Effects of tulathromycin on incidence of various diseases and growth of young heifers

Amy L. Stanton Department of Dairy Science, College of Agriculture and Life Sciences, University of Wisconsin-Madison, Madison, WI 53706.

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David F. Kelton Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, N1G 2W1 ON, Canada.

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Stephen J. LeBlanc Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, N1G 2W1 ON, Canada.

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Jeanne Wormuth CY Heifer Farm, 5327 Watson Rd, Elba, NY 14058.

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Lawrence K. Fox Department of Animal Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164.

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Kenneth E. Leslie Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, N1G 2W1 ON, Canada.

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Abstract

Objective—To determine the effects of administration of 1 dose of tulathromycin on the incidence of various diseases and growth, identify risk factors for slow growth, and determine the association of Mycoplasma bovis status with the incidence of otitis media in calves.

Design—Randomized controlled trial and cross-sectional study.

Animals—788 dairy heifer calves (median age, 3 days).

Procedures—Calves received tulathromycin or a saline (0.9% NaCl) solution control treatment once. Calves were observed daily for 8 weeks by farm staff to detect diseases. Nasal swab specimens were collected from some calves for Mycoplasma spp culture.

Results—Tulathromycin-treated calves had significantly lower odds of developing otitis media (OR, 0.41; 95% confidence interval, 0.58 to 0.82) versus control calves. Control calves had significantly higher odds of developing diarrhea (OR, 1.8; 95% confidence interval, 1.2 to 2.6) versus tulathromycin-treated calves. Control calves and those with failure of passive transfer, fever, lameness, respiratory tract disease, or diarrhea had significantly lower average daily gain versus other calves. Seventeen of the 66 (26%) calves that underwent repeated testing had positive Mycoplasma spp culture results, but positive results were not associated with otitis media. One of 42 calves with otitis media tested for Mycoplasma spp had positive results, and 1 of 43 age-matched calves without otitis media had positive results.

Conclusions and Clinical Relevance—Tulathromycin-treated calves in this study had a lower incidence of diarrhea and otitis media versus control calves. Various diseases had negative effects on average daily gain. Mycoplasma bovis status was not associated with otitis media in calves.

Abstract

Objective—To determine the effects of administration of 1 dose of tulathromycin on the incidence of various diseases and growth, identify risk factors for slow growth, and determine the association of Mycoplasma bovis status with the incidence of otitis media in calves.

Design—Randomized controlled trial and cross-sectional study.

Animals—788 dairy heifer calves (median age, 3 days).

Procedures—Calves received tulathromycin or a saline (0.9% NaCl) solution control treatment once. Calves were observed daily for 8 weeks by farm staff to detect diseases. Nasal swab specimens were collected from some calves for Mycoplasma spp culture.

Results—Tulathromycin-treated calves had significantly lower odds of developing otitis media (OR, 0.41; 95% confidence interval, 0.58 to 0.82) versus control calves. Control calves had significantly higher odds of developing diarrhea (OR, 1.8; 95% confidence interval, 1.2 to 2.6) versus tulathromycin-treated calves. Control calves and those with failure of passive transfer, fever, lameness, respiratory tract disease, or diarrhea had significantly lower average daily gain versus other calves. Seventeen of the 66 (26%) calves that underwent repeated testing had positive Mycoplasma spp culture results, but positive results were not associated with otitis media. One of 42 calves with otitis media tested for Mycoplasma spp had positive results, and 1 of 43 age-matched calves without otitis media had positive results.

Conclusions and Clinical Relevance—Tulathromycin-treated calves in this study had a lower incidence of diarrhea and otitis media versus control calves. Various diseases had negative effects on average daily gain. Mycoplasma bovis status was not associated with otitis media in calves.

Dairy heifers are increasingly reared in commercial heifer-raising facilities that do not include milking cows. In the United States, the proportion of dairy operations that sent calves to commercial heifer-raising facilities increased from 3.6% in 2002 to 4.7% in 2007.1 In 2007, 11.5% of heifers in the United States were from farms that sent their heifers (primarily calves that had not been weaned) to such facilities to be raised. In commercial heifer-rasing facilities, personnel can spend a large portion of time on the recognition, management, and treatment of diseases of calves. Such management reduces the risk of transfer of diseases from adult cows to calves after the first week after birth. In traditional dairy cow facilities, owners or managers must allocate their time, money, and other resources among lactating and nonlactating animals. Commercial heifer-raising facilities have potential problems such as exposure of calves to other calves of the same age from multiple source farms, which is a risk factor for various diseases.2 However, the incidence of disease in commercial heifer-raising facilities has not been thoroughly investigated. For example, a National Animal Health Monitoring System survey excluded heifer-raising facilities on the basis of the requirement that herds have at least 1 cow intended for milk production.3

The prophylactic administration of antimicrobials has been used to reduce the risk of infectious disease for dairy replacement heifers4 and veal calves5 (particularly during BRD outbreaks) at the time of weaning or movement to group housing. However, this practice has been studied more thoroughly for prevention of respiratory diseases in cattle in US beef feedlots6 than it has for dairy or veal calves. In 1999, personnel at 83% of feedlots prophylactically or metaphylactically administered antimicrobials via an oral route to calves and personnel at 42% of feedlots administered antimicrobials via an injectable route to animals at high risk for development of respiratory disease.7 There are similarities between beef cattle entering a feedlot and dairy calves entering a commercial heifer-raising facility. Both types of cattle are vulnerable to infection because they are exposed to infectious organisms in animals from multiple geographic sites. Beef cattle entering feedlots are likely to have been recently weaned and may have undergone transportation for a long period, during which time they may have been exposed to animals at ≥ 1 sales barn; these factors are associated with suppression of immune system function.8 Neonatal dairy calves have naïve immune systems, and immunity in such animals is primarily dependent on maternally derived antibodies in colostrum. This is a high-risk period for calves; almost one-quarter of all calves develop diarrhea during the period before weaning, and 12% of calves develop respiratory disease during that time.9 Such susceptibility to disease and exposure of calves to other calves from multiple sources may increase the risk of morbidity and death. No studies have been conducted to investigate the effectiveness of a single injection of a long-acting antimicrobial drug administered to calves at the time of arrival at a commercial heifer-raising facility for the control and prevention of disease.

Although metaphylactic administration of antimicrobials is a controversial approach to control and prevention of disease, such protocols may reduce overall use of antimicrobials in heifer-raising facilities because disease transmission to immunologically naïve animals may be prevented. Metaphylactic administration of antimicrobials to calves from farms with animals infected by Mycoplasma bovis at the time of arrival at a heifer-raising facility should reduce the spread of this organism to immunologically naïve calves that arrive from other locations. Animals at source farms from which calves originated could be monitored and management practices changed to reduce or eliminate the spread of M bovis to calves.

Tulathromycin is a long-acting macrolide antimicrobial triamilide compound. Unlike many other currently available antimicrobials, effective concentrations of tulathromycin against pathogens commonly associated with BRD are maintained for up to 10 days after administration to cattle.10 Tulathromycin is approved for the treatment and control of BRD in beef cattle and nonlactating dairy cattle. Tulathromycin is effective for the treatment of BRD in 3- to 9-week-old dairy bull calves experimentally infected with M bovis.11,12 However, tulathromycin has not been evaluated for the treatment of calves naturally infected with M bovis, to the authors' knowledge.

The first objective of the study reported here was to determine the effectiveness of a single SC injection of tulathromycin administered at the time of arrival at a commercial heifer-raising facility for treatment and prevention of various diseases in young dairy heifers during the early postnatal period. The hypothesis was that SC administration of 1 dose of tulathromycin at the time of arrival at a commercial heifer-raising facility would reduce the incidence of diseases or signs of disease (eg, otitis media, BRD, and fever) in calves during the first 8 weeks after birth. Another objective was to determine the effects of various diseases on growth of calves in a commercial heifer-raising facility. The hypothesis was that FPT and development of diarrhea, fever, BRD, or otitis media would negatively affect ADG of calves. Another objective was to determine the incidence of M bovis infection in calves and the association between M bovis infection and development of otitis media. The hypothesis was that M bovis infection would be associated with otitis media in calves and that calves with otitis media would be more likely to have nasal swab specimens with positive M bovis culture results versus calves without otitis media.

Materials and Methods

Animals—All study procedures were approved by the Animal Care Council of the University of Guelph. All calves included in this study were housed at a commercial heifer-raising facility in western New York State; 788 heifer calves were enrolled in the study between October 2007 and June 2008. Each calf was from 1 of 5 source farms in western New York State. Each source farm contributed between 43 and 315 calves for the study. Personnel at each source farm assigned a score for each calf regarding difficulty of birth by use of the National Association of Animal Breeders 5-point scale for grading calving difficulty.13

Heifer management and housing—Calves were between 0 and 10 days old at the time of arrival at the heifer-raising facility (median age, 3 days). At the time of arrival, calves were processed in accordance with a standard protocol and then individually housed in 1 of 6 naturally ventilated nursery barns or 47 individual outdoor hutches. The standard protocol included collection of tissue specimens for bovine viral diarrhea virus testing (ear tissue specimen obtained via an ear notch procedure or tail tissue specimen obtained via a tail docking procedure, depending on the preference of personnel at the source farm), a physical examination (to identify congenital abnormalities), and determination of serum total protein concentration with a digital refractometer. All calves had negative results for persistent bovine viral diarrhea virus infection. A modified-live vaccinea against infectious bovine rhinotracheitis, bovine viral diarrhea virus types 1 and 2, bovine respiratory syncytial virus, and parainfluenza-3 virus was administered IM to calves when they were 2 and 4 weeks old.

Calves were fed 4 L of milk replacerb twice daily (8 L/d) and had ad libitum access to calf starter feed (23% protein and 5% fat) and water. Weaning from milk replacer was started when calves were 5 weeks old; at that time, they received 4 L of milk replacer once per day, and milk replacer feeding was discontinued when calves were 6 weeks old. Calves were moved from individual pens or hutches to group housing 8 weeks after arrival at the heifer-raising facility, at which time the study ended.

Treatments—Calves were randomly assigned to a tulathromycin or control treatment group by use of a random number table and balanced allocation in blocks of 20 on the basis of the order in which calves were processed by staff at the time of arrival at the heifer-raising facility. Investigators and barn staff were unaware of the treatment group to which calves had been assigned. All calves in the tulathromycin treatment group received 100 mg (1.0 mL) of tulathromycinc (approximate dose, 2.5 mg/kg; the dose for the calves in this study was determined on the assumption that calves weighed 40 kg [88 lb]) SC on the day of arrival at the heifer-raising facility. Tulathromycin is labeled in the United States for the control of respiratory disease in nonlactating dairy heifers at high risk for development of BRD, including M bovis. Calves in the control treatment group received 1 mL of a mixture of propylene glycol and sterile saline (0.9% NaCl) solution (50:50 ratio) SC; that mixture had an identical appearance to the tulathromycin formulation.

Outcome measures—Calves were monitored twice daily for detection of signs of clinical disease by barn staff who were trained by a farm manager in the identification of disease; standardized definitions were used for determination of disease status (Appendix). The incidence of disease for calves in this study was calculated on the basis of the number of calves that developed disease during the 8-week study period.14 Calves with FPT were identified via detection of a serum total protein concentration < 5.4 g/dL.15 Information regarding administration of treatments was recorded via standardized forms at the time of administration, and data were later entered in a farm management computer program.d Information regarding all calves that developed diarrhea was recorded. Calves with diarrhea that had a rectal temperature ≥ 39.5°C (103.1°F) received an oral electrolyte solution and ceftiofur.e Calves with diarrhea that had a rectal temperature ≤ 39.5°C only received an electrolyte solution. Farm staff recorded information regarding unilateral or bilateral ear droop or tilted head posture of calves; a presumptive diagnosis of otitis media was made for calves with such clinical signs. Such calves received enrofloxacinf for treatment of otitis media; treatments were administered by barn staff at the time clinical signs were first observed.

Calves were weighed with an electronic scaleg and height at the withers (ie, at the most dorsal aspect of the shoulders) was measured with a yardstick at the time of arrival at the heifer-raising facility and at the end of the study 8 weeks later. Height values were rounded to the nearest unit.

Testing for Mycoplasma spp—Nasal swab specimens were collected from some of the calves during the study. Every other week during the study period, the 5 youngest calves with no history of ear droop underwent collection of nasal swab specimens for Mycoplasma spp testing; nasal swab specimen collection and testing of these calves were repeated 2 and 4 weeks later. This testing schedule was determined on the basis of the theory that some calves had M bovis infection at the time of arrival at the facility and that the organism would be transmitted among calves after that time. We expected that some calves would have positive results for M bovis at the time of arrival at the facility and some calves with negative results at that time would develop positive results during the testing period.

In addition, nasal swab specimens were collected twice per month from some calves with ear droop and age-matched healthy calves. Every other week during the study, nasal swab specimens were obtained from 2 calves in which ear droop had been identified and for which enrofloxacin had been administered by farm staff within the previous 24 hours; nasal swab specimens were also obtained from 2 calves without ear droop that were closest in age to those affected calves. Nasal swab specimens were obtained only once for such calves with ear droop and age-matched healthy calves. These calves were tested for M bovis to determine whether the incidence of positive results for M bovis was higher for calves with ear droop than it was for healthy calves without that finding.

Nasal swab specimens were collected by investigators wearing sterile disposable gloves. Swabs moistened with Mycoplasma enrichment medium were used to swab the nares of calves selected for testing. Nasal swab specimens were placed in enrichment medium and stored in a shipping box with cold packs. The specimens were shipped overnight to the Mastitis Research Laboratory at Washington State University, Pullman, Wash. At the time of arrival at the laboratory, medium was incubated at 37°C in 10% CO2 for 4 days. Then, 100 μL of incubated enrichment medium was streaked on an agar plate for detection of Mycoplasma spp.16 Plates were incubated at 37°C in 10% CO2 for 10 days. Plates were examined with a 15×-dissecting microscope 7 and 10 days after incubation was started to identify Mycoplasma spp colonies with a distinctive fried-egg appearance.16 Results were considered positive for plates with ≥ 1 Mycoplasma spp colony, and results were considered negative for plates without Mycoplasma spp colonies. Mycoplasma spp culture specimens were stored at −90°C in a 30% glycerol solution for 1 year prior to speciation and DNA fingerprinting analyses.17 Speciation was performed via PCR assay,18 and fingerprinting analysis to determine Mycoplasma spp type was performed via pulsed-field gel electrophoresis.19 The different Mycoplasma spp types were arbitrarily assigned a letter name to differentiate the strains.

Statistical analysis—Statistical analyses were performed with softwareh; statistical significance was determined on the basis of values of P ≤ 0.05 via the type III test for fixed effects. Statistical models were determined via backward stepwise elimination. Distributions of residual values were evaluated to assess for all linear models.

The associations between detection of disease and ADG and height of calves at the end of the study were determined via a linear mixed modeli with random effects for source farm, location of barn or hutch on the heifer-raising facility property, and cohort group nested in housing location. A cohort group was defined as calves that were housed in the same housing system at the same time. Disease outcomes included neonatal calf diarrhea complex, otitis media (bilateral or unilateral), fever, lameness, umbilical infection, and BRD. The associations of treatment, calf birth difficulty score, housing type (hutch vs barn), and FPT with amount of growth (ADG and height increase) of calves were tested in separate models from those that were used to determine the associations between growth and disease of calves. This method was used because disease events were likely to be intervening variables between risk factors and decreased growth and therefore could not be included in the same model as other variables. Models for ADG and height increase of calves included weight and height at the time of arrival at the heifer-raising facility, respectively, and age at the end of the study as fixed effects.

Potential predictors for development of neonatal calf diarrhea complex, unilateral and bilateral ear droop, and fever in calves were evaluated via mixed models with a binary distribution and logit transformation.j Source farm, location of barn or hutch system on the heifer-raising facility property, and cohort group nested within housing system location were included as random effects. A cohort group was defined as all calves housed in the same housing system at the same time. Models of unilateral and bilateral ear droop were determined separately because it was not known whether unilateral and bilateral ear droop had the same risk factors. The model for unilateral ear droop included calves with unilateral ear droop versus calves with no recorded history of ear droop. The model for bilateral ear droop included calves with bilateral ear droop versus calves with no recorded history of ear droop. Treatment, birth difficulty score, housing system type (hutch vs barn), and FPT were tested as predictor variables in all disease models.

The association between treatment group and death of calves was determined with a χ2 test. No statistical analysis was performed to determine the association between source farm and Mycoplasma spp infection of calves because of the low number of nasal swab specimens with positive results for such organisms.

Results

Demographics and diseases of calves—At the time of enrollment in the study, the mean ± SD age of calves was 3 ± 2 days, the mean ± SD weight of calves was 41.2 ± 4.4 kg (90.6 ± 9.7 lb), and the mean ± SD height of calves at the withers was 80 ± 3 cm. The most frequently detected diseases were neonatal calf diarrhea complex (659/788 [84%] calves) and otitis media (616/788 [78%] calves; Table 1). Unilateral and bilateral ear droop were observed for 32 (4%) and 414 (53%) of the 788 calves, respectively. Farm staff did not record whether ear droop was unilateral or bilateral at the time of administration of the first dose of enrofloxacin for 170 of the 616 calves treated for ear droop. Calves for which the number of droopy ears was not recorded were excluded from analyses. None of the calves had signs of ataxia. Only 40 (5%) calves had FPT (serum total protein concentration, ≤ 5.4 g/dL); serum total protein concentration was not measured for 10 calves.

Table 1—

Incidence and median age of health problems for 788 calves at a commercial heifer-raising facility during the first 8 weeks after arrival.

ProblemNo. (%) of calvesMedian age of calves when clinical signs were first observed (d)
Neonatal calf diarrhea complex659 (84)10
Otitis media616 (78)8
Unilateral ear droop32 (4)8
Bilateral ear droop414 (53)7
Unspecified laterality of ear droop170 (22)11
Fever115 (15)28
BRD21 (3)35
Lameness16 (2)17
Umbilical infection16 (2)7
Hernia*5 (1)19
Bloat2 (0.3)17
FPT40 (5)
No signs of disease27 (3)

Umbilical hernia that can be observed visually and confirmed with palpation.

Distension of the left side of the body.

Failure of passive transfer status was not determined for 10 calves because serum total protein concentrations were not determined.

— = Not applicable.

Age, weight, and height of calves at the time of enrollment in the study were not significantly different between the tulathromycin treatment group and the control group. Diarrhea was detected in 345 of 395 (87%) control calves and 314 of 393 (80%) tulathromycin-treated calves. Control calves were 1.8 (95% CI, 1.2 to 2.6; P = 0.005) times as likely to have neonatal calf diarrhea complex as were tulathromycin-treated calves, controlling for source farm, housing location at the heifer-raising facility, and group nested within housing location as random effects. Calves housed in a nursery barn were at higher risk for diarrhea, compared with calves housed in hutches (OR, 2.4; 95% CI, 0.9 to 6.4); however, this result was not significant (P = 0.08).

Of the 393 tulathromycin-treated calves, 11 (3%) had unilateral ear droop, 193 (49%) had bilateral ear droop, and the number of droopy ears was not recorded for 86 (22%). Of the 395 control calves, 21 (5%) had unilateral ear droop, 221 (56%) had bilateral ear droop, and the number of droopy ears was not recorded for 84 (21%). Tulathromycin-treated calves had significantly (P = 0.002) lower odds of developing otitis media (unilateral or bilateral ear droop) versus control calves (OR, 0.41; 95% CI, 0.60 to 0.82), controlling for source farm, housing location at the heifer-raising facility, and group nested within housing location as random effects. Ear droop was observed for 29 of 47 (62%) calves housed in hutches and 587 of 741 (79%) calves housed in nursery barns; those results were significantly (P = 0.006) different. Study treatment group was the only variable that was significant in the final statistical models for unilateral and bilateral ear droop that controlled for group and source farm as random effects. Tulathromycin-treated calves were 0.26 (95% CI, 0.11 to 0.65; P = 0.03) times as likely to have unilateral ear droop versus control calves. Tulathromycin-treated calves had significantly (P = 0.003) lower odds (OR, 0.58; 95% CI, 0.40 to 0.83) of having bilateral ear droop versus control calves.

Fifty-two of the 393 (13%) calves in the tulathromycin treatment group and 71 of the 395 (18%) calves in the control group had fever. Calves in the control group had higher odds of developing fever, compared with calves in the tulathromycin treatment group (OR, 1.5; 95% CI, 1.0 to 2.2), controlling for source farm, housing location at the heifer-raising facility, and group nested within housing location as random effects; however, that result was not significant (P = 0.07). No significant (P = 0.12) differences in the proportion of calves that developed fever were detected between calves housed in hutches and those housed in nursery barns. Bovine respiratory disease was detected in 9 of 393 (2%) tulathromycin-treated calves and 12 of 395 (3%) control calves; those proportions were not significantly (P = 0.52) different. Six of 393 (2%) calves in the tulathromycin treatment group and 10 of 395 (3%) calves in the control group had lameness; these proportions were not significantly (P = 0.32) different.

Growth—Weights for 3 calves were not determined at the end of the study before they were returned to their source farm; data for these calves were excluded from analyses of calf ADG and height increase. In addition, data for 14 calves that died during the study period were excluded from analyses of ADG and height increase. At the end of the study, the mean ± SD age of calves was 58 ± 7 days and the mean ± SD weight of calves was 75 ± 11 kg (165 ± 24 lb). The ADG of calves during the study was 0.61 ± 0.13 kg/d (1.34 ± 0.29 lb/d).

The mean ± SD height of calves at the end of the study was 92 ± 3 cm. The mean ± SD height increase for calves during the study was 11 ± 3 cm.

Association between diseases and ADG—Failure of passive transfer and treatment group status were significantly associated with ADG, controlling for weight at the time of arrival at the heifer-raising facility, with group and source farm as random effects. The calves with FPT had a mean ± SD ADG that was 0.04 ± 0.02 kg/d (0.09 ± 0.04 lb/d) lower than that for calves without FPT; this result was significant (P = 0.03). The calves in the tulathromycin treatment group had a mean ± SD ADG that was 0.02 ± 0.01 kg/d (0.04 ± 0.02 lb/d) higher than that for calves in the control group; this result was significant (P = 0.01). No significant (P = 0.54) interaction of treatment group and FPT status was detected. The ADG of calves housed in hutches was not significantly (P = 0.79) different from that for calves housed in barns.

Diarrhea, lameness, BRD, and fever status were significantly associated with ADG, controlling for body weight at the start of the study and age at the end of the study as fixed effects and source farm, treatment group, and treatment group within housing type as random effects (Table 2). For calves with unilateral ear droop, the mean ± SD ADG was 0.05 ± 0.02 kg/d (0.11 ± 0.04 lb/d) lower than that for calves without ear droop; this result was significant (P = 0.04). The ADG was not significantly different between calves with bilateral ear droop (P = 0.99) or calves with an unknown number of droopy ears (P = 0.98) and calves without ear droop.

Table 2—

Average daily gain (kg/d) for calves with and without various diseases during the first 8 weeks after arrival at a heifer-raising facility.

DiseaseWith diseaseWithout diseaseDifference in ADG between calves with disease and those without disease
Diarrhea (n = 659)0.49 ± 0.030.46 ± 0.020.03 ± 0.0a
Fever (n = 115)0.51 ± 0.020.44 ± 0.030.07 ± 0.01b
BRD (n = 21)0.53 ± 0.020.42 ± 0.030.10 ± 0.03b
Lameness (n = 16)0.56 ± 0.020.39 ± 0.040.16 ± 0.03b

Data are mean ± SD.

Data are significantly (P < 0.05) different between calves with disease and those without disease.

Data are significantly (P < 0.001) different between calves with disease and those without disease.

Statistical analyses were controlled for birth weight and age at the end of the study as fixed effects and source farm, treatment group (tulathromycin or control treatment), and treatment group within barn as random effects.

Association between diseases and height increase—Failure of passive transfer status was significantly associated with height of calves at the end of the study. The mean ± SD height of calves with FPT was 1 ± 0.4 cm less than that for calves without FPT; that result was significant (P < 0.001), controlling for height of calves at the start of the study and age at the end of the study, with source farm, housing location at the heifer-raising facility, and group nested within housing location as random effects. The mean ± SD height of calves in the tulathromycin treatment group was 0.3 ± 0.2 cm higher than that for calves in the control group at the end of the study; that finding was not significant (P = 0.08). No significant (P = 0.20) difference in height was detected between calves housed in hutches and calves housed in barns.

Diarrhea, otitis media, and fever were significantly associated with lower height of calves at the end of the study versus calves without those findings, controlling for height at the start of the study as a fixed effect and source farm, housing location at the heifer-raising facility, and treatment group nested within housing location as random effects. The least square means ± SE height of calves with diarrhea was 1 ± 0.2 cm less than that for calves without diarrhea at the end of the study; this result was significant (P = 0.01). The mean ± SD height of calves with unilateral ear droop was 2 ± 0.5 cm less than that for calves without ear droop at the end of the study; that result was significant (P = 0.001). The height of calves with bilateral ear droop and calves for which the number of droopy ears was not recorded were not significantly (P = 0.32 and 0.12, respectively) different from the height of calves without ear droop. The mean ± SD height of calves with fever was 1 ± 0.2 cm less than that for calves without fever at the end of the study; that finding was significant (P < 0.001).

Mycoplasma spp testing—Nasal swab specimens were obtained during the first week of enrollment in the study and 2 and 4 weeks later from 66 calves; of these, 17 (26%) calves had 1 positive test result for Mycoplasma spp. Of those 66 calves, 59 (89%) developed diarrhea and 49 (74%) developed ear droop during the study (Table 3). None of the nasal swab specimens collected from the calves during their first week of enrollment in the study had positive Mycoplasma spp culture results; results were positive for nasal swab specimens collected from 2 calves 2 weeks after that time and 15 calves 4 weeks after that time. Of the 17 calves with a positive Mycoplasma spp culture result, 9 were in the tulathromycin treatment group. Ear droop was detected during the study for 10 of the 17 calves with positive Mycoplasma spp culture results. Of those 10 calves, 9 developed ear droop during the time between collection of the second and third nasal swab specimens. Positive Mycoplasma spp culture results were detected for calves from 4 of the 5 source farms (Table 4). The farm without calves with a positive result was a small facility, and only 2 calves from this farm were tested for Mycoplasma spp during the study.

Table 3—

Incidence of various health problems for calves with positive or negative Mycoplasma spp culture results when they were between 2 and 4 weeks old.

ProblemCalves with positive culture result (n = 17)Calves with negative culture result (n = 49)P value
Diarrhea14 (82)45 (92)0.36
Ear droop10 (59)39 (80)0.11
Fever1 (6)7 (14)0.67
BRD1 (6)1 (2)0.45
Lameness0 (0)2 (4)1.0
Umbilical infection1 (6)2 (4)1.0
FPT0 (0)5 (10)0.32
No health problem2 (12)3 (6)0.60

Data are number (%) of calves with positive or negative Mycoplasma spp culture results that had a health problem.

Table 4—

Mycoplasma spp culture results for calves from each of 5 source farms.

FarmCalves with positive results for Mycoplasma spp*Mycoplasma bovis strainCalves with culture specimens that died during freezer storage
ABCDUnknown  
18/36 (22)200141
23/15 (20)101001
33/8 (38)010011
43/5 (60)011001
50/2 (0)000000
Total17/66 (26)322154

Data are number of calves unless otherwise specified. Nasal swab specimens were collected from calves for Mycoplasma spp culture during the first week of the study and 2 and 4 weeks after that time.

Data are number of calves with a positive Mycoplasma spp culture result/number of calves tested (%).

Strain could not be determined because insufficient DNA was available for analysis.

Species could not be determined because organisms in culture specimens died during freezer storage before further analysis could be conducted.

Each M bovis strain was arbitrarily assigned a letter for differentiation.

Strains were determined for M bovis colonies cultured from nasal swab specimens of calves. Five M bovis strains were identified; calves from 4 of the 5 source farms had ≥ 2 M bovis strains. Insufficient DNA was available for DNA fingerprinting analysis of 5 of the M bovis specimens; therefore, strains could not be determined for these colonies. Additionally, 4 other Mycoplasma spp culture specimens degraded during storage prior to speciation and DNA fingerprinting analyses; species and strains could not be determined for these colonies.

Nasal swab specimens were obtained for 42 calves in which ear droop had been identified and for which enrofloxacin had been administered by farm staff within the previous 24 hours and for 43 age-matched calves without ear droop; only 1 calf in each of those groups had positive M bovis culture results. These animals were from different source farms. The calf with ear droop had the M bovis strain assigned the identification of strain A for the purposes of this study. The age-matched calf from the other source farm developed ear droop within 24 hours after collection of the nasal swab specimen. Not enough DNA was available for the M bovis strain obtained from the age-matched calf without ear droop to complete DNA fingerprinting analysis; therefore, the strain of that organism could not be identified.

Mortality rate—Fourteen of 788 calves died during the 8-week study (mortality rate, 2%). Eight calves in the control group and 6 calves in the tulathromycin treatment group died. Causes of death of calves determined by farm staff included diarrhea (n = 3), bloat (2), high fever (2), chronic poor health (2), swelling of neck or throat (2), paralysis (1), gastric ulcer (1), and severe lameness (1). No deaths of calves were attributed to ear droop.

Discussion

Factors that affect diseases of calves are likely different for a commercial heifer-raising facility versus a traditional farm, on which replacement animals for the farm are raised. Personnel at heifer-raising facilities are likely to allocate more time to monitoring growth and diseases of calves than personnel at traditional farms because heifer-raising facility personnel must report and justify the cost of rearing calves to the source farms. In addition, the risk factors of calves for diseases are likely different for each of those types of facilities because calves at a heifer-raising facility are isolated from older animals but are exposed to calves from multiple sources. Eighty-four percent of calves in the present study developed diarrhea, which was substantially higher than the previously reported9,20–23 incidence of diarrhea in calves (7% to 39%). The finding that a high percentage of calves developed diarrhea during the present study was likely attributable to careful monitoring of calves by personnel and the definition of diarrhea (unformed soft feces) used in this study. In addition, transport of calves to the heifer-raising facility and exposure to other animals a short time after birth may also have increased the incidence of diarrhea in calves in this study.

Personnel at the heifer-raising facility of this study identified calves with a rectal temperature ≥ 39.5°C as having fever. This definition was not specific for identification of calves with BRD; therefore, calves identified as having fever in this study may have had respiratory disease or another problem. As a result, data regarding calves with fever and those with BRD were not combined for analysis. However, the percentage of calves with BRD or fever in the present study (17%) was similar to the incidence of respiratory disease of calves (12%) determined in another study.9

The percentage of calves with FPT in the present study (5%) was less than that determined in other studies (19% to 37%).21,24–26 The low percentage of calves with FPT in the present study was likely attributable to education offered by the manager of the heifer-raising facility for personnel of source farms and the high cost charged by the facility for raising of calves with that problem. The percentage of calves in the present study that died (2%) was substantially lower than it was for calves in another study9 (7.8%).

Results of another study9 indicate the median weight of Holstein heifer calves between 56 and 62 days old in the United States during 2007 was 80 kg (176 lb).9 The mean weight of calves at the end of the present study (when they were approx 8 weeks old) was 75 ± 11 kg, which was slightly less than the median weight of calves at that age in that other study.9

Bovine respiratory disease, fever, diarrhea, and lameness affected ADG of calves in the present study. Bovine respiratory disease and fever were associated with an ADG approximately 0.10 and 0.07 kg/d (0.22 and 0.15 lb/d) lower, respectively, compared with the ADG of healthy calves. Results of other studies indicate ADG decreases by 0.07 kg/d (0.15 lb/d) for calves with BRD during the first month of after birth,21 and BRD decreases ADG by 0.01 kg/d (0.02 lb/d) during the first 6 months after birth,27 versus healthy calves. Because one of those other studies27 was conducted during a 6-month period, enough time was allowed for determination of the effects of recovery from BRD or other diseases, diet, social interactions among animals, and movement to group housing on growth of calves; therefore, results of that study were likely affected by factors other than BRD alone.

Results of the present study indicated diarrhea was associated with an ADG that was 0.03 kg/d (0.07 lb/d; range, 0.01 to 0.05 kg/d [0.02 to 0.11 lb/d]) lower, compared with the ADG of healthy calves. This finding was consistent with the finding of another study27 that diarrhea decreases ADG of calves by 0.013 kg/d (0.029 lb/d) versus healthy calves. However, results of another study21 indicate diarrhea has no effect on ADG of calves; this finding may have been attributable to the methods used to determine weight gain of calves in the study. Weights of calves were determined with an electronic scale in the study,27 with results indicating that diarrhea decreased ADG of calves, whereas weights of calves in the other study21 were estimated via weight tape measurements. Weight tape measurement error may have falsely decreased the effects of diarrhea on ADG of calves in that other study.21

Otitis media did not have an effect on ADG of calves in the present study. This finding was different from the finding of another study28 that calves with otitis media had a mean weight gain 4.68 kg (10.30 lb) less than that for calves without that problem. However, results of the present study were similar to results of another study29 that experimentally induced M bovis infection of calves does not have a significant effect on ADG during the subsequent 18 days for calves treated with antimicrobials. Differences in findings between the present study and that other study28 regarding the effects of otitis media on ADG of calves may have been attributable to various factors. Data were not analyzed via statistical methods in that other study28; therefore, comparisons between results of the present study and results of that other study were difficult to perform. Early detection of a disease is associated with a decrease in the severity of clinical signs and the duration of convalescence,30 and the careful monitoring and early treatment of calves in the present study may have minimized the effect of otitis media on ADG. Alternatively, bilateral ear droop in some calves of the present study may have been attributable to signs of depression caused by other diseases (eg, diarrhea); this may have affected results because otitis media was diagnosed only via detection of ear droop in calves of this study. The definition of otitis media used in the present study was intended to be easily applied because the study was conducted at a commercial facility and advanced diagnostic methods were not used. The small number of calves with unilateral ear droop in this study limited our ability to determine the effects of unilateral otitis media on ADG. However, further research regarding the effects of otitis media on ADG may be warranted.

In the present study, FPT was associated with an ADG of 0.04 kg/d (0.09 lb/d) lower than that in healthy calves. This finding was consistent with findings of another study30 that FPT decreases ADG of calves by 0.05 kg/d during the first month after birth21 versus health calves. The ADG for calves in the tulathromycin treatment group was 0.02 kg/d less than that for control calves of the present study. Successful passive transfer of maternally derived antibodies and administration of tulathromycin were associated with a lower risk of disease for calves in this study. Calves with FPT are more susceptible to diseases that negatively affect ADG versus calves without FPT.27 Tulathromycin is typically used to treat respiratory disease. However, results of this study indicated tulathromycin had a beneficial effect on the incidence of neonatal calf diarrhea complex. This finding may have been attributable to a reduction in the incidence of BRD and otitis media, which may have enabled calves to mount a strong immune response against diarrhea-causing organisms. No significant interaction was detected between tulathromycin treatment and successful passive transfer of maternally derived antibodies for calves in the present study; both factors seemed to protect calves against disease. This finding may have been attributable to the low number of calves with FPT in the study, which may have limited the power of the study to detect interaction between variables. Results of this study indicated tulathromycin treatment significantly reduced the incidence of unilateral and bilateral ear droop and diarrhea in calves; such treatment reduced the incidence of fever, although that result was not significant. Results of another study28 indicate prophylactic administration of tulathromycin reduces the incidence of otitis media in milk-fed calves. However, tulathromycin was administered to calves in that study on days 1 and 7 after arrival at the study facility, whereas calves in the present study received tulathromycin once. An OR calculated with data reported28 by those other authors indicated the odds of development of otitis media was 3.8 (95% CI, 1.8 to 9.8) times as great for calves that received a placebo treatment as it was for calves that received tulathromycin on days 1 and 7 of that study. This finding was similar to the finding of the present study that the control calves were 3.7 (95% CI, 1.6 to 9.1) times as likely to develop unilateral ear droop and 1.7 (95% CI, 1.2 to 2.5) times as likely to develop bilateral ear droop as were calves in the tulathromycin treatment group. Results of the present study suggested that administration of 1 dose of tulathromycin reduced the incidence of otitis media in neonatal calves; further studies may be warranted to confirm these findings.

Results of the present study suggested that some calves had M bovis infection and that calves were more likely to have positive M bovis culture results when they were ≥ 2 weeks old. This finding suggested that there was a delay between development of clinical signs of disease and shedding of M bovis; that finding was consistent with findings of another studyk that calves experimentally infected with M bovis a short time after birth develop clinical signs but do not have positive bacteriologic culture results for nasal swab specimens during the 14 days after development of infection.k Clinical signs of otitis media were primarily detected in calves < 2 weeks old in the present study. Moreover, results of this study indicated calves were likely to shed > 1 strain of M bovis and that calves from different source farms had different strains of that organism. These findings suggested that M bovis was transmitted among calves from different source farms during the study.

We identified 3 potential reasons for the finding of the present study that there was no association between positive results for M bovis infection and development of otitis media in calves. Mycoplasma bovis may not be an important pathogen for otitis media in young dairy calves. Alternately, results of bacteriologic cultures may have been falsely negative for M bovis because of the nasal swab specimen collection schedule or antimicrobial administration to calves at the heifer-raising facility. In addition, M bovis organisms may have died during specimen collection. Results of another study2 indicate that M bovis infection is associated with respiratory disease, arthritis, and otitis in dairy calves. Personnel at the heifer-raising facility administered antimicrobials to calves at the time of determination of a diagnosis of otitis media in the present study. Because nasal swab specimens were typically obtained 2 to 12 hours after treatment of calves, growth of M bovis in cultures may have been inhibited and some results may have been falsely negative. Some M bovis organisms may have died during transportation and storage of nasal swab specimens. All nasal swab specimens were shipped from New York State to Washington State. Although these specimens were sent overnight with cold packs, temperatures may have varied and other organisms may have grown during shipping. Some M bovis organisms may also have died during frozen storage after culture and prior to speciation analysis. Freezing of culture specimens decreases recovery of M bovis organisms.18,19,31 Before speciation analysis, Mycoplasma spp organisms in 4 of the 17 culture specimens died. Death of organisms and administration of antimicrobials to calves prior to collection of nasal swab specimens may have decreased our ability to detect an association between positive bacteriologic culture results for M bovis and development of otitis media. We were unable to determine the effects of these factors on the results of this study.

Metaphylactic administration of antimicrobial drugs should be thoroughly evaluated in other studies. To minimize the risk of resistance of organisms to antimicrobials, such antimicrobials should only be administered to animals during a period of high risk for disease. Antimicrobials should not be administered to calves to increase growth, but rather to reduce the spread of disease among animals. Other variables (eg, accuracy of records, cleanliness of facilities, ventilation, and feeding of colostrum) should also be managed to reduce the need for antimicrobial treatment of calves. Although effective treatments for BRD are available, calves that are treated for BRD and survive have decreased growth and long-term survival rates versus calves without BRD.32 Mycoplasma bovis infection contracted at a source farm fit our previously established criteria for metaphylaxis on the basis of the high incidence of disease following movement to the heifer-raising facility and the difficulty of treating M bovis–associated disease as reported by Caswell and Archambault.33 However, the finding of the present study that there was no significant association between development of otitis media and positive M bovis culture results suggested that further studies should be conducted to determine the most appropriate times for metaphylactic administration of antimicrobials.

The incidence of ear droop in the calves that had negative M bovis culture results in the present study seemed to be higher than the incidence of ear droop in calves with positive culture results for that organism. However, this finding may have been confounded by the fact that calves with ear droop were treated with enrofloxacin. Heifers for which nasal swab specimens were obtained after a diagnosis of otitis media had been determined and enrofloxacin had been administered may have been less likely to shed Mycoplasma spp organisms versus calves that had not been treated with that antimicrobial before collection of specimens.

Results of the present study suggested that administration of tulathromycin decreased the incidence of unilateral and bilateral ear droop and diarrhea in calves that had been transported from various source farms to a heifer-raising facility during the early postnatal period. In addition, tulathromycin treatment seemed to decrease the incidence of fever in calves, although that result was not significant. The incidence of diarrhea was reduced for tulathromycin-treated calves, most likely because of strong immune function resulting from a reduction in the incidence of respiratory diseases. Reduction in the incidence of diseases in calves is important for producers because fever, BRD, FPT, lameness, and neonatal calf diarrhea complex compromise growth of calves. However, implementation of a metaphylactic antimicrobial administration protocol for a heifer-raising facility would require determination of the Mycoplasma spp infection status of calves from each source farm. Results of this study indicated M bovis infection was not associated with development of otitis media in calves. Improvements in microbial culture methods and decreased administration of antimicrobial drugs to calves may have increased our ability to detect an association between clinical signs of otitis media and positive culture results for M bovis. Further studies to determine the role of Mycoplasma spp in the development of diseases in young dairy calves may be warranted. The results of this study suggested that administration of tulathromycin was efficacious for the reduction of the incidence of various diseases in neonatal calves.

ABBREVIATION

ADG

Average daily gain

BRD

Bovine respiratory disease complex

CI

Confidence interval

FPT

Failure of passive transfer

a.

Vista-5, Intervet Schering-Plough Animal Health, Boxmeer, The Netherlands.

b.

Excel Calf Milk Replacer 26/18, Grober Nutrition, Cambridge, ON, Canada.

c.

Draxxin, Pfizer Animal Health Group, New York, NY.

d.

DairyComp 305, Valley Agriculture Software Inc, Tulare, Calif.

e.

Excede, Pfizer Animal Health Group, New York, NY.

f.

Baytril 100, Bayer Animal Health, Leverkusen, Germany.

g.

Tru-test ID3000, Tru-Test Inc, Mineral Wells, Tex.

h.

SAS, version 9.1, SAS Institute Inc, Cary, NC.

i.

PROC mixed, SAS, version 9.1, SAS Institute Inc, Cary, NC.

j.

PROC GLIMMIX, SAS, version 9.1, SAS Institute Inc, Cary, NC.

k.

Maunsell FP. Oral inoculation of dairy calves with Mycoplasma bovis results in respiratory infection and otitis media: establishment of a model of an emerging problem. In: Mycoplasma bovis infection of dairy calves. PhD thesis. Gainesville, Fla: University of Florida, 2007;153–188.

References

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    • Search Google Scholar
    • Export Citation
  • 2. Maunsell F, Donovan GA. Biosecurity and risk management for dairy replacements. Vet Clin North Am Food Anim Pract 2008; 24: 155190.

  • 3. USDA. Dairy 2007, part V: changes in dairy cattle health and management practices in the United States, 1996–2007. No. 519.0709. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2009.

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  • 4. Stanton AL, Kelton DF & LeBlanc SJ, et al. The effect of treatment with long-acting antibiotic at postweaning movement on respiratory disease and on growth in commercial dairy calves. J Dairy Sci 2010; 93: 574581.

    • Crossref
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  • 5. Catry B, Duchateau L & Ven de Van J, et al. Efficacy of metaphylactic florfenicol therapy during natural outbreaks of bovine respiratory disease. J Vet Pharmacol Ther 2008; 31: 479487.

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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
  • 8. Carroll J, Forsberg NE. Influence of stress and nutrition on cattle immunity. Vet Clin North Am Food Anim Pract 2007; 23: 105149.

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    • Search Google Scholar
    • Export Citation
  • 10. Nowakowski MA, Inskeep PB & Risk JE, et al. Pharmacokinetics and lung tissue concentrations of tulathromycin, a new triamilide antibiotic, in cattle. Vet Ther 2004; 5: 6074.

    • Search Google Scholar
    • Export Citation
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  • 12. Godinho KS, Rae A & Windsor GD, et al. Efficacy of tulathromycin in the treatment of bovine respiratory disease associated with induced Mycoplasma bovis infections in young dairy calves. Vet Ther 2005; 6: 96112.

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  • 13. Weigel K. Complete and accurate recording of calving ease and stillbirth is key. Available at: www.extension.org/pages/11036/complete-and-accurate-recording-of-calving-ease-and-stillbirth-data-is-key. Accessed Jan 18, 2013.

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  • 20. Svensson C, Lundborg K & Emanuelson U, et al. Morbidity in Swedish dairy calves from birth to 90 days of age and individual calf-level risk factors for infectious diseases. Prev Vet Med 2003; 58: 179197.

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  • 21. Virtala AMK, Mechor GD, Grohn YT. 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
  • 22. Donovan GA, Dohoo IR & Montgomery DM, et al. Associations between passive immunity and morbidity and mortality in dairy heifers in Florida, USA. Prev Vet Med 1998; 34: 3146.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Waltner-Toews D, Martin SW & Meek AH, et al. Dairy calf management, morbidity and mortality in Ontario Holstein herds. I. The data. Prev Vet Med 1986; 4: 103124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. USDA. Dairy 2007, part IV: reference of dairy cattle health and management practices in the United States, 2007. No. N494.0209. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2009.

    • Search Google Scholar
    • Export Citation
  • 25. Van Donkersgoed J, Ribble C & Boyer LG, et al. Epidemiological study of enzootic pneumonia in dairy calves in Saskatchewan. Can J Vet Res 1993; 57: 247254.

    • Search Google Scholar
    • Export Citation
  • 26. Trotz-Williams LA, Leslie KE, Peregrine AS. Passive immunity in Ontario dairy calves and investigation of its association with calf management practices. J Dairy Sci 2008; 91: 38403849.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Donovan GA, Dohoo IR & Montgomery DM, et al. Calf and disease factors affecting growth in female Holstein calves in Florida, USA. Prev Vet Med 1998; 33: 110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Sockett DC, Jicinsky SA & Earleywine TJ, et al. Efficacy of tulathromycin and oxytetracycline on reducing the incidence of otitis media caused by Mycoplasma bovis in preweaned Holstein dairy calves, in Proceedings. 41st Annu Am Assoc Bovine Pract Conf 2008;8.

    • Search Google Scholar
    • Export Citation
  • 29. Stipkovits L, Ripley PH & Tenk M, et al. The efficacy of valnemulin (Econor) in the control of disease caused by experimental infection of calves with Mycoplasma bovis. Res Vet Sci 2005; 78: 207215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. McGuirk SM. Disease management of dairy calves and heifers. Vet Clin Food Anim 2008; 24: 139153.

  • 31. Biddle MK, Fox LK & Hancock DD, et al. Effects of storage time and thawing methods on the recovery of Mycoplasma species in milk samples from cows with intramammary infections. J Dairy Sci 2004; 87: 933936.

    • Crossref
    • Search Google Scholar
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  • 32. 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.

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Appendix

DiseaseDefinition
Ear droop1 or both ears drooping or head maintained in a tilted position
Neonatal calf diarrhea complex (diarrhea)Feces soft without form
BRDRectal temperature ≥ 39.5°C with high respiratory rate, nasal discharge, or cough
FeverDull and listless with a rectal temperature > 39.5°C and no signs of diarrhea or high respiratory rate, nasal discharge, cough, lameness, or umbilical infection
LamenessAbnormal gait with unknown cause
Umbilical infectionUmbilicus swollen or calf has signs of pain during palpation of umbilicus
  • 1. USDA. Dairy 2007, part II: changes in the U.S. dairy cattle industry, 1991–2007. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2007.

    • Search Google Scholar
    • Export Citation
  • 2. Maunsell F, Donovan GA. Biosecurity and risk management for dairy replacements. Vet Clin North Am Food Anim Pract 2008; 24: 155190.

  • 3. USDA. Dairy 2007, part V: changes in dairy cattle health and management practices in the United States, 1996–2007. No. 519.0709. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2009.

    • Search Google Scholar
    • Export Citation
  • 4. Stanton AL, Kelton DF & LeBlanc SJ, et al. The effect of treatment with long-acting antibiotic at postweaning movement on respiratory disease and on growth in commercial dairy calves. J Dairy Sci 2010; 93: 574581.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Catry B, Duchateau L & Ven de Van J, et al. Efficacy of metaphylactic florfenicol therapy during natural outbreaks of bovine respiratory disease. J Vet Pharmacol Ther 2008; 31: 479487.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Van Donkersgoed J. Meta-analysis of field trials of antimicrobial mass medication for prophylaxis of bovine respiratory disease in feedlot cattle. Can Vet J 1992; 33: 786795.

    • Search Google Scholar
    • Export Citation
  • 7. USDA. National Animal Health Monitoring System. Part III: health management and biosecurity in U.S. feedlots, 1999. No. N336.1200. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2000.

    • Search Google Scholar
    • Export Citation
  • 8. Carroll J, Forsberg NE. Influence of stress and nutrition on cattle immunity. Vet Clin North Am Food Anim Pract 2007; 23: 105149.

  • 9. USDA. Dairy 2007, heifer calf health and management practices on U.S. dairy operations, 2007. No. 550.0110. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2010.

    • Search Google Scholar
    • Export Citation
  • 10. Nowakowski MA, Inskeep PB & Risk JE, et al. Pharmacokinetics and lung tissue concentrations of tulathromycin, a new triamilide antibiotic, in cattle. Vet Ther 2004; 5: 6074.

    • Search Google Scholar
    • Export Citation
  • 11. Godinho KS, Sarasola P & Renoult E, et al. Use of deep nasopharyngeal swabs as a predictive diagnostic method for natural respiratory infections in calves. Vet Rec 2007; 160: 2225.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Godinho KS, Rae A & Windsor GD, et al. Efficacy of tulathromycin in the treatment of bovine respiratory disease associated with induced Mycoplasma bovis infections in young dairy calves. Vet Ther 2005; 6: 96112.

    • Search Google Scholar
    • Export Citation
  • 13. Weigel K. Complete and accurate recording of calving ease and stillbirth is key. Available at: www.extension.org/pages/11036/complete-and-accurate-recording-of-calving-ease-and-stillbirth-data-is-key. Accessed Jan 18, 2013.

    • Search Google Scholar
    • Export Citation
  • 14. Dohoo IR, Martin SW, Stryhn H. Veterinary epidemiologic research. Charlottetown, PE, Canada: AVC Inc, 2003.

  • 15. Tyler JW, Hancock DD & Wiksie SE, et al. Use of serum protein concentration to predict mortality in mixed-source dairy replacement heifers. J Vet Intern Med 1998; 12: 7983.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Hogan JS, González RN & Harmon RJ, et al. National Mastitis Council laboratory handbook on bovine mastitis. Madison, Wis: National Mastitis Council, 1999.

    • Search Google Scholar
    • Export Citation
  • 17. Boonyayatra S, Fox LK & Besser TE, et al. Effects of storage methods on the recovery methods of Mycoplasma species from milk samples. Vet Microbial 2010; 144: 210213.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Boonyayatra S, Fox LK & Besser TE, et al. A PCR assay and PCR-restriction fragment length polymorphism combination identifying the 3 primary Mycoplasma species causing mastitis. J Dairy Sci 2012; 95: 196205.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Biddle MK, Fox LK & Evans SJ, et al. Pulsed-field gel electrophoresis patterns of Mycoplasma isolates from various body sites in dairy cattle with Mycoplasma mastitis. J Am Vet Med Assoc 2005; 227: 455459.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Svensson C, Lundborg K & Emanuelson U, et al. Morbidity in Swedish dairy calves from birth to 90 days of age and individual calf-level risk factors for infectious diseases. Prev Vet Med 2003; 58: 179197.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Virtala AMK, Mechor GD, Grohn YT. 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
  • 22. Donovan GA, Dohoo IR & Montgomery DM, et al. Associations between passive immunity and morbidity and mortality in dairy heifers in Florida, USA. Prev Vet Med 1998; 34: 3146.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Waltner-Toews D, Martin SW & Meek AH, et al. Dairy calf management, morbidity and mortality in Ontario Holstein herds. I. The data. Prev Vet Med 1986; 4: 103124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. USDA. Dairy 2007, part IV: reference of dairy cattle health and management practices in the United States, 2007. No. N494.0209. Fort Collins, Colo: USDA APHIS Veterinary Services Centers for Epidemiology and Animal Health, 2009.

    • Search Google Scholar
    • Export Citation
  • 25. Van Donkersgoed J, Ribble C & Boyer LG, et al. Epidemiological study of enzootic pneumonia in dairy calves in Saskatchewan. Can J Vet Res 1993; 57: 247254.

    • Search Google Scholar
    • Export Citation
  • 26. Trotz-Williams LA, Leslie KE, Peregrine AS. Passive immunity in Ontario dairy calves and investigation of its association with calf management practices. J Dairy Sci 2008; 91: 38403849.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Donovan GA, Dohoo IR & Montgomery DM, et al. Calf and disease factors affecting growth in female Holstein calves in Florida, USA. Prev Vet Med 1998; 33: 110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Sockett DC, Jicinsky SA & Earleywine TJ, et al. Efficacy of tulathromycin and oxytetracycline on reducing the incidence of otitis media caused by Mycoplasma bovis in preweaned Holstein dairy calves, in Proceedings. 41st Annu Am Assoc Bovine Pract Conf 2008;8.

    • Search Google Scholar
    • Export Citation
  • 29. Stipkovits L, Ripley PH & Tenk M, et al. The efficacy of valnemulin (Econor) in the control of disease caused by experimental infection of calves with Mycoplasma bovis. Res Vet Sci 2005; 78: 207215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. McGuirk SM. Disease management of dairy calves and heifers. Vet Clin Food Anim 2008; 24: 139153.

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