The association between calfhood bovine respiratory disease complex and subsequent departure from the herd, milk production, and reproduction in dairy cattle

Aaron P. Schaffer Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Robert L. Larson Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Natalia Cernicchiaro Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Gregg A. Hanzlicek Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Steven J. Bartle Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Daniel U. Thomson Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Abstract

OBJECTIVE To describe the frequency of calfhood producer-identified bovine respiratory disease complex (BRDC) in Holstein replacement heifers on 1 large farm and determine associations between development of BRDC at ≤ 120 days of age (BRDC120) with milk production estimate, calving interval, and risk of departure from the herd (DFH).

DESIGN Retrospective, observational study.

ANIMALS 14,024 Holstein heifer calves born on 1 farm.

PROCEDURES Data were obtained from herd management records. Cox proportional hazard and generalized linear mixed-effects models were used to assess associations for variables of interest (BRDC120 status, demographic data, and management factors) with DFH, milk production estimate, and calving interval.

RESULTS Except for the year 2007, animals identified as having BRDC120 were 1.62 to 4.98 times as likely to leave the herd before first calving, compared with those that did not have this designation. Calves identified as having BRDC prior to weaning were 2.62 times as likely to have DFH before first calving as those classified as developing BRDC after weaning. Cows identified as having BRDC120 were 1.28 times as likely to have DFH between the first and second calving as were other cows. The BRDC120 designation was associated with a 233-kg (513-lb) lower 305-day mature equivalent value for first lactation milk production, but was not associated with longer or shorter calving intervals at maturity.

CONCLUSIONS AND CLINICAL RELEVANCE Dairy cattle identified as having BRDC120 had increased risk of DFH before the first or second calving and lower first-lactation milk production estimates, compared with results for cattle without this finding. Further investigation of these associations is warranted.

Abstract

OBJECTIVE To describe the frequency of calfhood producer-identified bovine respiratory disease complex (BRDC) in Holstein replacement heifers on 1 large farm and determine associations between development of BRDC at ≤ 120 days of age (BRDC120) with milk production estimate, calving interval, and risk of departure from the herd (DFH).

DESIGN Retrospective, observational study.

ANIMALS 14,024 Holstein heifer calves born on 1 farm.

PROCEDURES Data were obtained from herd management records. Cox proportional hazard and generalized linear mixed-effects models were used to assess associations for variables of interest (BRDC120 status, demographic data, and management factors) with DFH, milk production estimate, and calving interval.

RESULTS Except for the year 2007, animals identified as having BRDC120 were 1.62 to 4.98 times as likely to leave the herd before first calving, compared with those that did not have this designation. Calves identified as having BRDC prior to weaning were 2.62 times as likely to have DFH before first calving as those classified as developing BRDC after weaning. Cows identified as having BRDC120 were 1.28 times as likely to have DFH between the first and second calving as were other cows. The BRDC120 designation was associated with a 233-kg (513-lb) lower 305-day mature equivalent value for first lactation milk production, but was not associated with longer or shorter calving intervals at maturity.

CONCLUSIONS AND CLINICAL RELEVANCE Dairy cattle identified as having BRDC120 had increased risk of DFH before the first or second calving and lower first-lactation milk production estimates, compared with results for cattle without this finding. Further investigation of these associations is warranted.

Bovine respiratory disease complex is a multifaceted disease caused by a combination of viral and bacterial pathogens that affect immunosuppressed calves. In dairy cattle, Pasteurella multocida is the most common bacterial pathogen; however, Mannheimia haemolytica, Histophilus somni, and Mycoplasma bovis have been also implicated in causing disease.1,2 Viruses commonly associated with BRDC in cattle include bovine viral diarrhea virus, bovine respiratory syncytial virus, bovine herpes virus-1, and parainfluenza type 3 virus.2

Bovine respiratory disease complex is associated with considerable economic costs. One economic model created in 20013 to assess losses associated with this disease on a typical Dutch dairy farm provided BRDC-associated cost estimates equivalent to $24 to $77 2014 US dollars/heifer present at the dairy (reported cost in euros converted with an online calculatora). However, it is difficult to determine a true cost of calfhood BRDC, considering that little is known about the long-term implications for subsequent productivity at maturity. Results of some studies4,5 have revealed that calfhood BRDC decreased survival in the herd prior to first calving, but these same studies had conflicting results regarding the association between calfhood BRDC and age at first calving. Other studies5–7 failed to find an association of calfhood BRDC with decreased survival in the herd after calving or an association between calfhood BRDC and first lactation production.

With the exception of those few studies,5–7 little research has been conducted to examine the effects of calfhood BRDC in dairy replacement heifers on subsequent milk production and reproductive variables after first calving. The excellent health and production records kept by the dairy industry and by individual dairies provide an opportunity to evaluate associations of demographic and management factors with production and reproduction variables through the use of existing data sets. Such evaluation could provide dairy managers with valuable information to assist key management decisions.

The objective of the study reported here was to describe the frequency of development of calfhood BRDC in Holstein replacement dairy heifers as identified by farm production staff and to determine associations of producer-identified BRDC120, as well as other demographic and management factors, with milk production, calving interval, and the subsequent risk of DFH on a large commercial dairy cattle operation in central Utah.

Materials and Methods

Animals

Cattle present in the herd of a commercial 5,000-cow dairy farm located near Provo, Utah, from January 1, 2007, to November 11, 2012, were included in the retrospective study. Data were collected from farm records by use of herd management software.b All calves were born on the farm and raised according to industry standards at the time of the study. Calves were housed in individual hutches from shortly after birth until they were weaned and then moved into group housing at approximately 60 days of age. At approximately 120 days of age, calves were moved into open-lot grower pens where they were managed as replacement heifers and bred at approximately 13 months of age. After calving, they were moved into the milking herd and housed in multiple free-stall barns.

Case selection

All calves ≤ 120 days of age at the time of record collection were excluded from the analysis because they were still at risk for developing calfhood BRDC. In this study, 120 days of age was chosen as the cutoff, as this was the approximate age at which calves moved from group housing into open-lot grower pens. For records to be included in the analysis of the various milk production or calving interval variables, an animal could not have departed from the herd before the date recorded for the event and had to have complete data for management, milk production, reproductive, and demographic variables.

A calf was assessed as having BRDC120 if it had been treated at least once for respiratory disease by a trained animal health technician during the first 120 days of age. An animal was determined to have BRDC if it had any combination of the following clinical signs: depression, droopy ears, nasal discharge, ocular discharge, decreased appetite, coughing, difficulty breathing, and rectal temperature > 39.5°C (103.1°F). The overall incidence rate of producer-identified BRDC120 by year was calculated by dividing the number of new cases of BRDC120 each year by the number of animals born that year, and the case fatality rate was calculated by dividing the number of deaths attributed to BRDC each year by the number of new cases of BRDC120 identified each year. A death was attributed to BRDC if the most recent health record indicated the animal had BRDC. The incidence rate of producer-identified BRDC by week of age was calculated by dividing the number of new cases per age group by the number of animal-days at risk in that age group. The date of DFH was defined as the date of death or removal from the farm.

Model building and statistical analysis

All models were constructed in a similar manner. Initially, a causal web diagram was constructed to visualize potential associations between independent variables and outcome variables. Next, a univariable analysis was performed to model the association of each independent variable with the outcome. Any variable with a P value ≤ 0.40 was retained in the model to ensure that all potentially significant variables were considered for inclusion in the multivariable analysis. Following the univariable analysis, both Pearson and Spearman correlation analyses of the variables were performed to ensure that if 2 variables were collinear (r > |0.8|), both were not included in the multivariable analysis. The linearity assumption for all continuous variables was evaluated with graphic methods; if the linearity assumption was not met, the variables were categorized.

The main-effects model was constructed with variables that passed the univariable screening and were identified by assessment of the causal web diagram. After all significant (P < 0.05) main effects were included in the model, some variables considered a priori confounders in the causal web model were assessed for confounding by introducing them individually and evaluating for a change of > 20% to 30% in the coefficients of the main effects. Two-way interactions were constructed between potential confounders or effect modifiers, which were considered a priori on the basis of assessment of causal models, and main effects were tested by adding 1 interaction at a time in the model. Only significant (P < 0.05) interactions were kept. The final model was built including all significant main effects, 2-way interactions, and a random intercept for weekly cohorts. Finally, distribution of the best linear unbiased predictors of the cohort variable was plotted to ensure normality, and residuals (eg, Martingale and deviance residuals for survival models) at the lower level (ie, data for calves) were also plotted to evaluate the functional form of the model and to check for potential outliers and influential observations. The distribution of the best linear unbiased predictors appeared normal, and no outliers were identified.

Dependent variables included DFH, lactation-1 milk production, lactation-2 milk production, and calving interval. Days at risk for DFH prior to first calving was modeled as a continuous variable and was calculated as the total number of days between birth and either DFH or first calving. The number of days at risk for DFH between the first and second calving was defined as the number of days between first calving and either DFH or calving a second time, and the number of days at risk between second and third calving was defined as the number of days between second calving and either DFH or calving a third time. For each of the 3 time intervals, animals that had not departed from the herd and had not reached the end of that respective time interval at the end of data collection were censored.

Milk production was adjusted through the herd management softwareb for location, age, and season of calving to a mature-cow basis, and the data were used to project a 305-day lactation production value, designated as the 305ME value. Calving interval for each cow was defined as the number of months between 2 sequential calvings and was calculated by determining the number of days between sequential calvings and dividing this number by 30. Calving interval was then categorized as < 12.0, 12.0 to 13.4, 13.5 to 15.0, and > 15.0 months on the basis of previous research designs.8

Independent variables included in the different models were as follows: birth year, birth season, season in which BRDC120 was identified, calving season, age at first calving, milk production, presence of producer-identified BRDC120, age at BRDC determination, and duration of the calving interval. The birth year was defined as calendar year and modeled as a categorical variable, where each year from 2007 through 2012 represented 1 category. Seasons for the various analyses were defined as follows: winter (December 1 to the end of February [mean temperature consistently < 4°C]), spring (March 1 to the end of May [mean temperature increasing from 4° to 16°C]), summer (June 1 to the end of September [mean temperature consistently > 16°C]), and fall (October 1 to the end of November [mean temperature decreasing from 16° to 4°C]) on the basis of ambient temperatures for the experimental period recorded for Provo, Utah.c Milk production was originally recorded and modeled on a continuous scale, but when modeled as an independent variable, the data did not meet the linearity assumption; therefore, it was categorized on the basis of quartiles. Lactation-1 milk production was categorized as follows: 3,383 to 11,885 kg (7,443 to 26,147 lb), 11,886 to 13,224 kg (26,149 to 29,093 lb), 13,225 to 14,473 kg (29,095 to 31,841 lb), and 14,474 to 19,761 kg (31,843 to 43,474 lb). For lactation-2 milk production, quartiles were as follows: 4,594 to 12,517 kg (10,107 to 27,537 lb), 12,518 to 13,855 kg (27,540 to 30,481 lb), 13,856 to 15,080 kg (30,483 to 33,176 lb), and 15,081 to 19,631 kg (33,178 to 43,188 lb). Producer-identified BRDC120 was modeled as a dichotomous predictor on the basis of whether it was reported before (through 60 days of age) or after (from 61 through 120 days of age) weaning according to the date of birth. Age at first calving was modeled as a continuous variable ranging from 19.0 to 31.0 months. Calving interval, when considered as an explanatory variable, was modeled in a manner similar to that used when it was considered as an outcome variable.

Commercially available software was used for statistical analysis.d A multivariable Cox proportional hazards analysis was used to model associations between demographic or management variables and DFH. A generalized linear mixed-effects multivariable model was used to model associations between variables of interest and milk production, and a mixed-effects multivariable model was used for analysis of associations between demographic or management variables and calving interval. Mixed models used a Gaussian distribution, identity link, maximum likelihood estimation, and Kenward-Rogers degrees of freedom for models pertaining to lactation-1 and lactation-2 milk production outcomes, and a multinomial distribution and quadrature estimation for the outcome pertaining to calving interval. In all models, a weekly cohort variable, created on the basis of date of birth, was included as random intercept.

Results

On examination of records, 927 of 14,969 (6.2%) calves born on the study farm were excluded from the analysis because they were still at risk for developing calfhood BRDC. Eighteen additional animals were excluded from the study because the reported dates of BRDC identification or calving dates were not compatible with the reported date of DFH. Of the 14,024 cows included in the study, 868 (6.2%) were categorized as having BRDC120 (Table 1). Of those animals, 177 died, resulting in an overall mortality rate of 1.3% attributable to BRDC and a case fatality rate of 20.4%. The incidence rate of producer-identified BRDC120 was 0.056 cases/100 animal-days at risk. The highest reported incidence of BRDC was during the first week of age (0.24 cases/100 animal-days at risk), and the lowest incidence was during the 9th and 18th weeks of age (0 cases/100 animal-days at risk; Table 2).

Table 1—

Incidence of producer-identified BRDC120 and case fatality risk by birth year for 14,024 Holstein heifer calves on 1 large farm in Provo, Utah, in a retrospective study to describe the frequency of the disease in this population and assess associations of BRDC120 with subsequent milk production, calving interval, and subsequent risk of DFH.

YearNo. of calves born (% of total)No. of cases of BRDC (% of calves born)No. of deaths attributed to BRDC (case fatality risk [%])
20072,042 (14.6)111 (5.4)12 (10.8)
20082,351 (16.8)306 (13.0)58 (19.0)
20092,521 (18.0)162 (6.4)44 (27.2)
20102,864 (20.4)53 (1.9)10 (18.9)
20112,642 (18.8)64 (2.4)15 (23.4)
20121,604 (11.4)172 (10.7)38 (22.I)
Total14,024868 (6.2)177 (20.4)

Data were collected by use of farm management software. A calf was determined to have BRDC120 if it had been treated at least once for respiratory disease by a trained animal health technician during this time. An animal was determined to have BRDC if it had any combination of the following clinical signs: depression, droopy ears, nasal discharge, ocular discharge, decreased appetite, coughing, difficulty breathing, and rectal temperature > 39.5°C (103.1°F).

Table 2—

Proportions of animals with producer-identified BRDC120 and incidence rate/100 animal-days for the 868 affected calves in Table 1, categorized by age at the time BRDC was identified.

Age (wk)No. of affected calves (% of total)Incidence rate/100 animal-days
1229 (26.4)0.24
262 (7.I)0.07
348 (5.5)0.05
430 (3.5)0.03
533 (3.8)0.04
619 (2.2)0.02
717 (2.0)0.02
816 (1.8)0.02
93 (0.4)0.00
1012 (1.4)0.01
1121 (2.4)0.02
1237 (4.3)0.04
1378 (9.0)0.08
1494 (10.8)0.10
1573 (8.4)0.07
1647 (5.4)0.05
1744 (5.1)0.04
18*5 (0.6)0.00

Includes only data from the first day of the 18th week.

DFH

Of the 14,024 heifers, 2,590 (18%) departed from the herd prior to first calving. Only 2,288 of 13,156 (17%) heifers not identified as having BRDC120 had DFH prior to first calving, compared with 302 of 868 (35%) heifers reported as having BRDC120. The multivariable model of the associations between independent variables and DFH prior to first calving indicated a significant (P < 0.001) interaction between birth year and BRDC120 associated with DFH prior to first calving; there were no other independent variables significantly associated with this outcome. Because of this finding, associations between BRDC status and outcome were summarized by birth year (Table 3). The analysis indicated that the designation of having BRDC120 in all birth years except 2007 was significantly associated with DFH prior to first calving, with hazard ratios for this outcome for affected animals ranging from 1.62 to 4.98 (P < 0.001 for all comparisons) for the years 2008 through 2012, compared with those for animals of the same birth year that were not identified as having had the disease.

Table 3—

Results of multivariable Cox proportional hazards analysis for DFH prior to first calving for the same 14,024 heifers as in Table I.

Birth yearHR (95% CI)P value
20071.03 (0.63–1.69)0.916
20081.62 (1.30–2.03)< 0.001
20092.06 (1.59–2.66)< 0.001
20102.58 (1.70–3.92)< 0.001
20113.71 (2.52–5.47)< 0.001
20124.98 (3.74–6.65)< 0.001

The hazard ratio (HR) represents the risk for the outcome of interest for animals that were categorized as having BRDC120, compared with those that were not.

CI = Confidence interval.

Of the 868 animals with a record of having BRDC120, 454 (52%) developed the illness before weaning (through 60 days of age) and 414 (48%) became ill after weaning (61 through 120 days of age). Among calves that became ill before weaning, 201 of 454 (44%) had DFH prior to first calving, compared with 101 of 414 (24%) calves that became ill after weaning. The analysis of the relationship between independent variables and DFH prior to first calving for animals identified as having BRDC120 showed that, for those identified as having BRDC before weaning, the hazard for DFH prior to first calving was 2.62 times that of those found to develop the disease after weaning (P < 0.001; Table 4). In addition, birth year (2008 through 2012 vs a referent of 2007) was significantly associated with a greater hazard for DFH prior to first calving (P ≤ 0.009 for all comparisons).

Table 4—

Results of multivariable Cox proportional hazards analysis for associations of age (categorized by weaning status) at the time of BRDC identification and birth year with DFH prior to first calving for the 868 animals in Table 1.

VariableCategoryCoefficientSEHR (95% CI)P value*
Age at BRDC identificationBefore weaning0.960.132.62 (2.02–3.41)< 0.001
 After weaningReferenceReferenceReference (NA)Reference
Birth year2007ReferenceReferenceReference (NA)Reference
 20080.740.282.09 (1.21–3.64)0.009
 20091.270.293.56 (2.01–6.31)< 0.001
 20101.190.343.29 (1.69–6.41)< 0.001
 20111.700.335.50 (2.89–10.47)< 0.001
 20122.190.308.91 (4.93–16.12)< 0.001

Calves were weaned at approximately 60 days of age.

P value derived from F test.

NA = Not applicable.

See Table 3 for remainder of key.

In total, 7,287 of the 14,024 (52%) study cattle had complete data and were included in the analysis of DFH between first and second calving. Heifers from birth years 2011 and 2012 did not have complete data and were not included in the analysis. Of the cows that had complete records, 430 (6%) were identified as having had BRDC120. Of those 430 animals, 124 (29%) departed from the herd between first and second calving, compared with 1,418 of 6,857 (21%) cows that did not have this designation. Analysis of associations between independent variables and DFH between first and second calving revealed that animals categorized as having BRDC120 were 1.28 times as likely to have DFH between first and second calving as those that were not (P = 0.023; Table 5). Birth year (for years 2009 and 2010 vs the referent of 2007), quartile for lactation-1 milk production (for the 3 highest production categories vs the referent of lowest production category), and age at first calving were also all significantly (P < 0.001 for all comparisons) associated with risk of DFH between first and second calving, with a higher risk associated with later birth years and age at first calving and a lower risk associated with higher milk production categories.

Table 5—

Results of multivariable Cox proportional hazards analysis for associations between variables of interest (presence of producer-identified BRDC120, birth year, 305ME lactation-1 milk production estimate, and age at first calving) and DFH between the first and second calving for 7,287 of the animals in Table 1 that had data available.

VariableCategoryCoefficientSEHR (95% CI)P value*
BRDCNoReferenceReferenceReference (NA)Reference
 Yes0.250.121.28 (1.03–1.59)0.025
Birth year2007ReferenceReferenceReference (NA)Reference
 2008−0.070.090.93 (0.78–1.11)0.432
 20090.510.091.67 (1.39–2.01)< 0.001
 20100.440.111.56 (1.26–1.93)< 0.001
Lactation-1 production (kg)3,383–11,885ReferenceReferenceReference (NA)Reference
 11,886–13,224−1.480.080.23 (0.20–0.26)< 0.001
 13,225–14,473−1.960.090.14 (0.12–0.17)< 0.001
 14,474–19,761−2.330.100.10 (0.08–0.12)< 0.001
Age at first calvingContinuous0.080.021.08 (1.04–1.13)< 0.001

To convert milk production in kilograms to pounds, multiply by 2.2.

For analysis, age at first calving was considered a continuous variable ranging from 19.0 to 31.0 months.

See Tables 3 and 4 for remainder of key.

Of the 430 calves that were categorized as having BRDC120 and remained in the herd until second calving, 222 (52%) and 208 (48%) were identified as having the disease before and after weaning, respectively, and although identification of BRDC120 was positively associated with DFH between first and second calving, the age at which BRDC reportedly developed (before or after weaning at approx 60 days of age) was not associated (P = 0.76) with this outcome. Sixty-seven of 222 (30%) animals that had the illness before weaning, and 57 of 208 (27%) of those that had the illness after weaning had DFH between the first and second calving.

A total of 4,011 cows had complete data sets for DFH available for use in the analysis of DFH between second and third calving, and of those, 262 (7%) were identified as having had BRDC120. The model of the independent variables associated with DFH did not find an association between BRDC120 classification and DFH between second and third calving (P = 0.51).

Milk production and calving interval

In total, 4,005 cows had complete data sets for lactation-1 production and were included in this analysis. Of those 4,005 cows, 261 (7%) had producer-identified BRDC120. There were 1,717 cows that had the complete data to be included in the analysis of lactation-2 production. Of those cows, 7% (126/1,717) were classified as having had BRDC120. The multivariable analysis of the associations between independent variables and lactation-1 production indicated that a classification of having BRDC120 was associated with a 233 ± 113-kg (513 ± 249-lb) lower 305ME lactation-1 production (P = 0.04; Table 6), compared with results for cows that did not have the illness identified. However, there was no association between the identification of BRDC120 and 305ME production in lactation-2 (P = 0.67; Table 7). Birth year and calving interval were both significantly associated with lactation-1 and lactation-2 305ME production. However, the identification of BRDC120 was not associated with a difference in calving interval duration (P = 0.53).

Table 6—

Results of multivariable Cox proportional hazards analysis for associations of producer-identified BRDC120, birth year, and calving interval with 305ME lactation-1 milk production estimates for 4,005 of the animals in Table 1 for which data were available.

VariableCategoryDifference in estimated milk production (95% CI [kg])SEP value*
BRDCYesReference (NA)ReferenceReference
 No233 (11 to 456)1130.040
Birth year2007−327 (−1, 118 to 465)4040.419
 2008−1085 (−1,877 to −294)4040.007
 2009−84 (−876 to 707)4030.834
 2010Reference (NA)ReferenceReference
Calving interval (mo)< 12.0−814 (−998 to −631)94< 0.001
 12.0–13.4−492 (−671 to −314)91< 0.001
 13.5–15.0−228 (−437 to −19)1070.032
 > 15.0Reference (NA)ReferenceReference

Heifers in birth years 2011 and 2012 did not have complete data and were not included in the analysis.

See Tables 3 and 4 for remainder of key.

Table 7—

Results of multivariable Cox proportional hazards analysis for associations of producer-identified BRDC120, birth year, and calving interval with 305ME lactation-2 milk production estimates for 1,717 of the animals in Table 1 for which data were available.

VariableCategoryDifference in estimated milk production (95% CI [kg])SEP value*
BRDC   0.667
 YesReference (NA)ReferenceReference
 No−70 (−391 to 250)1630.667
Birth year   0.049
 2007−831 (−1,489 to −172)3350.014
 2008−781 (−1,439 to −132)3350.020
 2009Reference (NA)ReferenceReference
Calving interval (mo)   < 0.001
 < 12.0−961 (−1,210 to −712)127< 0.001
 12.0–13.4−415 (−658 to −172)1240.008
 13.5–15.0−124 (−406 to 158)1440.388
 > 15.0Reference (NA)ReferenceReference

Heifers in birth years 2010 through 2012 had not completed these data and are not included in the analysis.

Overall P value for test.

See Tables 3 and 4 for remainder of key.

Discussion

Our data indicated that producer-identified BRDC120 was associated with an increased risk of DFH prior to first calving, an increase in risk of DFH between first and second calving, and decreased 305ME lactation-1 milk production. Differences between the results of this study and those of previous studies may be attributable to differences in the numbers of dairy cattle evaluated, geographic location, or different management practices.

Caution must be used when interpreting results of the present study, which was an observational, retrospective study conducted on a single dairy. Thus, it cannot be determined how well these results can be extrapolated to dairies in other geographic locations or under other management practices. In addition, observational studies should not be used to determine causality or to determine which risk factors pertain to duration or disease incidence.9 It is important to note that BRDC was identified by the animal health technicians on the dairy in our study and was therefore dependent on their recognition of clinical signs of BRDC and their documentation of the findings. This is similar to the methods used in previous studies4,10,11 that have been conducted, but it must be considered that diagnosis was not made by veterinarians, that no test for BRDC is 100% sensitive or specific, and that the condition is sometimes misidentified or misdiagnosed.12

In the present study, the incidence rate of producer-identified calfhood BRDC (0.056 cases/100 animal-days at risk) was lower than that reported in another study10 (0.1 cases/100 animal-days at risk). The peak incidence rate in our study was also higher than that in the previous study (0.24 vs 0.18 cases/100 animal-days at risk10), although in both studies, the peak incidence rate was found for calves ≤ 1 week of age. This was unexpected because clinical signs of BRDC are typically not seen until 7 to 10 days after a stressful event,2 and it raises the question of whether farm personnel had accurately identified BRDC in both studies. Following the initial peak in reported BRDC incidence, the incidence in the present study apparently decreased during the next few weeks of age and then began to increase again slightly after 9 weeks of age. Calves in the present study were commingled and moved to group housing at approximately 9 weeks of age. Weaning and commingling, well-known risk factors for BRDC,2 may explain the subjectively observed increase in BRDC incidence after this time.

Similar to the findings for overall incidence rate, the incidence risk of producer-identified BRDC120 in the present study was lower than risks found for young cattle in previous studies.10,13 Sivula et al10 reported the risk of BRDC in calves from birth to 16 weeks of age on 30 Minnesota dairy farms to be 64 of 845 (7.6%), and Virtala et al13 reported the incidence risk of BRDC in calves from birth to 12 weeks of age on dairies in New York state to be 45 of 410 (11%) or 105 of 410 (25.6%), depending on whether status was determined by a caretaker or clinician, respectively. This raises the question of whether variations in incidence are attributable to differences in environmental factors such as temperature, humidity, or precipitation; differences in the ability of farm production staff to accurately identify BRDC; or differences in dairy management strategies. It is interesting to note the high degree of variability for the annual incidence of producer-identified BRDC120 in the present study, which ranged from a high of 306 of 2,351 (13.0%) calves born in 2008 to a low of 53 of 2,864 (1.9%) calves born in 2010. When this was discussed with dairy staff, they commented that they had had some employee compliance issues related to colostrum management and had changed vaccination protocols during this time frame, which supported the value of management strategies as potential risk factors for BRDC.

Although the overall morbidity risk in the present study (868/14,024 [6.2%] calves) was lower than those reported in other publications (64/845 [7.6%]10 and 105/410 [25.6%]14), our overall case fatality risk was higher (177/868 [20.4%] vs 6/64 [9.4%]10). The variation in case fatality risks could be attributable to differences in the ability of calf caregivers to promptly recognize and appropriately treat disease, considering that differences in management strategies in this regard can have a substantial impact on outcomes in dairy calves.

Our finding that heifers identified as having BRDC120 had increased risk for DFH prior to first calving (compared with those that were not identified as having the disease) was consistent with the results of other studies4,5; however, in the present study, this association was dependent on the year of birth. The only birth year in which this variable was not associated with an increase in DFH prior to first calving was 2007. During the remaining years of the study, producer-identified BRDC was associated with a higher risk for DFH. The change in hazard ratios may have reflected a change in culling practices over time. During the early years of the study period, the dairy was expanding from existing stock and was not aggressively culling cattle. In more recent years, the dairy began to cull calves with lower growth performance (compared with others in their same age groups). It was estimated in a previous study15 with beef calves that BRDC decreases growth by as much as 10.6 kg (23.3 lb) from birth to 6 months of age. Therefore, because of the change in culling practices on this dairy, calves deemed to have developed BRDC may have had a greater likelihood of being culled during the later years of the study.

Interestingly, animals identified as having BRDC prior to weaning in the present study were more likely to have DFH prior to first calving than were those found to have BRDC after weaning. To the best of our knowledge, an association between age at the time of BRDC identification and early DFH has not been reported in previous studies. However, the median age of death attributable to BRDC for calves has been reported to be ≤ 60 days,4,16 and therefore, the increased risk of early DFH found for calves designated as having BRDC prior to weaning in the present study may have been attributable to a higher mortality rate among calves of that age group, compared with older calves.

The present study also found a significant association for DFH between first and second calving and BRDC120. This differed from findings of other investigators5,6; however, our study included a larger sample of animals, which may have increased the power to find an association between calfhood BRDC and DFH between first and second calving. It should also be noted that the study reported here was observational, all animals were raised on 1 farm, and there were many factors that could not be measured or controlled for that could have contributed to this difference.

Results of the present study revealed a significantly lower lactation-1 305ME milk production estimate for cattle identified as having BRDC120, compared with results for those that were not. This is different from previous studies5,7,16 in which no association between calfhood BRDC and first lactation milk production was identified. It is also interesting to note that animals born in 2008 had significantly lower projected 305ME milk production than did animals born during 2010. However, similar results were not found for animals born in 2007 and 2009. This is pointed out because 2008 was the birth year for which the highest percentage of BRDC cases was identified, and it raises the possibility that multiple factors could have influenced the risk of BRDC or other conditions that could have been associated with decreased subsequent milk production for calves born that year. It is also important to note that many calves had DFH prior to first calving, and thus, we do not know what the milk production of those calves would have been as they matured; because of this, taken together with a degree of uncertainty in regard to identification of BRDC and unknown contributions of other farm-related factors, a true association between calfhood BRDC and milk production could not be determined. However, the factors in the present study that were significantly associated with producer-identified BRDC120 (greater risk of DFH prior to first or second calving and lower projected milk yield during lactation-1, compared with findings for cattle not identified as having this condition) could substantially affect dairy profitability.

Acknowledgments

This manuscript represents a portion of a thesis submitted by Mr. Schaffer to the Kansas State University Department of Clinical Sciences as partial fulfillment of the requirements for a Master of Science degree.

Supported by the Beef Cattle Institute at Kansas State University.

The authors declare that there were no conflicts of interest.

ABBREVIATIONS

305ME

305-day mature equivalent

BRDC

Bovine respiratory disease complex

BRDC120

Bovine respiratory disease complex at or before 120 days of age

DFH

Departure from the herd

Footnotes

a.

OANDA currency converter, OANDA Corp, Davidson, NC. Available at: www.oanda.com/currency/converter/. Accessed Aug 14, 2013.

b.

DHI-Provo, Provo, Utah.

c.

Weather Underground, The Weather Channel Interactive Inc, Atlanta, Ga. Available at: www.wunderground.com/history/. Accessed Aug 14, 2013.

d.

SAS, version 9.3, SAS Institute Inc, Cary, NC.

References

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  • 2. Griffin D, Chengappa MM, Kuszak J, et al. Bacterial pathogens of the bovine respiratory disease complex. Vet Clin North Am Food Anim Pract 2010; 26: 381394.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. van der Fels-Klerx HJ, Sørensen JT, Jalvingh AW, et al. An economic model to calculate farm-specific losses due to bovine respiratory disease in dairy heifers. Prev Vet Med 2001; 51: 7594.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Waltner-Toews D, Martin SW, Meek AH. The effect of early calfhood health status on survivorship and age at first calving. Can J Vet Res 1986; 50: 314317.

    • Search Google Scholar
    • Export Citation
  • 5. Stanton AL, Kelton DF, LeBlanc SJ, et al. The effect of respiratory disease and a preventative antibiotic treatment on growth, survival, age at first calving, and milk production of dairy heifers. J Dairy Sci 2012; 95: 49504960.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Warnick LD, Erb HN, White ME. The relationship of calfhood morbidity with survival after calving in 25 New York Holstein herds. Prev Vet Med 1997; 31: 263273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Warnick LD, Erb HN, White ME. Lack of association between calf morbidity and subsequent first lactation milk production in 25 New York Holstein herds. J Dairy Sci 1995; 78: 28192830.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Arbel R, Bigun Y, Ezra E, et al. The effect of extended calving intervals in high-yielding lactating cows on milk production and profitability. J Dairy Sci 2001; 84: 600608.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Dohoo IR, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. Charlottetown, PE, Canada: VER Inc, 2009.

  • 10. Sivula NJ, Ames TR, Marsh WE, et al. Descriptive epidemiology of morbidity and mortality in Minnesota dairy heifer calves. Prev Vet Med 1996; 27: 155171.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Windeyer MC, Leslie KE, Godden SM, et al. Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med 2014; 113: 231240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Apley M. Bovine respiratory disease: pathogenesis, clinical signs, and treatment in lightweight calves. Vet Clin North Am Food Anim Pract 2006; 22: 399411.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Virtala AM, Mechor GD, Grohn YT, et al. The effect of calfhood diseases on growth of female dairy calves during the first 3 months of life in New York state. J Dairy Sci 1996; 79: 10401049.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Virtala AM, Mechor GD, Grohn YT, et al. Epidemiologic and pathologic characteristics of respiratory tract disease in dairy heifers during the first three months of life. J Am Vet Med Assoc 1996; 208: 20352042.

    • Search Google Scholar
    • Export Citation
  • 15. Rezac DJ, Thomson DU, Bartle SJ, et al. Prevalence, severity, and relationships of lung lesions, liver abnormalities, and rumen health scores measured at slaughter in beef cattle. J Anim Sci 2014; 92: 25952602.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Curtis CR, Scarlett JM, Erb HN, et al. Path model of individualcalf risk factors for calfhood morbidity and mortality in New York Holstein herds. Prev Vet Med 1988; 6: 4362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 1. Dabo SM, Taylor JD, Confer AW. Pasteurella multocida and bovine respiratory disease. Anim Health Res Rev 2007; 8: 129150.

  • 2. Griffin D, Chengappa MM, Kuszak J, et al. Bacterial pathogens of the bovine respiratory disease complex. Vet Clin North Am Food Anim Pract 2010; 26: 381394.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. van der Fels-Klerx HJ, Sørensen JT, Jalvingh AW, et al. An economic model to calculate farm-specific losses due to bovine respiratory disease in dairy heifers. Prev Vet Med 2001; 51: 7594.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Waltner-Toews D, Martin SW, Meek AH. The effect of early calfhood health status on survivorship and age at first calving. Can J Vet Res 1986; 50: 314317.

    • Search Google Scholar
    • Export Citation
  • 5. Stanton AL, Kelton DF, LeBlanc SJ, et al. The effect of respiratory disease and a preventative antibiotic treatment on growth, survival, age at first calving, and milk production of dairy heifers. J Dairy Sci 2012; 95: 49504960.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Warnick LD, Erb HN, White ME. The relationship of calfhood morbidity with survival after calving in 25 New York Holstein herds. Prev Vet Med 1997; 31: 263273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Warnick LD, Erb HN, White ME. Lack of association between calf morbidity and subsequent first lactation milk production in 25 New York Holstein herds. J Dairy Sci 1995; 78: 28192830.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Arbel R, Bigun Y, Ezra E, et al. The effect of extended calving intervals in high-yielding lactating cows on milk production and profitability. J Dairy Sci 2001; 84: 600608.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Dohoo IR, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. Charlottetown, PE, Canada: VER Inc, 2009.

  • 10. Sivula NJ, Ames TR, Marsh WE, et al. Descriptive epidemiology of morbidity and mortality in Minnesota dairy heifer calves. Prev Vet Med 1996; 27: 155171.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Windeyer MC, Leslie KE, Godden SM, et al. Factors associated with morbidity, mortality, and growth of dairy heifer calves up to 3 months of age. Prev Vet Med 2014; 113: 231240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Apley M. Bovine respiratory disease: pathogenesis, clinical signs, and treatment in lightweight calves. Vet Clin North Am Food Anim Pract 2006; 22: 399411.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Virtala AM, Mechor GD, Grohn YT, et al. The effect of calfhood diseases on growth of female dairy calves during the first 3 months of life in New York state. J Dairy Sci 1996; 79: 10401049.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Virtala AM, Mechor GD, Grohn YT, et al. Epidemiologic and pathologic characteristics of respiratory tract disease in dairy heifers during the first three months of life. J Am Vet Med Assoc 1996; 208: 20352042.

    • Search Google Scholar
    • Export Citation
  • 15. Rezac DJ, Thomson DU, Bartle SJ, et al. Prevalence, severity, and relationships of lung lesions, liver abnormalities, and rumen health scores measured at slaughter in beef cattle. J Anim Sci 2014; 92: 25952602.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Curtis CR, Scarlett JM, Erb HN, et al. Path model of individualcalf risk factors for calfhood morbidity and mortality in New York Holstein herds. Prev Vet Med 1988; 6: 4362.

    • Crossref
    • Search Google Scholar
    • Export Citation

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