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ANIMAL PRODUCTION |
Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, 0110, South Africa
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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Key Words: bovine respiratory disease • cattle • economic impact • feedlot • growth • lung lesion
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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; Smith, 2000), causing mortality, reduced ADG, increased days on feed (DOF), and poor carcass quality (Wittum et al., 1996; Gardner et al., 1999). Lesions resulting from BRD are frequently found at slaughter, often in animals in which clinical disease has never been detected, and the presence of such lesions is a better predictor of reduced ADG than are BRD treatment records (Wittum et al., 1996; Bryant et al., 1999). Because both clinical and subclinical BRD affect growth, both should be accounted for in estimating the overall effect of BRD on feedlot cattle performance.
Bryant et al. (1999) proposed that future studies should use lesion scoring combined with health records to measure the true incidence of BRD; to our knowledge, this has not yet been done. Clinical BRD occurs most commonly during the first 3 to 6 wk after arrival at the feedlot (Jensen et al., 1976; Radostits et al., 2000); however, it is unclear whether the effect on ADG is due to the original disease episode or the chronic effects of the lesions, or both. It seems logical that lesion type and severity should influence ADG, but this has not been clearly shown. Wittum et al. (1996) looked separately at the effect of pleuritis on ADG and found it to be the same as that of bronchopneumonic lesions. Bryant et al. (1999) found that although the presence of lung lesions depressed growth rate, the extent of parenchymal involvement was not associated with ADG.
The objectives of this study were therefore to estimate the effect of BRD on growth during early (processing to d 35) and late (d 35 to slaughter) finishing periods in 2 South African feedlots using a case definition combining both clinical diagnosis of BRD and presence of lung lesions at slaughter, to investigate the effects of lesion type and severity on growth rate, and to quantify the hidden economic cost of reduced growth due to BRD.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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Animal Management
Animals (n = 2,036) were purchased by the feedlot operator in the normal course of business, during the fall of 2003 (April and May), having been sourced from auctions or directly from farms in various districts in South Africa. Predominantly steers, representing a wide variety of breeds and crossbreeds, between the ages of 5 and 10 mo at the start of the trial and with a BW between 150 and 300 kg, were included in the trial.
Upon arrival at the feedlot (d 0), animals were placed in receiver pens with fresh water and hay ad libitum for 24 h. On d 1, cattle were individually identified with a numbered ear tag and weighed. An acaricide (Ectoline, Bayer Animal Health, Isando, South Africa) was topically applied, and a vaccine containing modified live strains of infectious bovine rhinotracheitis, bovine viral diarrhea virus, parainfluenza-3 virus, and bovine respiratory syncytial virus was administered (Bovishield; Pfizer Animal Health, Sandton, South Africa).
On d 5 after arrival, calves were processed. During processing animals were weighed and vaccinated against botulism (Botuvax Intervet SA, Edenvale, South Africa), lumpy skin disease (Lumpy Skin Disease; Onderstepoort Biological Products, Onderstepoort, South Africa), anthrax (Anthravax; Intervet SA), and clostridial diseases (Siteguard MLG; Schering Plough Animal Health, Isando, South Africa). A growth stimulant containing 36 mg of zeranol (Ralgro; Schering Plough) was given s.c. behind the left ear, bulls were castrated with a Burdizzo, and tip dehorning was done.
Feeding throughout the finishing period was done 3 times daily at 0630, 0930, and 1300. A corn silage-based complete diet was fed throughout. On d 35 and 56, all animals were weighed again. On d 56, another implant containing 140 mg of trenbolone acetate and 28 mg of estradiol-17ß (Revalor-S; Intervet SA) was administered to cattle weighing less than 225 kg.
Cattle were individually selected for market readiness by visual appraisal by the feedlot manager and sent to the abattoir for slaughter. Slaughter of the trial animals took place between August and October 2003. Postbleeding weight was recorded 6 min after stunning and bleeding. Live slaughter weight was then calculated as postbleeding weight x 100/96.5, assuming that blood comprised 7% of live weight and that 50% of this was bled out after 5 to 6 min (Wilson, 1991). Average daily gain was then calculated for each animal for the periods from processing to d 35, d 35 to slaughter, and processing to slaughter.
Health Evaluation
Throughout the finishing period, each pen of cattle was checked daily at 0600 and 1500 by experienced feedlot personnel. Animals were first observed from a distance before being stirred by the personnel slowly walking through the pen. Calves with little interest in their surroundings or that showed one or more of the following signs were removed from the pen: lethargy or listlessness, drooping ears, excessive salivation, ocular or nasal discharge, dirty nostrils, decreased rumen fill compared with pen-mates, or increased respiratory rate and effort. Identified animals were walked to the treatment area, where respiratory rate and effort were assessed after the walk, and rectal temperatures were taken. All cattle with a rectal temperature >40°C were treated for BRD unless specific signs indicating another disease were present (e.g., anemia or icterus indicating anaplasmosis), in which case appropriate treatment was given. Animals with a rectal temperature <40°C but showing other signs of respiratory disease (e.g., coughing, polypnea/dyspnea, or nasal or ocular discharge) were also treated for BRD.
The BRD treatment protocol prescribed by the consulting veterinarian was as follows: on the day of diagnosis animals were administered oxytetracycline (Engemycin; Intervet SA; approximately 10 mg/kg i.v.) and tylosin (Tylan 200; Elanco AH, Bryanston, South Africa; approximately 10 mg/kg i.m.); on the following day, animals were treated again with the same dosages of these antibiotics, but oxytetracycline was administered i.m. instead of i.v.; on the third day, animals were treated with trimethoprim/sulfadiazine (Norodine 24; Bayer; approximately 15 mg/kg i.m.). If a marked clinical improvement was not observed by the fourth day, the same protocol was repeated. No further laboratory diagnostic procedures were performed.
Lung Lesion Evaluation
Lungs were inspected in the abattoir at line speed (average of 20/h) by a single examiner as they hung with their dorsal aspect facing the observer at eye level. Scoring was done visually and by palpation of each of the lung lobes beginning cranially. Lung lesions were recorded using a system modified from Bryant et al. (1999), paying specific attention to cranioventral lesions (considered to result from bronchopneumonia). A bronchopneumonia score was assigned to each set of lungs [0 = no visible or palpable lesions, or mild hyperemia of the cranioventral lung lobes without any consolidation; 1 = consolidation of up to 50% of the cranioventral lobe(s); and 2 = consolidation of 51 to 100% of the cranioventral lobe(s)]. In addition, a pleural adhesion score was recorded for each set of lungs (0 = no adhesions or pleuritis; 1 = adhesions or pleuritis present, but involving <50% of the lung/pleural surface; and 2 = adhesions or pleuritis present, involving >50% of the lung/pleural surface). Any other lesions occurring elsewhere in the lungs were recorded as other and not differentiated with regard to type or area of involvement.
Case Definition
The presence of lung lesions at slaughter was defined as a bronchopneumonia score of 1 or more, or a pleural adhesion score of 1 or more, or both. An animal was then defined as having suffered from BRD during the finishing period if it showed lung lesions at slaughter, or had been treated for BRD, or both. Thus, an animal was regarded not to have suffered from BRD during the finishing period only if it had not been treated for BRD and showed no lung lesions at slaughter. This combined case definition was used to provide a better estimate of the true incidence of BRD and therefore to obtain a more realistic estimate of its effect on performance, compared with using the various criteria individually.
Statistical Analysis
For all analyses, the experimental unit was the individual animal. Associations between discrete variables were assessed by cross-tabulation and analyzed using 
2 or Fisher’s exact test. Univariable associations of the main independent variables (treatment for BRD, presence of lung lesions, bronchopneumonia score, pleural adhesion score, and overall occurrence of BRD) and potential confounders [site, region of origin, sex (recorded as steer, bull castrated on arrival, or heifer), processing weight, d 56 implant, and other disease] with the dependent variables ADG and DOF were analyzed using simple linear regression. Animals originated from 21 different regions; origin was therefore modeled as 20 binary indicator variables. Regardless of significance in the simple linear regression analyses, all independent variables were then entered into multiple regression models. Site, however, was completely explained by region of origin (all animals from any particular origin went to one feedlot site only), and was therefore not included in the multiple regression analysis. In addition, 2-way interactions between the main independent variable and sex, d 56 implant, and other disease were included in each multiple regression model. The models were then developed by backward elimination; variables were retained in the model if they remained significant (Wald’s P 
0.05) or if their removal resulted in a >10% change in the coefficient for the main independent variable. Finally, the multiple linear regression models were assessed for linearity, homoscedasticity, and normality by examining residual scatter plots and histograms. Statistical analyses were done using NCSS 2004 statistical software (NCSS, Kaysville, UT) and a public-domain statistical calculator, EpiCalc 2000 (http://www.brixtonhealth.-com/epicalc.html).
Economic Analysis
Because the aim of the study was to quantify the hidden costs of BRD, only the indirect variable costs of reduced growth rate resulting from BRD were calculated. The labor and medicine costs of treatment and the cost of mortality were not included. Amounts were converted from South African Rand to US dollar at the rate for May 1, 2003 ($1 = 7.26 ZAR; XE.com, 2005). Indirect variable costs (IVC) per animal entering the feedlot were calculated as follows:
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in which the incidence of BRD was calculated using the combined case definition. The meat price was $1.79/kg at the time.
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RESULTS AND DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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The peak incidence of respiratory disease occurred on d 18 after arrival, and by d 35, 87% of all treatments for BRD had been administered. This is within the range previously reported (Wilson et al., 1985; Bateman et al., 1990). Management in the first 4 to 6 wk after arrival in the feedlot is critical; this is clearly the period of greatest risk for BRD. A total of 461 animals (22.6%) were treated for clinical BRD; of these, 17.5% were treated twice or more. This is within the range of 16% to 50% previously reported for North America (Bateman et al., 1990; Bryant et al., 1999; Gardner et al., 1999). Variations in findings between studies could be due to differences in stressors, breeds of calves, origin of calves, season, severity of microbial challenge, and calf management. The only other disease condition that occurred in significant numbers during the trial period was anaplasmosis, which affected 122 animals (6.0%).
Case Definition of BRD
Lung lesions were present at slaughter in 42.8% of all animals. This is similar to that reported by Bryant et al. (1999) and Gardner et al. (1999), but lower than that reported by Wittum et al. (1996). Lesions were present in 38.5% of animals never treated for BRD, in 55.4% of animals treated once for BRD, and in 66.7% of animals treated twice or more for BRD. Overall, animals treated for BRD were more likely to have lung lesions at slaughter than those not treated (relative risk = 1.49; 95% confidence interval 1.35 to 1.65; P < 0.001). However, of animals with lung lesions at slaughter, 69.5% had never been treated for BRD, indicating that many cases were either subclinical or were missed, and/or that animals may have entered the feedlot with preexisting lung lesions. Of animals without lung lesions at slaughter, 16.9% had been treated for BRD, indicating that some lung lesions may have resolved before slaughter, and/or that some false positive BRD diagnoses were made. Although lung lesion detection at slaughter is a more sensitive measure of BRD occurrence than treatment records, neither method alone is satisfactory, and information from both sources should be used.
Using the combined case definition (animals treated for BRD and/or showing lung lesions at slaughter), the estimated overall incidence of respiratory disease was 52.5%. This was markedly greater than the incidence of clinical BRD (22.6%; P < 0.001) or the prevalence of lung lesions at slaughter (42.8%; P < 0.001) and may represent the true incidence of BRD during the finishing period. However, the presence of any animals with preexisting lung lesions that persisted to slaughter, as well as other diseases misdiagnosed as BRD during the finishing period, may have resulted in an overestimate of the true BRD incidence. On the other hand, the occurrence of undiagnosed cases of BRD resulting in lesions that resolved before slaughter may have resulted in an underestimate of the true incidence. The relative magnitude of these 2 biases was impossible to measure.
Nevertheless, the combined case definition may provide a more accurate estimate of BRD incidence than either component separately. Of all animals estimated by this definition to have suffered from BRD, 43.2% (95% confidence interval 40.3%, 46.3%) had been treated for BRD, and 81.5% (95% confidence interval 79%, 83.8%) had lung lesions present at slaughter. Subject to the biases mentioned above, these respectively provide estimates of the sensitivity of using either treatment records alone or lung lesion recording alone to measure BRD incidence.
Effect of BRD on Performance
The final multiple regression models estimating the effect of the various measures of BRD on ADG are shown in Tables 1 to 7. The residual scatter plots and histograms for the final models showed no obvious violations of the assumptions of linearity, homoscedasticity, and normality.
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) and with a 2.7 d increase in DOF (P = 0.006; Table 7), compared with calves not showing clinical BRD. This effect on ADG is very similar to some previous North American reports (Jim et al., 1993; Wittum et al., 1996), but much less than others; Bateman et al. (1990) and Gardner et al. (1999) reported reductions in ADG of 60 g.
Differences between studies regarding the impact of morbidity on performance may be due to several factors. The BRD case definition differed between studies. In some studies a fever had to be present for diagnosis of BRD (Jim et al., 1993), whereas others used clinical signs together with rectal temperature (Bateman et al., 1990; Gardner et al., 1999). Thus, some studies might have identified only the more severe cases. Viral causes of BRD with no secondary bacterial involvement and causing no persistent lung lesions may affect ADG much less than bacterial cases resulting in lung lesions, although viral cases may still be detected and treated. The accuracy of the clinical diagnosis of BRD, as well as the severity of the disease, may vary greatly between feedlots, and this will also influence estimates of the effect of BRD on performance.
Calves treated for BRD showed a 169 g reduction in ADG during the early finishing period (P < 0.001) but no reduction in ADG from d 35 onward (Table 1). This is comparable to the 140 g reduction in ADG in treated calves over the first 28 d of the finishing period reported by Bateman et al. (1990) and Van Donkersgoed et al. (1993). Because most clinical cases of BRD occur during the first few weeks of the finishing period (Jensen et al., 1976; Radostits et al., 2000), it is likely that this large reduction in growth rate is associated with the actual episode of clinical disease. Sowell et al. (1999) reported that animals diagnosed with BRD spent less time at, and/or made fewer trips to, the feed bunk during their first 4 d in the feedlot and for several days before they were clinically identified as being sick. Furthermore, during the time they spend in the hospital pens, sick animals are fed a ration with lower NE content. This reduced feed and energy intake is probably a major factor contributing to the reduced ADG shown by sick cattle during this period. Jim et al. (1993) showed that animals classified as sick during the first 4 wk after arrival had a lower daily DMI but, in contrast to our study, failed to show a reduction in ADG during that period.
There was no evidence in this study of a difference in ADG between animals treated once for BRD and those treated more than once (P = 0.63). This is in contrast to Morck et al. (1993), who found that re-treated animals had decreased gains nearly twice those of animals treated once only, and Gardner et al. (1999), who found a 140 g decrease in ADG for animals treated more than once vs. animals treated once only. The reason for this difference is not clear, although it is possible that in he current study early detection of clinical BRD and effective antimicrobial therapy may have limited the development of severe, chronic lesions to a greater extent than in other studies.
Effect of Clinical vs. Subclinical BRD.
Subclinical BRD occurred in 29.7% and clinical BRD in 22.6% of calves in this study. After adjustment for origin and sex, there was no difference in processing weight among animals that did not suffer from BRD, those that developed subclinical BRD, and those that were subsequently treated for clinical BRD (P = 0.69). However, at d 35, those that had subclinical BRD were 3.8 ± 1.8 kg lighter (P = 0.03) and those that had been treated for BRD were 8.1 ± 2.0 kg lighter (P < 0.001) than animals that remained free from BRD. At slaughter, no difference was observed among weights of the 3 categories of animals; however, animals that had suffered from BRD, whether subclinical or clinical, took approximately 5 d longer to reach this same slaughter weight (P < 0.001; Table 7).
The greater reduction in ADG in calves with clinical vs. subclinical BRD during the early finishing period (Table 2) might have been because of reduced feed and energy intake during their stay in the hospital pen and because the treated animals tended to be those with more severe pneumonia. However, from d 35 onward, the treated clinical BRD cases tended (P = 0.11) to grow faster (by 27 g/d) than animals with subclinical BRD, and by the end of the finishing period, no difference (P = 0.51) was detected in overall ADG between clinical and subclinical BRD cases. Therefore, treatment of clinical cases was effective in curtailing much of the potential economic losses due to BRD, although it did not restore growth to the level of that of healthy animals. The absence, due to ethical reasons, of an untreated group with clinical BRD prevented us from quantifying the effect of antibiotic treatment.
The fact that subclinical BRD had a marked effect on ADG indicates that reduced feed and energy intake during the hospital period is not the only reason for the reduced growth rate associated with BRD. It is likely that not only latent clinical cases but also subclinical cases exhibit the reduction in feeding behavior reported by Sowell et al. (1999). In addition, a febrile response, which is typical of BRD and which may also occur in subclinical cases, is known to accelerate protein and energy metabolism (Howard, 1972), and the protein or caloric cost of fever can theoretically be calculated (Loew, 1974).
Williams et al. (1993) also showed that a high degree of immune stimulation depressed feed intake, apparent nitrogen digestibility, tissue growth, and weight gain of pigs. Although the slightly (15 g/d) higher ADG during the late finishing period in animals treated for BRD compared with that of healthy animals was not significant (P = 0.34; Table 2), it raises the possibility that some compensatory growth may occur in successfully treated cases. This has been reported following clinical pneumonia caused by Mycoplasma hyopneumoniae in pigs (Clark et al., 1990) and over a longer period following enzootic pneumonia in beef calves (Thomas et al., 1978), but to our knowledge has not been shown in feedlot calves.
Effect of Lung Lesions.
Lesions resulting from BRD in feedlot calves occur in the cranioventral lung lobes and are characterized by bronchopneumonia or its sequelae, including collapse/consolidation, pleural adhesions, abscesses, parenchymal fibrosis, or emphysema (Bryant et al., 1999). In this study, parenchymal bronchopneumonic lesions were found at slaughter in 8.6% and pleural adhesions in 38.8% of calves. An interaction (P = 0.009) was found between sex and the presence of lung lesions (bronchopneumonia and/or adhesions/pleuritis) at slaughter, in their effect on ADG for the overall finishing period (Table 3). Lesions were associated with an approximately 40 g reduction in ADG of males but had no significant effect in heifers. The reason for this is unclear, and it was not seen individually in either the early or the late period. The average effect of the presence of lung lesions at slaughter on overall ADG in this study was a 23 g reduction (P = 0.02), similar to the 26 g reduction reported by Bryant et al. (1999) but less than the 76 g reported by Wittum et al. (1996) and the 180 g reported by Gardner et al. (1999). The difference between studies in the effect of lung lesions on ADG could be due to different methods of lung lesion scoring or differences in severity of respiratory disease and extent of resultant lesions. The presence of lung lesions was more strongly associated with reduced ADG than the occurrence of clinical disease, presumably because it can be assumed that only more severe BRD will cause lung lesions that persist long after clinical recovery. Lung lesions at slaughter were also associated with a 5.5 d increase in DOF (Table 7).
The model in Table 4 shows little evidence of an association between the extent of bronchopneumonic lesions found at slaughter and ADG during the early finishing period (P = 0.3). Thomson et al. (1975) reported that in 6- to 10-mo-old calves (n = 44) shipped from western Canada to Ontario, 40 (91%) showed lung lesions when slaughtered 12 d after arrival, and clinically ill animals had more extensive lung lesions 12 d after arrival than apparently healthy calves. Most lung lesions therefore probably develop early in the finishing period, and during that period more extensive lesions appear to be associated with more severe disease. However, as suggested by Bryant et al. (1999), differences in healing rates and fibrin contraction may result in the extent of the lesions seen at slaughter not being representative of the original extent of the pneumonia. Our results would support such a hypothesis.
However, extensive bronchopneumonia (score 2) at slaughter was associated with an 88 g reduction in ADG during the late finishing period (P = 0.02; Table 4), and this effect tended (P = 0.14) to be greater than that of score 1. This suggests that the extent of lesions affects growth rate during the late finishing period, and more extensive lesions, with more persistent active inflammation, have a more sustained negative effect on growth.
In animals with lung lesions at slaughter, Gardner et al. (1999) differentiated between those with active and those with inactive bronchial lymph nodes but did not assess extent or severity; those with active lymph nodes had 18% lower ADG over the entire 150-d finishing period. In our study, activity of the bronchial lymph nodes was not assessed, but those with active bronchial lymph nodes may have had more extensive bronchopneumonia at slaughter. The association between extent of bronchopneumonia and reduced growth during the late finishing period may also be due to some animals developing BRD late in their finishing period, when pen observation may have been less diligently applied, resulting in cases being overlooked. Over the entire finishing period, the presence of parenchymal bronchopneumonic lesions at slaughter was associated with a 38 g reduction in ADG (P = 0.03).
Table 5 shows that pleural adhesions affected ADG over the entire finishing period with score 2 tending to have a more severe effect than score 1 (83 vs. 21 g reduction; P = 0.11). In contrast to bronchopneumonic lesions, however, pleural adhesions at slaughter were indicative of large reductions in ADG during the early, rather than the late, finishing period; more extensive adhesions had a larger effect. The presence of adhesions at slaughter therefore likely indicates that a severe episode of BRD occurred during the early finishing period. After d 35, however, the effect of adhesion score on ADG was no longer significant, suggesting that persistent pleural adhesions had little effect on growth later during the finishing period in this study. Over the entire period from processing to slaughter, the presence of pleural adhesions was associated with a 24 g reduction in ADG (P = 0.02), comparable to the 38 g reduction associated with parenchymal bronchopneumonic lesions. To our knowledge, only Wittum et al. (1996) examined the effect of pleuritis on ADG, and found it to be the same as that of bronchopneumonic lesions (76 g reduction in ADG over the entire finishing period). Our study showed that although the overall effects of the 2 lesions found at slaughter may be comparable, they are indicative of production losses having occurred at different times during the finishing period.
Overall Effect of BRD.
The final multiple regression models estimating the overall effect of BRD on ADG, using the combined case definition, are shown in Table 6. The greatest effect of BRD on growth occurred during the early finishing period with little effect noted in the later period. The occurrence of BRD in this study was associated with a 24 g decrease in ADG for the period from processing to slaughter (P = 0.02) and with a 5.1 d increase in DOF (P < 0.001). This estimate of the effect of BRD on DOF is close to that produced by only considering the presence of lung lesions at slaughter but quite different from that produced when considering only clinical BRD. This demonstrates the inadequacy of using only treatment records to determine the extent and impact of BRD.
Economic Effect of BRD
The economic loss due to reduced growth rate in calves treated for BRD or with subclinical BRD, for a mean DOF of 137 d and a mean dressing percent of 58%, was $3.41/calf. At the BRD incidence of 52.5% found in this study, this equated to $1.79/calf entering the feedlot. This figure is lower than estimates of the effect of BRD in North America (Jim et al., 1993; Gardner et al., 1999; Smith, 2000). However, it is difficult to compare the 2 regions because of differences in the meat price and DOF, and an extremely volatile currency exchange rate. The approximate throughput of cattle in all South African feedlots is 1.35 million animals per year (SAFA, 2004). If these results are generalized to the entire country, they indicate an estimated annual loss of approximately $2.42 million to the South African feedlot industry. To calculate the overall impact of the disease, this value should be added to the direct medicine and labor costs of treating BRD cases, the losses due to BRD-associated mortality, and the costs of prophylactic measures.
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IMPLICATIONS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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Footnotes |
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3 Present address: Schering-Plough Animal Health, PO Box 46, Isando, 1600, South Africa.
2 Corresponding author: peter.thompson{at}up.ac.za
Received for publication April 19, 2005. Accepted for publication September 24, 2005.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONIMPLICATIONSLITERATURE CITED |
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