and treatment and serum IgG concentrations (n = 601)

Calves with serum IgG concentrations < 8 g/L did not have significantly different odds of death or treatment than did calves with serum IgG concentrations above this cutoff (P > 0.25). Likewise, the odds of treatment and mortality were not different between calves with less than marginal and those with adequate passive transfer (cutoff = 16 g/L) (P > 0.25). In contrast, the odds of death were 1.6 times higher (95% CI, 1.1 to 2.3, P= 0.02) in calves with serum IgG concentrations below 24 g/L than in calves with concentrations above this threshold, after accounting for herd selenium and vitamin E use. Similarly, the odds of treatment were higher in calves with serum IgG concentrations below 24 g/L (OR = 1.5; 95% CI, 1.0 to 2.3, P = 0.07) than in calves with concentrations above this threshold, after accounting for selenium/vitamin E injections.

Discussion

Serum IgG concentrations and the effects of FPT on calf health have been thoroughly described in dairy calves (3,4,1416). However, few studies have investigated risk factors for FPT in beef calves and these described either calves in research herds or singleton calves born without dystocia (6,7). To our knowledge, this is the 1st study to describe serum IgG concentrations in North American beef herds without such restrictions. This study of 935 calves from 152 herds provides an extensive description of serum IgG concentrations in western Canadian beef calves and examines factors associated with passive transfer.

Enterocytes absorb intact immunoglobulins during the first 36 h of life, causing serum IgG concentrations to peak around 32 h (1,2). Concentration levels then decline until the production of antibodies exceeds the decay of passively acquired antibodies (2,17). In this study, calves were selected based on their presence in the calving area at the time of sampling. This sampling strategy caused a wide age-range of calves to be selected. The risk factor analysis excluded calves < 2 d old to avoid including animals that had not achieved peak IgG levels. Calves between 2 and 8 d old were studied, because the IgG levels were declining at a steady rate of 1.6 g/L/d. Calves older than 8 d had a decreased rate of antibody decline, presumably due to their active production of antibodies, and were excluded from the risk factor analysis. Other investigators have also studied serum IgG concentrations in calves between 2 and 8 d of age (3,7,16,18). Although Filteau et al (7) did not find an association between IgG levels and age, others (18), like us, have also found it necessary to control for age when describing serum IgG concentrations in this age range.

Serum IgG concentrations were associated with 3 calving factors: twinning, dystocia, and birth to a heifer. Recent studies of FPT in beef cattle have excluded calves from non-normal births (6,7); however, twinning and dystocia have been associated with FPT in dairy cattle (1921). Each of these factors can prolong birth, which increases the risk of acidosis. Acidotic calves have decreased vigor, take longer to nurse, and may be too weak to consume adequate volumes of colostrum (1,19). In a study that controlled the timing and volume of colostrum consumption, calves with respiratory acidosis had lower serum IgG concentrations at 12 h than did calves with normal blood levels. Thus, in addition to decreased volume or pH and PCO2 delayed consumption of colostrum, acidotic calves may absorb immunoglobulins less efficiently (22).

Heifers may have a lower volume, concentration, or quality of colostrum than have mature cows, although numerous studies in Holstein cattle have found no difference between colostrum IgG1 concentrations from heifers and cows with other parities (1,19). Subjectively, heifers may have poorer quality colostrum, if their exposure to endemic pathogens on the farm has been limited because they have been managed separately from the main cow herd (2). Different antibody profiles between mature cows and heifers could provide a biological explanation for the statistical association in these data.

The 3 predictors of serum IgG concentration could delay a calf’s consumption of colostrum, which can affect passive transfer as the gut closure progresses increasingly quickly in calves more than 12 h old (2). Heifers are more likely than mature cows to reject their calf, which prevents or delays suckling (23). Similarly, dystocia increases the risk of calf or cow injury and fatigue, which may delay colostrum consumption. Twins plausibly could each receive less colostrum. This is exacerbated if a producer assumes that both calves have received colostrum based on the fullness of the cow’s mammary glands. Close supervision is needed to determine if both calves have suckled.

In a study in Quebec, beef calves were more likely to experience FPT if they were born in a stanchion rather than a pen (7). The authors of this study speculated that stanchions restricted maternal bonding and that calves took longer to stand on cement flooring, thus delaying colostrum consumption. Although few beef calves in western Canada are born in stanchions, the risk factors identified in the present study could also lead to delayed colostrum consumption, resulting in lower serum IgG concentrations. Filteau et al (7) found that bottle-fed calves were less likely to have FPT than were calves left without assistance or calves led to the mammary gland. Individual calf-level data on the route of colostrum consumption were not collected in our study. However, the results from our study and that of Filteau et al (7) collectively indicate that interventions to ensure that high risk calves consume adequate colostrum should maximize serum IgG concentrations.

Other investigators have found that beef calves with FPT are at greater risk for adverse health outcomes (6). In contrast, we found in this study that calves with FPT (serum IgG concentrations < 8 g/L) and calves with levels below adequate passive transfer (serum IgG concentrations <16 g/L) were not at greater risk for these negative health outcomes. This apparent contradiction is probably because few of the calves that were sampled in this study had marginal or failed passive transfer, resulting in insufficient power to identify such relationships. However, increasing serum IgG concentrations were associated with decreased odds of treatment and mortality in these calves. Most importantly, the odds of a negative health outcome decreased with increasing serum IgG concentrations at levels well above the traditional definition for FPT.

In a previous study, a serum IgG threshold of 24 g/L was found to be most useful for describing the likelihood of morbidity and mortality in beef calves (6). In that study, this degree of passive transfer optimized health and production before weaning. In our study, calves with IgG levels > 24 g/L were at significantly lower odds of death or treatment before 3 mo of age. Together, these studies contradict the dogma that improving passive transfer beyond adequate levels is of little value (1). In fact, our findings directly contradict recommendations that dairy producers only aim for serum total protein levels above 50 g/L (roughly equivalent to serum IgG levels > 10 g/L), because this is reasonable and attainable (3). Instead, beef producers should aim to maximize passive transfer and optimize the protective health benefits of colostrum.

Calves born in herds where producers routinely administered combined selenium and vitamin E injections had substantially lower odds of receiving treatment and of dying than did calves born into herds not using this management intervention. Selenium is an essential micronutrient that works with vitamin E to protect cell membranes. Their role in immune protection and in beef cow and calf health are becoming increasingly recognized (24,25). Vitamin E does not cross the placenta, making calves dependent on vitamin E from colostrum (26). Selenium readily crosses the placenta and is also available to calves in colostrum (26,27). However, cows supplemented with selenium can still have inadequate selenium in their colostrum (28). The selenium status of calves in Alberta and Saskatchewan has not been described; however, selenium deficiency is common in the black and grey wooded soils of Saskatchewan and Alberta (29). These findings indicate that the relationship between selenium status and beef cattle health in this region warrants further study.

Failure of passive transfer was relatively uncommon in these western Canadian beef calves compared with that reported for North American dairy calves (4). Although FPT was relatively uncommon, calves with serum IgG concentrations < 24 g/L (a level of passive immunity traditionally considered adequate) faced an increased chance of death and treatment. This demonstrates the importance of neonatal calf management on subsequent health. Calves born to heifers, as twins, or from difficult births were more likely to have low serum IgG levels. Identifying calves at risk for low serum IgG concentrations will assist beef producers’ efforts to ensure that calves receive adequate colostrum early in life.

Acknowledgments

The data in this paper were collected as part of the field research activities for the Western Canada Study of the Animal Health Effects Associated with Exposure to Emissions from Oil and Natural Gas Field Facilities. CVJ

Footnotes

Authors’ contributions

Dr. Waldner was responsible for the design, implementation, and management of all data collection of the study and was involved in the editing and revision of the manuscript. Dr. Rosengren analyzed the data, wrote the manuscript, and was involved in the editing and revision of the manuscript.

Funding for this study was provided by the Western Interprovincial Scientific Studies Association (WISSA), Saskatchewan Cattle Marketing Deductions Fund, and Saskatchewan Horned Cattle Fund.

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