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Incidence of clostridial dermatitis (cellulitis) and factors for development of the disease in turkeys
C The Author 2016. Published by Oxford University Press on behalf of Poultry Science Association. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected].
Incidence of clostridial dermatitis (cellulitis) and factors for development of the disease in turkeys Megan E. Lighty,∗ Franc¸ois Elvinger,∗ Robert D. Evans,† Nammalwar Sriranganathan,‡ Tanya LeRoith,‡ and F. William Pierson∗,1 ∗
Department of Population Health Sciences, Virginia-Maryland College of Veterinary Medicine, Blacksburg, Virginia 24061-0442; † Elanco, Harrisonburg, Virginia 22801; and ‡ Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Blacksburg, Virginia 24061-0442
SUMMARY Clostridial dermatitis, also referred to as cellulitis, is a disease of serious concern in turkeys in the United States whose incidence appears to have increased since its emergence in the early 1990s. The disease leads to increased mortality with the presence of fluid- and gasfilled lesions in the subcutaneous tissues of the breast, thigh, and tail-head. Management factors may contribute to the development of clostridial dermatitis. An analysis of mortality and health records of turkey flocks conducted over a one-year period for one commercial turkey operation indicates that breed, flock type, weight at processing, and stocking density affected the incidence of clostridial dermatitis. Season of placement, season of onset, prior health events, and prior vaccination and/or medication did not affect the incidence of clostridial dermatitis. Development of clostridial dermatitis, flock type, season of placement, and season of onset of clostridial dermatitis affected livability. Breed did not affect livability. In a survey of 8 commercial turkey companies, 639 of 3,398 market turkey flocks (18.8%) had developed clostridial dermatitis, and 239 of 967 farms (24.7%) raising market turkeys had at least one flock develop clostridial dermatitis over the course of a calendar year, with an estimated increase in the cost of production for flocks that developed clostridial dermatitis of 0.031 to 5.5 cents per kilogram of meat produced. Key words: clostridial dermatitis, cellulitis, Clostridium, turkeys 2016 J. Appl. Poult. Res. 25:104–112 http://dx.doi.org/10.3382/japr/pfv065
DESCRIPTION OF PROBLEM Within the last 20 years the commercial turkey industry has experienced an increase in the frequency and severity of subcutaneous clostridial infections, and poultry veterinari1
Corresponding author: [email protected]
ans have ranked clostridial dermatitis as a top concern facing the turkey industry [1–4]. Clostridial dermatitis appears to be restricted to the commercial turkey industry; there have been no reports of this condition in wild, heritage breed, range-reared, or organic turkeys. Clostridial dermatitis, also referred to as cellulitis, is thought to be caused primarily by
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Primary Audience: Veterinarians, Live Production Managers, Flock Supervisors, Researchers
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The objectives of this study were to determine risk factors for occurrence of clostridial dermatitis in one commercial turkey operation and to evaluate incidence, disease management factors, and economic impact of clostridial dermatitis in commercial turkey operations across the United States.
MATERIALS AND METHODS Study 1: Regional Incidence and Risk Factors Production and health records were obtained from a commercial turkey company in the MidAtlantic region for 1,057 flocks placed on 167 farms between January 1, 2007, and December 31, 2007, for a retrospective analysis of incidence and risk factors for the development of clostridial dermatitis. Eight hundred eighteen flocks were light-hen flocks, which were processed at a median age of 13.1 wk (minimum 12.1; maximum 14.1) with an average weight of 7.1 ± 0.44 (mean ± standard deviation) kilograms at processing. One hundred eighty-one flocks were heavy-hen flocks, which were processed at a median age of 17.3 wk (minimum 16.3; maximum 18.4) with an average weight of 10.4 ± 0.52 kilograms. Fifty-eight flocks were identified as tom flocks, which were processed at a median age of 20.1 wk (minimum 15.1; maximum 21) with an average weight at processing of 18.5 ± 1.16 kilograms. Two hundred twenty-five flocks placed were Hybrid breed turkeys, 734 flocks were Nicholas (Aviagen Turkeys, Inc.) breed turkeys, and 96 flocks were composed of a mixture of Hybrid and Nicholas turkeys. Identification of flocks positive for clostridial dermatitis was based on visual confirmation of postmortem lesions consistent with clostridial dermatitis as determined by the flock supervisors and/or the company veterinarian. Health and production data were reviewed for each flock from the time of placement through the time of processing. Descriptive statistics were generated using JMP 8.0 software [13]. SAS 9.3 software was used to analyze risk factors for development of clostridial dermatitis by either Proc LOGISTIC or Proc FREQ [14]. Proc LOGISTIC was used to evaluate the effect of flock type, breed, stocking density, final weight at processing, prior
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Clostridium septicum [5, 6]. Clostridium perfringens and C. sordellii also may be involved [5–7]. For an individual bird to be considered a case of clostridial dermatitis based on the official definition developed by veterinarians and industry representatives, the bird must present with at least 2 of the following 7 signs: 1) subcutaneous emphysema; 2) subcutaneous serum and/or serosanguinous fluid; 3) vesicles on the skin, especially on the breast-inguinal area; 4) moist, dark, wrinkled skin, especially on the breast-inguinal area; 5) cellular necrosis (microscopic); 6) organ involvement (spleen and/or liver); and 7) vesicles on the skin, moist, dark, wrinkled skin, or both on the tail area [6]. A flock is diagnosed with clostridial dermatitis if the mortality with lesions characteristic of the disease is greater than or equal to 0.5 dead birds per 1,000 birds per d for 2 consecutive 24-hr periods [6]. Personal communications with flock supervisors and company veterinarians suggest that elevated mortality with characteristic necrotic lesions on the breast and inguinal regions is the main criterion used in the field to identify clostridial dermatitis-positive flocks. Histopathology and bacteriological isolation are generally not performed in routine diagnostics. The pathogenesis of clostridial dermatitis is not fully understood. It is hypothesized that the natural route of infection is via hematogenous spread of organisms invading or leaking from the gastrointestinal tract [6, 8]. While similarities exist between clostridial dermatitis of turkeys and gangrenous dermatitis of broiler chickens, the subcutaneous lesions of clostridial dermatitis are typically not accompanied by skin scratches and lesions seen in classic gangrenous dermatitis in broiler chickens. Some laboratories have reported success with experimental models to study clostridial dermatitis in turkeys by subcutaneous and intravenous injection of C. septicum [5, 9, 10]. However, it is thought that an oral challenge model would be better suited to study this disease since a gastrointestinal source of Clostridium species may be implicated in natural infections [9]. The limited success of oral challenge models in eliciting the disease has led some researchers to believe that the natural route of infection is through breaks or scratches in the skin [6, 9, 11, 12].
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Study 2: National Incidence and Economic Impact A 2-part survey was e-mailed to the member companies of the National Turkey Federation in March 2009. A first questionnaire was directed to the flock supervisors or servicepersons in each company and included questions on the incidence of clostridial dermatitis and aspects of disease management (Table 1). The second questionnaire was directed to the live production and/or complex managers to obtain information on the economic impact of clostridial dermatitis on their operation (Table 2). Questions pertained to turkey flocks marketed during the 2008 calendar year. Completed company responses were collected by the National Turkey Federation’s legal counsel. All identifying company information was removed and anonymized responses were sent to the authors for analysis.
RESULTS AND DISCUSSION Study 1: Regional Incidence and Risk Factors Fifty-three of 167 farms (31.7%) had at least one flock placed in 2007 that developed clostridial dermatitis, which affected 120 of 1057 placed flocks (11.4%; Table 3). Flock type affected the incidence of clostridial dermatitis (P < 0.0001). The incidence of clostridial der-
matitis was highest in tom flocks and lowest in light-hen flocks, as is generally reported by the industry [6]. The odds of tom flocks to develop clostridial dermatitis were 4.9 times the odds of light-hen flocks to develop the disease (95% confidence interval (CI): [2.7; 9.2]). The odds of heavy-hen flocks to develop cellulitis were 3.4 times the odds of light-hen flocks to develop the disease (95% CI: [2.2; 5.3]). Breed affected the incidence of clostridial dermatitis (P = 0.0216). Twenty-one of 225 (9.3%) Hybrid flocks, 95 of 734 (12.9%) Nicholas flocks, and 4 of 96 (4.2%) mixed flocks developed clostridial dermatitis. However, when flock type and breed were both included in a stepwise selection logistic regression model, only flock type remained significant (P < 0.0001). This corresponds to results from a 2010 USDA study evaluating risk factors for the development of clostridial dermatitis in which effect of breed also was found not significant [7]. Flock type was not evaluated in the USDA study. It has been reported that incidence and severity of cellulitis are worse in the summer and early fall [2, 7, 15]. In this study, season of placement was not associated with the occurrence of cellulitis (P = 0.2240; Table 4). No flocks placed in 2007 developed clostridial dermatitis in January through April 2007; however, this does not necessarily imply that no flocks developed clostridial dermatitis during those months since flocks placed in 2006 (which were not included in this study) may have developed clostridial dermatitis during that time period. Flocks placed in January 2007 would be outside the expected age range for onset of clostridial dermatitis in January and February 2007. Onset of clostridial dermatitis was associated with season (P = 0.0003; Table 5); few flocks, however, were truly at risk for developing clostridial dermatitis during winter 2007 since many of these flocks were younger than the expected age range for onset of clostridial dermatitis. When data for winter 2007 were omitted from the analysis, season was not associated with onset of disease (P = 0.7141). Results from this study do not show evidence for a seasonal effect on clostridial dermatitis incidence. The age at time of onset of clostridial dermatitis varied with flock type (P = 0.0018). For light-hen flocks the minimum, maximum,
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health events, and prior vaccination and/or medication on the development of clostridial dermatitis. Proc FREQ with Fisher’s exact was used to evaluate the effect of season of placement and season of onset on the development of clostridial dermatitis. Proc GLM was used to determine the factors affecting livability in a model containing development of clostridial dermatitis, flock type, breed, season of placement, and all 2-way interactions with development of clostridial dermatitis. Effect of season of onset on livability was evaluated in a separate model that included flock type, breed, season of onset, and all 2- and 3-way interactions. Interactions that were not significant were removed from the final models. Livabilities are reported as least square means ± standard error. The effect of a factor was determined to be significant at P < 0.05.
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Table 1. Questions included in survey distributed to flock supervisors/servicepersons within each member company of the National Turkey Federation. 1. In 2007, the National Turkey Federation developed a definition of clostridial dermatitis that included the signs and criteria listed below. What signs or criteria have you or would you have used in 2008 to determine that turkeys in flocks that you supervised had clostridial dermatitis? (please check all that apply) Subcutaneous emphysema (air-bubbles under the skin) Serum/serosanguineous subcutaneous fluid (fluid accumulation under the skin) Vesicles (blisters) on the skin, especially in the breast/inguinal area Moist, dark, wrinkled skin, especially in the breast/inguinal area Cellular necrosis (microscopic) Organ involvement (spleen/liver) Vesicles on the skin, and/or moist, dark, wrinkled skin in the tail area Clostridium septicum, C. perfringens type A, or C. sordelli isolated from fluid or affected skin/tissue samples of affected/dead birds Elevated mortality Other
For the following questions, please provide YOUR own opinion or knowledge derived from YOUR experience as a turkey flock supervisor/serviceperson. 8. What are your thoughts concerning the causes of and risk factors for clostridial dermatitis in turkeys? (Please rank in order of importance.) 9. What do you think are the best management/treatment options for flocks with clostridial dermatitis? (Please rank in order of importance.) 10. What do you think are the best options to prevent flocks from developing clostridial dermatitis? (Please rank in order of importance.)
and average (mean ± standard deviation) ages at time of onset were 8, 14, and 11.2 ± 1.12 wk; for heavy-hen flocks 4, 17, and 13.0 ± 2.97 wk; for tom flocks 7, 19, and 13.1 ± 3.40 wk. Historically, clostridial dermatitis lesions have
typically been seen in older birds near the time of market. Onset of the disease generally occurs between 13 and 18 wk of age, with the youngest age of onset reported to be 6 wk of age [2, 6, 9, 15]. Earlier age of onset observed in this
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For the following questions, please consider only those flocks that you supervised and which were marketed during the 2008 calendar year (January 1, 2008 – December 31, 2008). 2. How many FARMS did you supervise that had flocks marketed during 2008? 2a. What was the sum total of houses on these farms? 3. What is the average flock size for those flock types which you supervise? If you do not supervise a particular flock type, please write N/A. 3a. Average flock size (# of birds) for light hens 3b. Average flock size (# of birds) for heavy hens 3c. Average flock size (# of birds) for light toms 3d. Average flock size (# of birds) for heavy toms 4. How many FLOCKS under your supervision were marketed during the 2008 calendar year? 4a. Number of light hen flocks 4b. Number of heavy hen flocks 4c. Number of light tom flocks 4d. Number of heavy tom flocks 5. How many FARMS supervised by you had at least one flock marketed in 2008 that at some point during production had signs which you considered compatible with clostridial dermatitis? 6. How many FLOCKS supervised by you and marketed during the 2008 calendar year had signs that you considered compatible with clostridial dermatitis? 6a. Number of light hen flocks that had clostridial dermatitis 6b. Number of heavy hen flocks that had clostridial dermatitis 6c. Number of light tom flocks that had clostridial dermatitis 6d. Number of heavy tom flocks that had clostridial dermatitis 7. What was the average% livability for FLOCKS that developed clostridial dermatitis? 7a. Average% livability for light hen flocks with clostridial dermatitis 7b. Average% livability for heavy hen flocks with clostridial dermatitis 7c. Average% livability for light tom flocks with clostridial dermatitis 7d. Average% livability for heavy tom flocks with clostridial dermatitis
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Table 2. Questionnaire distributed to each live production/complex manager within each member company of the National Turkey Federation. 1. For flocks marketed during the 2008 calendar year, was there a difference in the live production costs between flocks that had clostridial dermatitis and flocks that did not have clostridial dermatitis? (yes or no) 2. If you answered yes to the previous question, please calculate the difference in average live production costs between flocks that had clostridial dermatitis and flocks that did not have clostridial dermatitis? (cents/lb)
Table 3. Incidence of clostridial dermatitis in flocks of one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). N
206 8 11 225
Hybrid NCD 2 16 2 3 21
%CD
3
N
7.8 25.0 27.3 9.3
522 165 47 734
Nicholas NCD %CD 45 36 14 95
8.6 21.8 29.8 12.9
N 88 8 0 96
Mixed NCD 2 2 0 4
%CD
N
2.3 25.0 n/a 4.2
8184 181 58 1057
All Breeds6 NCD %CD 63 40 17 120
7.7 22.1 29.3 11.4
1
Number of flocks. Number of flocks with clostridial dermatitis. 3 Percent of flocks with clostridial dermatitis. 4 The total number of light-hen flocks includes 2 flocks for which breed was not identified. 5 Flock type associated with incidence of clostridial dermatitis in univariate (P < 0.0001) and multivariate analysis (P < 0.0001). 6 Breed associated with incidence of clostridial dermatitis in univariate analysis (P = 0.0216). 2
Table 4. Incidence of clostridial dermatitis in flocks placed for grow-out in a particular season for farms from one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). Season of placement1
Total number of flocks placed
Number (percent) of flocks that developed clostridial dermatitis
Winter 2007 Spring 2007 Summer 2007 Fall 2007
195 298 314 250
28 (14.4) 38 (12.6) 32 (10.2) 22 (8.8)
1
Winter 2007 includes flocks placed in January, February, and March; spring 2007 includes flocks placed in April, May, and June; summer 2007 includes flocks placed in July, August, and September 2007; fall 2007 includes flocks placed in October, November, and December 2007.
study may be due to increased awareness of flock supervisors/veterinarians and a better ability to detect early signs of the disease. Given that weight at processing is dependent on flock type, the effect of average weight at time of processing was analyzed for each flock type separately (Table 6). For each additional kilogram of weight at time of processing, heavy hens were 3.92 times more likely to develop clostridial dermatitis (P = 0.0003). Weight at processing did not affect the odds of developing clostridial dermatitis in light hens (P = 0.6285) and toms (P = 0.8262). For light-hen flocks the minimum, maximum, and average (mean ± standard deviation) bird densities at time of placement were 2.2, 16.1, and
4.4 ± 1.33 birds per square meter; for heavy-hen flocks 1.3, 6.7, and 3.3 ± 0.49 birds per square meter; and for tom flocks 2.2, 4.2, and 2.7 ± 0.30 birds per square meter. Bird density had a limited effect on the incidence of clostridial dermatitis. Given that the amount of floor space allotted per bird varies with flock type, the analysis also was conducted for flocks within each flock type. Bird density was not associated with clostridial dermatitis in light hens (P = 0. 7026) or heavy hens (P = 0.8071); but there was a tendency in toms flocks that for every additional bird per square meter of floor space at time of placement tom flocks were 7.8 times more likely to develop clostridial dermatitis (P = 0.0772). Stocking density is also commonly reported in weight
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Light hens Heavy hens Toms All flocks5
1
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Table 5. Season of onset of clostridial dermatitis in turkey grow-out flocks placed in 2007 for farms of one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). Season of clostridial dermatitis onset1
Number of flocks present in a given season
Number (percent) of flocks developing clostridial dermatitis
Winter 2007 Spring 2007 Summer 2007 Fall 2007 Winter 2008
197 493 644 588 281
0 (0) 30 (6.1) 41 (6.4) 30 (5.1) 19 (6.8)
1 Winter 2007 includes flocks present in January, February, or March 2007; spring 2007 includes flocks present in April, May, or June 2007; summer 2007 includes flocks present in July, August, or September 2007; fall 2007 includes flocks present in October, November, or December 2007; winter 2008 includes flocks present in January, February, or March 2008.
Factor
Category
Odds ratio
95% Confidence interval
P-value
Weight at processing
Tom Heavy hen Light hen
0.948 3.921 1.155
[0.588; 1.529] [1.875; 8.199] [0.643; 2.075]
0.8262 0.0003 0.6285
Stocking density (birds)2
Tom Heavy hen Light hen
7.836 0.912 0.960
[0.799; 76.888] [0.437; 1.905] [0.779; 1.183]
0.0772 0.8071 0.7026
1
1 2
Live weight, in kilograms. Stocking density, in birds per square meter of floor space.
per unit area. When the analysis was conducted for weight in kilograms at time of processing per square meter of floor space, stocking density affected the incidence of clostridial dermatitis (P = 0.0032). For each additional kilogram of weight per square meter of floor space flocks were 1.025 (95% CI: [1.008; 1.041]) times more likely to develop clostridial dermatitis. This is consistent with other reports that associate increased stocking density with an increased incidence of clostridial dermatitis [6, 11] although stocking density by weight did not affect any of the individual flock types (P > 0.10) in this study. As C. septicum and C. perfringens are normal inhabitants of the turkey’s gastrointestinal tract, overgrowth of the organism and/or suppression of the bird’s immune system are thought to play important roles in the development of clostridial dermatitis. Maintenance of good intestinal health has been implicated as an important factor in preventing clostridial dermatitis [6, 8]. However, no association was found between prior health events and development of clostridial dermatitis (P = 0.9595); in particu-
lar, the presence of a prior enteric disease event had no impact on the incidence of clostridial dermatitis in this study (P = 0.9771). Prior leg issues, including conformational problems and synovitis, were not associated with an increased incidence of clostridial dermatitis (P = 0.9192). Administration of medications or vaccinations also had no effect on the incidence of clostridial dermatitis (P = 0.8306). Livability is defined as the percentage of birds placed that survive to the time of processing (percent livability = 100 - percent mortality). Livability was 88.8 ± 0.28% for all flocks without clostridial dermatitis and 87.8 ± 0.44% for all flocks that developed clostridial dermatitis (P = 0.0144). In the USDA 2010 study, average livability was reported to be between 89.3 and 89.9% for flocks without clostridial dermatitis and 83 to 85.8% for flocks with clostridial dermatitis [7]. Mortality risk associated with clostridial dermatitis has been reported as high as one to 2% per wk [7, 9]. Livability was 92.3 ± 0.26% in light-hen flocks, 90.4 ± 0.39% in heavy-hen flocks, and 82.2 ± 0.60% in tom flocks (P < 0.0001). Birds placed in spring 2007
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Table 6. Factors affecting incidence of clostridial dermatitis on farms of one commercial turkey company in the Mid-Atlantic region based on retrospective evaluation of mortality and health reports and univariate analysis of individual risk categories (Study 1).
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Table 7. Reports of clostridial dermatitis for commercial turkeys marketed during 2008 based on a national survey (Study 2).
Companies Farms Flocks Light hens Heavy hens Light toms Heavy toms 1
Total number
Number with clostridial dermatitis
Percent with clostridial dermatitis
8 967 3398 573 211 148 2466
6 2391 639 0 10 11 618
75 24.7 18.8 0 4.7 7.4 25.1
Farms with at least one flock marketed during 2008 that developed clostridial dermatitis.
Study 2: National Incidence and Economic Impact Incidence Thirty-nine flock supervisors/company veterinarians representing 8 turkey companies completed the questionnaire on incidence and disease management of flocks marketed in 2008 (Table 7). Clostridial dermatitis was reported on close to 25% of turkey farms in this questionnaire. In a 2010 USDA study of 15 turkey companies across the United States,
42.3% of turkey farms were reported to have at least a slight problem with clostridial dermatitis during the 12 months preceding the study [7]. In the 2007 regional study, Study 1, 7.7% of light-hen flocks developed clostridial dermatitis while no light-hen flocks were affected in Study 2. In Study 2, the national incidence of clostridial dermatitis in heavy-hen flocks was much lower than the incidence in Study 1, 4.7 versus 22.1%, respectively. Incidences of clostridial dermatitis in heavy-tom flocks were similar in Study 1 (29.3%) and Study 2 (25.1%). No comparison can be made for light-tom flocks as the company involved in Study 1 does not raise that type of bird. Livabilities for flocks with clostridial dermatitis ranged from 87 to 96% for heavy-hen flocks, 88 to 95% for light-tom flocks, and 80 to 92% for heavy-tom flocks. The livabilities obtained for heavy hens and toms in Study 1 fall within these ranges. Flock supervisors also were asked to identify the criteria of the official case definition for clostridial dermatitis they actually use in identifying flocks with clostridial dermatitis (Table 8). Nearly all respondents relied on the presence of subcutaneous emphysema (n = 37), serum/serosanguineous subcutaneous fluid (n = 38), and elevated flock mortality (n = 36) in identification of flocks with clostridial dermatitis. Twenty-seven respondents (69.2%) routinely relied on culture of C. septicum, C. perfringens type A, or C. sordelli from affected birds, and only 22 (56.4%) relied on the presence of spleen and liver lesions. Only 5 respondents (12.8%) took samples for histopathology to identify the presence of cellular necrosis at the microscopic level. These results suggest that flock supervisors rely most heavily on gross pathology
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had a livability of 89.3 ± 0.37%, 89.0 ± 0.39% in winter 2007, 88.7 ± 0.36% in summer 2007, and 86.2 ± 0.40% in fall 2007 (P < 0.0001). The effect of season of placement on livability may reflect the impact of environmental factors on mortality during the crucial brooding period. There was no effect of breed on livability (P = 0.3118) and all 2-way interactions with clostridial dermatitis were not significant and therefore not included in the final model. Livability was 92.0 ± 1.02% for light-hen flocks with clostridial dermatitis, 89.0 ± 1.14% for heavy-hen flocks with clostridial dermatitis, and 81.1 ± 1.50% for tom flocks with clostridial dermatitis (P < 0.0001). Livability of flocks that developed clostridial dermatitis in spring 2007 was 89.1 ± 1.27%, 88.4 ± 1.20% in summer 2007, 87.1 ± 1.28% in fall 2007, and 84.9 ± 1.37% in winter 2008 (P = 0.0264). Decreased livability for flocks that developed clostridial dermatitis in fall 2007 and winter 2008 is in contrast to the 2010 USDA study, which reported an increased severity (increased mortality associated with clostridial dermatitis) during the summer and fall months [7]. There was no breed effect on livability of flocks with clostridial dermatitis (P = 0.9093).
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Table 8. Criteria used in identification of clostridial dermatitis-positive flocks in 2008 based on a national survey of flock supervisors (Study 2). Responses from 39 flock supervisors representing 8 companies. Number (percent) of respondents using the criterion
Criterion Subcutaneous emphysema (air bubbles under the skin) Serum/serosanguineous subcutaneous fluid (fluid accumulation under the skin) Vesicles (blisters) on the skin, especially in the breast/inguinal area Moist, dark, wrinkled skin, especially in the breast/inguinal area Cellular necrosis (microscopic) Organ involvement (spleen/liver) Vesicles on the skin, and/or moist, dark, wrinkled skin in the tail area C. septicum, C. perfringens type A, or C. sordelli isolated from fluid or affected skin/tissue samples of affected/dead birds Elevated mortality
36 (92.3)
Table 9. Increase in cost of production associated with development of clostridial dermatitis in commercial turkeys marketed in 2008 based on a national survey (Study 2). Survey code
Company code
Increase in cost of production (cents/kilogram)
EI-1
3
EI-1
3
EI-2 EI-3 EI-4 EI-5 EI-6 EI-7 EI-8
4 5 6 6a 7 8 9
N/A (no cases of clostridial dermatitis) N/A (no cases of clostridial dermatitis) 1.1 2.2 5.5 4.6 0.79 0.031 (toms), 0.037 (hens) N/A (no cases of clostridial dermatitis)
clude: increased mortality pick-up (at least 2 to 3 times per day), administration of penicillin and/or lincomycin via water, full clean-out after every flock, and management to keep litter dry. Prevention strategies include: frequent mortality removal, full clean-out after every flock, maintenance of dry litter conditions, increased down time between flocks, and the use of preventive antibiotics/iodine in the water. These responses are in line with previously published recommendations [6, 7]. Economic impact Seven companies returned the questionnaire on economic impact (Table 9). Two of the 7 companies reported no cases of clostridial dermatitis in turkey flocks marketed during the 2008 calendar year. The average wholesale price for turkeys produced in the United States in 2008 was 124.6 cents per kilogram [17]. Development of clostridial
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findings and mortality when diagnosing flocks with clostridial dermatitis. Flock supervisors were asked to provide their thoughts on the causes and risk factors for the development of clostridial dermatitis, management/treatment options, and prevention strategies for the control of clostridial dermatitis in commercial turkey operations based on their own personal experiences. The most common responses regarding the cause and risk factors for development of clostridial dermatitis included: infrequent mortality removal, wet litter conditions, presence of built-up litter in the house, and stress. While it is commonly reported that increased frequency of mortality removal reduces the incidence and/or severity of clostridial dermatitis [6], the frequency of mortality removal was not associated with the disease status of turkey farms in the 2010 USDA study [7]. In the United States, turkey houses (finishing units) are often not cleaned out between flocks to keep costs down. The use of built-up litter in turkey houses has been implicated in the development of clostridial dermatitis as this practice allows for the accumulation of clostridial spores in the environment [6, 16]. Wet litter, resulting from water spills in the turkey house or from turkeys experiencing diuresis or diarrhea, has been associated with an increased incidence of clostridial dermatitis as it favors the proliferation of Clostridium species in the environment [6, 11]. Dexamethasone treatment, in the absence of C. septicum or C. perfringens challenge, results in the development of clostridial dermatitis, which suggests that stress may be a factor in the development of this disease [11]. Management and treatment options recommended by survey respondents in-
37 (94.9) 38 (97.4) 32 (82.0) 32 (82.0) 5 (12.8) 22 (56.4) 32 (82.0) 27 (69.2)
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112 dermatitis increased the cost of production for market turkey flocks by 0.031 to 5.5 cents per kilogram for the 5 companies that reported cases of clostridial dermatitis.
CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES 1. Rives, D., D. Mills, and S. Clark. 2006. Current health and industry issues facing the turkey industry. Report of the Committee on Transmissible Diseases of Poultry and Other Avian Species. Minneapolis, MN. 2. Carr, D., D. Shaw, D. Halvorson, B. Rings, and D. Roepke. 1996. Excessive mortality in market-age turkeys associated with cellulitis. Avian Diseases. 40:736–741.
Acknowledgments The authors are grateful for the cooperation of the National Turkey Federation and the numerous turkey companies that participated in the regional and national studies. Funding for this study was provided by Cargill Turkey Products, LLC, Harrisonburg, VA, and the Virginia Poultry Growers Cooperative, Hinton, VA.
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1. Flock type, breed, weight at time of processing, and stocking density affected the incidence of clostridial dermatitis. 2. Season of placement, season of onset, prior health events, and prior vaccinations and/or medications did not affect the incidence of clostridial dermatitis. 3. Livability was affected by development of clostridial dermatitis, flock type, season of placement, and season of onset but not by breed. 4. The incidence of clostridial dermatitis was lowest in light-hen flocks and highest in heavy-tom flocks in both studies. 5. The development of clostridial dermatitis increased the cost of production for market turkey flocks by 0.031 to 5.5 cents per kilogram. 6. When practical, producers should consider modifying the flock type, breed, stocking density, target BW, and timing of placement in order to minimize the incidence and/or severity of clostridial dermatitis. 7. Statistical analysis and development of a predictive model for which flocks are likely to develop clostridial dermatitis is constrained by the complex interactions between host, pathogen, and environmental factors that contribute to the development of this disease.
3. Fenstermacher, R., and B. Pomeroy. 1939. Clostridium infection in turkeys. Cornell Veterinary Journal. 29:25– 28. 4. Clark, S., B. Tilley, and D. Mills. 2009. Current health and industry issues facing the turkey industry. Pages 530–535 in Proc. 112th Annual Meeting of the USAHA, Greensboro, NC. Richardson Printing, Kansas City, MO. 5. Tellez, G., N. Pumford, M. Morgan, A. Wolfenden, and B. Hargis. 2009. Evidence for Clostridium septicum as a primary cause of cellulitis in commercial turkeys. Journal of Veterinary Diagnostic Investigation. 21:374–377. 6. Clark, S., R. Porter, B. McComb, R. Lippert, S. Olson, S. Nohner, and H. Shivaprasad. 2010. Clostridial dermatitis and cellulitis: an emerging disease of turkeys. Avian Diseases. 54:788–794. 7. USDA. 2012. Poultry 2010: Clostridial dermatitis on US turkey-grower farms. USDA-APHIS-VS-CEAHNAHMS. 8. Dibner, J. J. 2008. The role of gut barrier failure in gangrenous cellulitis of poultry. Page 20 in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis, Bllomington, MN. 9. Thachil, A., B. McComb, M. Anderson, D. Shaw, D. Halvorson, and K. Nagaraja. 2010. Role of Clostridium perfringens and Clostridium septicum in causing turkey cellulitis. Avian Diseases. 54:795–801. 10. Nagaraja, K., A. Thachil, and D. Halvorson. 2009. Role of Clostridium perfringens and septicum in cellulitis in turkeys. Page 10 in 58th Western Poultry Disease Conference Madison, WI. 11. Huff, G. R., W. E. Huff, and N. C. Rath. 2013. Dexamethasone immunosuppression resulting in turkey clostridial dermatitis: a retrospective analysis of seven studies, 1998– 2009. Avian Dis. 57:730–736. 12. Shivaprasad, H. 2008. Gangrenous dermatitis due to Clostridium septicum in turkeys. in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis Bloomington, MN. 13. JMP. 2008. Version 8. SAS Institute Inc., Cary, NC. 14. SAS User’s Guide. 2010. Version 9.3. SAS Inst. Inc., Cary, NC. 15. McComb, B. 2008. Upper midwest filed perspective of dermatitis in commercial turkeys. Pages 5–8 in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis, Bloomington, MN. 16. Thachil, A., B. McComb, M. Kromm, and K. Nagaraja. 2013. Vaccination of turkeys with Clostridium septicum bacterin-toxoid: evaluation of protection against clostridial dermatitis. Avian Dis. 57:214–219. 17. USDA. 2010. Poultry - Production and value, 2009 summary. National Agricultural Statistic Service.
Incidence of clostridial dermatitis (cellulitis) and factors for development of the disease in turkeys Megan E. Lighty,∗ Franc¸ois Elvinger,∗ Robert D. Evans,† Nammalwar Sriranganathan,‡ Tanya LeRoith,‡ and F. William Pierson∗,1 ∗
Department of Population Health Sciences, Virginia-Maryland College of Veterinary Medicine, Blacksburg, Virginia 24061-0442; † Elanco, Harrisonburg, Virginia 22801; and ‡ Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Blacksburg, Virginia 24061-0442
SUMMARY Clostridial dermatitis, also referred to as cellulitis, is a disease of serious concern in turkeys in the United States whose incidence appears to have increased since its emergence in the early 1990s. The disease leads to increased mortality with the presence of fluid- and gasfilled lesions in the subcutaneous tissues of the breast, thigh, and tail-head. Management factors may contribute to the development of clostridial dermatitis. An analysis of mortality and health records of turkey flocks conducted over a one-year period for one commercial turkey operation indicates that breed, flock type, weight at processing, and stocking density affected the incidence of clostridial dermatitis. Season of placement, season of onset, prior health events, and prior vaccination and/or medication did not affect the incidence of clostridial dermatitis. Development of clostridial dermatitis, flock type, season of placement, and season of onset of clostridial dermatitis affected livability. Breed did not affect livability. In a survey of 8 commercial turkey companies, 639 of 3,398 market turkey flocks (18.8%) had developed clostridial dermatitis, and 239 of 967 farms (24.7%) raising market turkeys had at least one flock develop clostridial dermatitis over the course of a calendar year, with an estimated increase in the cost of production for flocks that developed clostridial dermatitis of 0.031 to 5.5 cents per kilogram of meat produced. Key words: clostridial dermatitis, cellulitis, Clostridium, turkeys 2016 J. Appl. Poult. Res. 25:104–112 http://dx.doi.org/10.3382/japr/pfv065
DESCRIPTION OF PROBLEM Within the last 20 years the commercial turkey industry has experienced an increase in the frequency and severity of subcutaneous clostridial infections, and poultry veterinari1
Corresponding author: [email protected]
ans have ranked clostridial dermatitis as a top concern facing the turkey industry [1–4]. Clostridial dermatitis appears to be restricted to the commercial turkey industry; there have been no reports of this condition in wild, heritage breed, range-reared, or organic turkeys. Clostridial dermatitis, also referred to as cellulitis, is thought to be caused primarily by
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Primary Audience: Veterinarians, Live Production Managers, Flock Supervisors, Researchers
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The objectives of this study were to determine risk factors for occurrence of clostridial dermatitis in one commercial turkey operation and to evaluate incidence, disease management factors, and economic impact of clostridial dermatitis in commercial turkey operations across the United States.
MATERIALS AND METHODS Study 1: Regional Incidence and Risk Factors Production and health records were obtained from a commercial turkey company in the MidAtlantic region for 1,057 flocks placed on 167 farms between January 1, 2007, and December 31, 2007, for a retrospective analysis of incidence and risk factors for the development of clostridial dermatitis. Eight hundred eighteen flocks were light-hen flocks, which were processed at a median age of 13.1 wk (minimum 12.1; maximum 14.1) with an average weight of 7.1 ± 0.44 (mean ± standard deviation) kilograms at processing. One hundred eighty-one flocks were heavy-hen flocks, which were processed at a median age of 17.3 wk (minimum 16.3; maximum 18.4) with an average weight of 10.4 ± 0.52 kilograms. Fifty-eight flocks were identified as tom flocks, which were processed at a median age of 20.1 wk (minimum 15.1; maximum 21) with an average weight at processing of 18.5 ± 1.16 kilograms. Two hundred twenty-five flocks placed were Hybrid breed turkeys, 734 flocks were Nicholas (Aviagen Turkeys, Inc.) breed turkeys, and 96 flocks were composed of a mixture of Hybrid and Nicholas turkeys. Identification of flocks positive for clostridial dermatitis was based on visual confirmation of postmortem lesions consistent with clostridial dermatitis as determined by the flock supervisors and/or the company veterinarian. Health and production data were reviewed for each flock from the time of placement through the time of processing. Descriptive statistics were generated using JMP 8.0 software [13]. SAS 9.3 software was used to analyze risk factors for development of clostridial dermatitis by either Proc LOGISTIC or Proc FREQ [14]. Proc LOGISTIC was used to evaluate the effect of flock type, breed, stocking density, final weight at processing, prior
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Clostridium septicum [5, 6]. Clostridium perfringens and C. sordellii also may be involved [5–7]. For an individual bird to be considered a case of clostridial dermatitis based on the official definition developed by veterinarians and industry representatives, the bird must present with at least 2 of the following 7 signs: 1) subcutaneous emphysema; 2) subcutaneous serum and/or serosanguinous fluid; 3) vesicles on the skin, especially on the breast-inguinal area; 4) moist, dark, wrinkled skin, especially on the breast-inguinal area; 5) cellular necrosis (microscopic); 6) organ involvement (spleen and/or liver); and 7) vesicles on the skin, moist, dark, wrinkled skin, or both on the tail area [6]. A flock is diagnosed with clostridial dermatitis if the mortality with lesions characteristic of the disease is greater than or equal to 0.5 dead birds per 1,000 birds per d for 2 consecutive 24-hr periods [6]. Personal communications with flock supervisors and company veterinarians suggest that elevated mortality with characteristic necrotic lesions on the breast and inguinal regions is the main criterion used in the field to identify clostridial dermatitis-positive flocks. Histopathology and bacteriological isolation are generally not performed in routine diagnostics. The pathogenesis of clostridial dermatitis is not fully understood. It is hypothesized that the natural route of infection is via hematogenous spread of organisms invading or leaking from the gastrointestinal tract [6, 8]. While similarities exist between clostridial dermatitis of turkeys and gangrenous dermatitis of broiler chickens, the subcutaneous lesions of clostridial dermatitis are typically not accompanied by skin scratches and lesions seen in classic gangrenous dermatitis in broiler chickens. Some laboratories have reported success with experimental models to study clostridial dermatitis in turkeys by subcutaneous and intravenous injection of C. septicum [5, 9, 10]. However, it is thought that an oral challenge model would be better suited to study this disease since a gastrointestinal source of Clostridium species may be implicated in natural infections [9]. The limited success of oral challenge models in eliciting the disease has led some researchers to believe that the natural route of infection is through breaks or scratches in the skin [6, 9, 11, 12].
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Study 2: National Incidence and Economic Impact A 2-part survey was e-mailed to the member companies of the National Turkey Federation in March 2009. A first questionnaire was directed to the flock supervisors or servicepersons in each company and included questions on the incidence of clostridial dermatitis and aspects of disease management (Table 1). The second questionnaire was directed to the live production and/or complex managers to obtain information on the economic impact of clostridial dermatitis on their operation (Table 2). Questions pertained to turkey flocks marketed during the 2008 calendar year. Completed company responses were collected by the National Turkey Federation’s legal counsel. All identifying company information was removed and anonymized responses were sent to the authors for analysis.
RESULTS AND DISCUSSION Study 1: Regional Incidence and Risk Factors Fifty-three of 167 farms (31.7%) had at least one flock placed in 2007 that developed clostridial dermatitis, which affected 120 of 1057 placed flocks (11.4%; Table 3). Flock type affected the incidence of clostridial dermatitis (P < 0.0001). The incidence of clostridial der-
matitis was highest in tom flocks and lowest in light-hen flocks, as is generally reported by the industry [6]. The odds of tom flocks to develop clostridial dermatitis were 4.9 times the odds of light-hen flocks to develop the disease (95% confidence interval (CI): [2.7; 9.2]). The odds of heavy-hen flocks to develop cellulitis were 3.4 times the odds of light-hen flocks to develop the disease (95% CI: [2.2; 5.3]). Breed affected the incidence of clostridial dermatitis (P = 0.0216). Twenty-one of 225 (9.3%) Hybrid flocks, 95 of 734 (12.9%) Nicholas flocks, and 4 of 96 (4.2%) mixed flocks developed clostridial dermatitis. However, when flock type and breed were both included in a stepwise selection logistic regression model, only flock type remained significant (P < 0.0001). This corresponds to results from a 2010 USDA study evaluating risk factors for the development of clostridial dermatitis in which effect of breed also was found not significant [7]. Flock type was not evaluated in the USDA study. It has been reported that incidence and severity of cellulitis are worse in the summer and early fall [2, 7, 15]. In this study, season of placement was not associated with the occurrence of cellulitis (P = 0.2240; Table 4). No flocks placed in 2007 developed clostridial dermatitis in January through April 2007; however, this does not necessarily imply that no flocks developed clostridial dermatitis during those months since flocks placed in 2006 (which were not included in this study) may have developed clostridial dermatitis during that time period. Flocks placed in January 2007 would be outside the expected age range for onset of clostridial dermatitis in January and February 2007. Onset of clostridial dermatitis was associated with season (P = 0.0003; Table 5); few flocks, however, were truly at risk for developing clostridial dermatitis during winter 2007 since many of these flocks were younger than the expected age range for onset of clostridial dermatitis. When data for winter 2007 were omitted from the analysis, season was not associated with onset of disease (P = 0.7141). Results from this study do not show evidence for a seasonal effect on clostridial dermatitis incidence. The age at time of onset of clostridial dermatitis varied with flock type (P = 0.0018). For light-hen flocks the minimum, maximum,
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health events, and prior vaccination and/or medication on the development of clostridial dermatitis. Proc FREQ with Fisher’s exact was used to evaluate the effect of season of placement and season of onset on the development of clostridial dermatitis. Proc GLM was used to determine the factors affecting livability in a model containing development of clostridial dermatitis, flock type, breed, season of placement, and all 2-way interactions with development of clostridial dermatitis. Effect of season of onset on livability was evaluated in a separate model that included flock type, breed, season of onset, and all 2- and 3-way interactions. Interactions that were not significant were removed from the final models. Livabilities are reported as least square means ± standard error. The effect of a factor was determined to be significant at P < 0.05.
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Table 1. Questions included in survey distributed to flock supervisors/servicepersons within each member company of the National Turkey Federation. 1. In 2007, the National Turkey Federation developed a definition of clostridial dermatitis that included the signs and criteria listed below. What signs or criteria have you or would you have used in 2008 to determine that turkeys in flocks that you supervised had clostridial dermatitis? (please check all that apply) Subcutaneous emphysema (air-bubbles under the skin) Serum/serosanguineous subcutaneous fluid (fluid accumulation under the skin) Vesicles (blisters) on the skin, especially in the breast/inguinal area Moist, dark, wrinkled skin, especially in the breast/inguinal area Cellular necrosis (microscopic) Organ involvement (spleen/liver) Vesicles on the skin, and/or moist, dark, wrinkled skin in the tail area Clostridium septicum, C. perfringens type A, or C. sordelli isolated from fluid or affected skin/tissue samples of affected/dead birds Elevated mortality Other
For the following questions, please provide YOUR own opinion or knowledge derived from YOUR experience as a turkey flock supervisor/serviceperson. 8. What are your thoughts concerning the causes of and risk factors for clostridial dermatitis in turkeys? (Please rank in order of importance.) 9. What do you think are the best management/treatment options for flocks with clostridial dermatitis? (Please rank in order of importance.) 10. What do you think are the best options to prevent flocks from developing clostridial dermatitis? (Please rank in order of importance.)
and average (mean ± standard deviation) ages at time of onset were 8, 14, and 11.2 ± 1.12 wk; for heavy-hen flocks 4, 17, and 13.0 ± 2.97 wk; for tom flocks 7, 19, and 13.1 ± 3.40 wk. Historically, clostridial dermatitis lesions have
typically been seen in older birds near the time of market. Onset of the disease generally occurs between 13 and 18 wk of age, with the youngest age of onset reported to be 6 wk of age [2, 6, 9, 15]. Earlier age of onset observed in this
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For the following questions, please consider only those flocks that you supervised and which were marketed during the 2008 calendar year (January 1, 2008 – December 31, 2008). 2. How many FARMS did you supervise that had flocks marketed during 2008? 2a. What was the sum total of houses on these farms? 3. What is the average flock size for those flock types which you supervise? If you do not supervise a particular flock type, please write N/A. 3a. Average flock size (# of birds) for light hens 3b. Average flock size (# of birds) for heavy hens 3c. Average flock size (# of birds) for light toms 3d. Average flock size (# of birds) for heavy toms 4. How many FLOCKS under your supervision were marketed during the 2008 calendar year? 4a. Number of light hen flocks 4b. Number of heavy hen flocks 4c. Number of light tom flocks 4d. Number of heavy tom flocks 5. How many FARMS supervised by you had at least one flock marketed in 2008 that at some point during production had signs which you considered compatible with clostridial dermatitis? 6. How many FLOCKS supervised by you and marketed during the 2008 calendar year had signs that you considered compatible with clostridial dermatitis? 6a. Number of light hen flocks that had clostridial dermatitis 6b. Number of heavy hen flocks that had clostridial dermatitis 6c. Number of light tom flocks that had clostridial dermatitis 6d. Number of heavy tom flocks that had clostridial dermatitis 7. What was the average% livability for FLOCKS that developed clostridial dermatitis? 7a. Average% livability for light hen flocks with clostridial dermatitis 7b. Average% livability for heavy hen flocks with clostridial dermatitis 7c. Average% livability for light tom flocks with clostridial dermatitis 7d. Average% livability for heavy tom flocks with clostridial dermatitis
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Table 2. Questionnaire distributed to each live production/complex manager within each member company of the National Turkey Federation. 1. For flocks marketed during the 2008 calendar year, was there a difference in the live production costs between flocks that had clostridial dermatitis and flocks that did not have clostridial dermatitis? (yes or no) 2. If you answered yes to the previous question, please calculate the difference in average live production costs between flocks that had clostridial dermatitis and flocks that did not have clostridial dermatitis? (cents/lb)
Table 3. Incidence of clostridial dermatitis in flocks of one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). N
206 8 11 225
Hybrid NCD 2 16 2 3 21
%CD
3
N
7.8 25.0 27.3 9.3
522 165 47 734
Nicholas NCD %CD 45 36 14 95
8.6 21.8 29.8 12.9
N 88 8 0 96
Mixed NCD 2 2 0 4
%CD
N
2.3 25.0 n/a 4.2
8184 181 58 1057
All Breeds6 NCD %CD 63 40 17 120
7.7 22.1 29.3 11.4
1
Number of flocks. Number of flocks with clostridial dermatitis. 3 Percent of flocks with clostridial dermatitis. 4 The total number of light-hen flocks includes 2 flocks for which breed was not identified. 5 Flock type associated with incidence of clostridial dermatitis in univariate (P < 0.0001) and multivariate analysis (P < 0.0001). 6 Breed associated with incidence of clostridial dermatitis in univariate analysis (P = 0.0216). 2
Table 4. Incidence of clostridial dermatitis in flocks placed for grow-out in a particular season for farms from one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). Season of placement1
Total number of flocks placed
Number (percent) of flocks that developed clostridial dermatitis
Winter 2007 Spring 2007 Summer 2007 Fall 2007
195 298 314 250
28 (14.4) 38 (12.6) 32 (10.2) 22 (8.8)
1
Winter 2007 includes flocks placed in January, February, and March; spring 2007 includes flocks placed in April, May, and June; summer 2007 includes flocks placed in July, August, and September 2007; fall 2007 includes flocks placed in October, November, and December 2007.
study may be due to increased awareness of flock supervisors/veterinarians and a better ability to detect early signs of the disease. Given that weight at processing is dependent on flock type, the effect of average weight at time of processing was analyzed for each flock type separately (Table 6). For each additional kilogram of weight at time of processing, heavy hens were 3.92 times more likely to develop clostridial dermatitis (P = 0.0003). Weight at processing did not affect the odds of developing clostridial dermatitis in light hens (P = 0.6285) and toms (P = 0.8262). For light-hen flocks the minimum, maximum, and average (mean ± standard deviation) bird densities at time of placement were 2.2, 16.1, and
4.4 ± 1.33 birds per square meter; for heavy-hen flocks 1.3, 6.7, and 3.3 ± 0.49 birds per square meter; and for tom flocks 2.2, 4.2, and 2.7 ± 0.30 birds per square meter. Bird density had a limited effect on the incidence of clostridial dermatitis. Given that the amount of floor space allotted per bird varies with flock type, the analysis also was conducted for flocks within each flock type. Bird density was not associated with clostridial dermatitis in light hens (P = 0. 7026) or heavy hens (P = 0.8071); but there was a tendency in toms flocks that for every additional bird per square meter of floor space at time of placement tom flocks were 7.8 times more likely to develop clostridial dermatitis (P = 0.0772). Stocking density is also commonly reported in weight
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Light hens Heavy hens Toms All flocks5
1
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Table 5. Season of onset of clostridial dermatitis in turkey grow-out flocks placed in 2007 for farms of one commercial turkey company in the Mid-Atlantic region based on retrospective analysis of mortality and health reports (Study 1). Season of clostridial dermatitis onset1
Number of flocks present in a given season
Number (percent) of flocks developing clostridial dermatitis
Winter 2007 Spring 2007 Summer 2007 Fall 2007 Winter 2008
197 493 644 588 281
0 (0) 30 (6.1) 41 (6.4) 30 (5.1) 19 (6.8)
1 Winter 2007 includes flocks present in January, February, or March 2007; spring 2007 includes flocks present in April, May, or June 2007; summer 2007 includes flocks present in July, August, or September 2007; fall 2007 includes flocks present in October, November, or December 2007; winter 2008 includes flocks present in January, February, or March 2008.
Factor
Category
Odds ratio
95% Confidence interval
P-value
Weight at processing
Tom Heavy hen Light hen
0.948 3.921 1.155
[0.588; 1.529] [1.875; 8.199] [0.643; 2.075]
0.8262 0.0003 0.6285
Stocking density (birds)2
Tom Heavy hen Light hen
7.836 0.912 0.960
[0.799; 76.888] [0.437; 1.905] [0.779; 1.183]
0.0772 0.8071 0.7026
1
1 2
Live weight, in kilograms. Stocking density, in birds per square meter of floor space.
per unit area. When the analysis was conducted for weight in kilograms at time of processing per square meter of floor space, stocking density affected the incidence of clostridial dermatitis (P = 0.0032). For each additional kilogram of weight per square meter of floor space flocks were 1.025 (95% CI: [1.008; 1.041]) times more likely to develop clostridial dermatitis. This is consistent with other reports that associate increased stocking density with an increased incidence of clostridial dermatitis [6, 11] although stocking density by weight did not affect any of the individual flock types (P > 0.10) in this study. As C. septicum and C. perfringens are normal inhabitants of the turkey’s gastrointestinal tract, overgrowth of the organism and/or suppression of the bird’s immune system are thought to play important roles in the development of clostridial dermatitis. Maintenance of good intestinal health has been implicated as an important factor in preventing clostridial dermatitis [6, 8]. However, no association was found between prior health events and development of clostridial dermatitis (P = 0.9595); in particu-
lar, the presence of a prior enteric disease event had no impact on the incidence of clostridial dermatitis in this study (P = 0.9771). Prior leg issues, including conformational problems and synovitis, were not associated with an increased incidence of clostridial dermatitis (P = 0.9192). Administration of medications or vaccinations also had no effect on the incidence of clostridial dermatitis (P = 0.8306). Livability is defined as the percentage of birds placed that survive to the time of processing (percent livability = 100 - percent mortality). Livability was 88.8 ± 0.28% for all flocks without clostridial dermatitis and 87.8 ± 0.44% for all flocks that developed clostridial dermatitis (P = 0.0144). In the USDA 2010 study, average livability was reported to be between 89.3 and 89.9% for flocks without clostridial dermatitis and 83 to 85.8% for flocks with clostridial dermatitis [7]. Mortality risk associated with clostridial dermatitis has been reported as high as one to 2% per wk [7, 9]. Livability was 92.3 ± 0.26% in light-hen flocks, 90.4 ± 0.39% in heavy-hen flocks, and 82.2 ± 0.60% in tom flocks (P < 0.0001). Birds placed in spring 2007
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Table 6. Factors affecting incidence of clostridial dermatitis on farms of one commercial turkey company in the Mid-Atlantic region based on retrospective evaluation of mortality and health reports and univariate analysis of individual risk categories (Study 1).
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Table 7. Reports of clostridial dermatitis for commercial turkeys marketed during 2008 based on a national survey (Study 2).
Companies Farms Flocks Light hens Heavy hens Light toms Heavy toms 1
Total number
Number with clostridial dermatitis
Percent with clostridial dermatitis
8 967 3398 573 211 148 2466
6 2391 639 0 10 11 618
75 24.7 18.8 0 4.7 7.4 25.1
Farms with at least one flock marketed during 2008 that developed clostridial dermatitis.
Study 2: National Incidence and Economic Impact Incidence Thirty-nine flock supervisors/company veterinarians representing 8 turkey companies completed the questionnaire on incidence and disease management of flocks marketed in 2008 (Table 7). Clostridial dermatitis was reported on close to 25% of turkey farms in this questionnaire. In a 2010 USDA study of 15 turkey companies across the United States,
42.3% of turkey farms were reported to have at least a slight problem with clostridial dermatitis during the 12 months preceding the study [7]. In the 2007 regional study, Study 1, 7.7% of light-hen flocks developed clostridial dermatitis while no light-hen flocks were affected in Study 2. In Study 2, the national incidence of clostridial dermatitis in heavy-hen flocks was much lower than the incidence in Study 1, 4.7 versus 22.1%, respectively. Incidences of clostridial dermatitis in heavy-tom flocks were similar in Study 1 (29.3%) and Study 2 (25.1%). No comparison can be made for light-tom flocks as the company involved in Study 1 does not raise that type of bird. Livabilities for flocks with clostridial dermatitis ranged from 87 to 96% for heavy-hen flocks, 88 to 95% for light-tom flocks, and 80 to 92% for heavy-tom flocks. The livabilities obtained for heavy hens and toms in Study 1 fall within these ranges. Flock supervisors also were asked to identify the criteria of the official case definition for clostridial dermatitis they actually use in identifying flocks with clostridial dermatitis (Table 8). Nearly all respondents relied on the presence of subcutaneous emphysema (n = 37), serum/serosanguineous subcutaneous fluid (n = 38), and elevated flock mortality (n = 36) in identification of flocks with clostridial dermatitis. Twenty-seven respondents (69.2%) routinely relied on culture of C. septicum, C. perfringens type A, or C. sordelli from affected birds, and only 22 (56.4%) relied on the presence of spleen and liver lesions. Only 5 respondents (12.8%) took samples for histopathology to identify the presence of cellular necrosis at the microscopic level. These results suggest that flock supervisors rely most heavily on gross pathology
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had a livability of 89.3 ± 0.37%, 89.0 ± 0.39% in winter 2007, 88.7 ± 0.36% in summer 2007, and 86.2 ± 0.40% in fall 2007 (P < 0.0001). The effect of season of placement on livability may reflect the impact of environmental factors on mortality during the crucial brooding period. There was no effect of breed on livability (P = 0.3118) and all 2-way interactions with clostridial dermatitis were not significant and therefore not included in the final model. Livability was 92.0 ± 1.02% for light-hen flocks with clostridial dermatitis, 89.0 ± 1.14% for heavy-hen flocks with clostridial dermatitis, and 81.1 ± 1.50% for tom flocks with clostridial dermatitis (P < 0.0001). Livability of flocks that developed clostridial dermatitis in spring 2007 was 89.1 ± 1.27%, 88.4 ± 1.20% in summer 2007, 87.1 ± 1.28% in fall 2007, and 84.9 ± 1.37% in winter 2008 (P = 0.0264). Decreased livability for flocks that developed clostridial dermatitis in fall 2007 and winter 2008 is in contrast to the 2010 USDA study, which reported an increased severity (increased mortality associated with clostridial dermatitis) during the summer and fall months [7]. There was no breed effect on livability of flocks with clostridial dermatitis (P = 0.9093).
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Table 8. Criteria used in identification of clostridial dermatitis-positive flocks in 2008 based on a national survey of flock supervisors (Study 2). Responses from 39 flock supervisors representing 8 companies. Number (percent) of respondents using the criterion
Criterion Subcutaneous emphysema (air bubbles under the skin) Serum/serosanguineous subcutaneous fluid (fluid accumulation under the skin) Vesicles (blisters) on the skin, especially in the breast/inguinal area Moist, dark, wrinkled skin, especially in the breast/inguinal area Cellular necrosis (microscopic) Organ involvement (spleen/liver) Vesicles on the skin, and/or moist, dark, wrinkled skin in the tail area C. septicum, C. perfringens type A, or C. sordelli isolated from fluid or affected skin/tissue samples of affected/dead birds Elevated mortality
36 (92.3)
Table 9. Increase in cost of production associated with development of clostridial dermatitis in commercial turkeys marketed in 2008 based on a national survey (Study 2). Survey code
Company code
Increase in cost of production (cents/kilogram)
EI-1
3
EI-1
3
EI-2 EI-3 EI-4 EI-5 EI-6 EI-7 EI-8
4 5 6 6a 7 8 9
N/A (no cases of clostridial dermatitis) N/A (no cases of clostridial dermatitis) 1.1 2.2 5.5 4.6 0.79 0.031 (toms), 0.037 (hens) N/A (no cases of clostridial dermatitis)
clude: increased mortality pick-up (at least 2 to 3 times per day), administration of penicillin and/or lincomycin via water, full clean-out after every flock, and management to keep litter dry. Prevention strategies include: frequent mortality removal, full clean-out after every flock, maintenance of dry litter conditions, increased down time between flocks, and the use of preventive antibiotics/iodine in the water. These responses are in line with previously published recommendations [6, 7]. Economic impact Seven companies returned the questionnaire on economic impact (Table 9). Two of the 7 companies reported no cases of clostridial dermatitis in turkey flocks marketed during the 2008 calendar year. The average wholesale price for turkeys produced in the United States in 2008 was 124.6 cents per kilogram [17]. Development of clostridial
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findings and mortality when diagnosing flocks with clostridial dermatitis. Flock supervisors were asked to provide their thoughts on the causes and risk factors for the development of clostridial dermatitis, management/treatment options, and prevention strategies for the control of clostridial dermatitis in commercial turkey operations based on their own personal experiences. The most common responses regarding the cause and risk factors for development of clostridial dermatitis included: infrequent mortality removal, wet litter conditions, presence of built-up litter in the house, and stress. While it is commonly reported that increased frequency of mortality removal reduces the incidence and/or severity of clostridial dermatitis [6], the frequency of mortality removal was not associated with the disease status of turkey farms in the 2010 USDA study [7]. In the United States, turkey houses (finishing units) are often not cleaned out between flocks to keep costs down. The use of built-up litter in turkey houses has been implicated in the development of clostridial dermatitis as this practice allows for the accumulation of clostridial spores in the environment [6, 16]. Wet litter, resulting from water spills in the turkey house or from turkeys experiencing diuresis or diarrhea, has been associated with an increased incidence of clostridial dermatitis as it favors the proliferation of Clostridium species in the environment [6, 11]. Dexamethasone treatment, in the absence of C. septicum or C. perfringens challenge, results in the development of clostridial dermatitis, which suggests that stress may be a factor in the development of this disease [11]. Management and treatment options recommended by survey respondents in-
37 (94.9) 38 (97.4) 32 (82.0) 32 (82.0) 5 (12.8) 22 (56.4) 32 (82.0) 27 (69.2)
JAPR: Field Report
112 dermatitis increased the cost of production for market turkey flocks by 0.031 to 5.5 cents per kilogram for the 5 companies that reported cases of clostridial dermatitis.
CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES 1. Rives, D., D. Mills, and S. Clark. 2006. Current health and industry issues facing the turkey industry. Report of the Committee on Transmissible Diseases of Poultry and Other Avian Species. Minneapolis, MN. 2. Carr, D., D. Shaw, D. Halvorson, B. Rings, and D. Roepke. 1996. Excessive mortality in market-age turkeys associated with cellulitis. Avian Diseases. 40:736–741.
Acknowledgments The authors are grateful for the cooperation of the National Turkey Federation and the numerous turkey companies that participated in the regional and national studies. Funding for this study was provided by Cargill Turkey Products, LLC, Harrisonburg, VA, and the Virginia Poultry Growers Cooperative, Hinton, VA.
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1. Flock type, breed, weight at time of processing, and stocking density affected the incidence of clostridial dermatitis. 2. Season of placement, season of onset, prior health events, and prior vaccinations and/or medications did not affect the incidence of clostridial dermatitis. 3. Livability was affected by development of clostridial dermatitis, flock type, season of placement, and season of onset but not by breed. 4. The incidence of clostridial dermatitis was lowest in light-hen flocks and highest in heavy-tom flocks in both studies. 5. The development of clostridial dermatitis increased the cost of production for market turkey flocks by 0.031 to 5.5 cents per kilogram. 6. When practical, producers should consider modifying the flock type, breed, stocking density, target BW, and timing of placement in order to minimize the incidence and/or severity of clostridial dermatitis. 7. Statistical analysis and development of a predictive model for which flocks are likely to develop clostridial dermatitis is constrained by the complex interactions between host, pathogen, and environmental factors that contribute to the development of this disease.
3. Fenstermacher, R., and B. Pomeroy. 1939. Clostridium infection in turkeys. Cornell Veterinary Journal. 29:25– 28. 4. Clark, S., B. Tilley, and D. Mills. 2009. Current health and industry issues facing the turkey industry. Pages 530–535 in Proc. 112th Annual Meeting of the USAHA, Greensboro, NC. Richardson Printing, Kansas City, MO. 5. Tellez, G., N. Pumford, M. Morgan, A. Wolfenden, and B. Hargis. 2009. Evidence for Clostridium septicum as a primary cause of cellulitis in commercial turkeys. Journal of Veterinary Diagnostic Investigation. 21:374–377. 6. Clark, S., R. Porter, B. McComb, R. Lippert, S. Olson, S. Nohner, and H. Shivaprasad. 2010. Clostridial dermatitis and cellulitis: an emerging disease of turkeys. Avian Diseases. 54:788–794. 7. USDA. 2012. Poultry 2010: Clostridial dermatitis on US turkey-grower farms. USDA-APHIS-VS-CEAHNAHMS. 8. Dibner, J. J. 2008. The role of gut barrier failure in gangrenous cellulitis of poultry. Page 20 in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis, Bllomington, MN. 9. Thachil, A., B. McComb, M. Anderson, D. Shaw, D. Halvorson, and K. Nagaraja. 2010. Role of Clostridium perfringens and Clostridium septicum in causing turkey cellulitis. Avian Diseases. 54:795–801. 10. Nagaraja, K., A. Thachil, and D. Halvorson. 2009. Role of Clostridium perfringens and septicum in cellulitis in turkeys. Page 10 in 58th Western Poultry Disease Conference Madison, WI. 11. Huff, G. R., W. E. Huff, and N. C. Rath. 2013. Dexamethasone immunosuppression resulting in turkey clostridial dermatitis: a retrospective analysis of seven studies, 1998– 2009. Avian Dis. 57:730–736. 12. Shivaprasad, H. 2008. Gangrenous dermatitis due to Clostridium septicum in turkeys. in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis Bloomington, MN. 13. JMP. 2008. Version 8. SAS Institute Inc., Cary, NC. 14. SAS User’s Guide. 2010. Version 9.3. SAS Inst. Inc., Cary, NC. 15. McComb, B. 2008. Upper midwest filed perspective of dermatitis in commercial turkeys. Pages 5–8 in MTRPC Gold Medal Panel on [cellulitis] clostridial dermatitis, Bloomington, MN. 16. Thachil, A., B. McComb, M. Kromm, and K. Nagaraja. 2013. Vaccination of turkeys with Clostridium septicum bacterin-toxoid: evaluation of protection against clostridial dermatitis. Avian Dis. 57:214–219. 17. USDA. 2010. Poultry - Production and value, 2009 summary. National Agricultural Statistic Service.