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Abstract

Gangrenous dermatitis (GD) is a disease of chickens and turkeys that causes severe economic losses in the poultry industry worldwide. Clostridium septicum, Clostridium perfringens type A, and occasionally Clostridium sordellii are considered the main causes of GD, although Staphylococcus aureus and other aerobic bacteria may also be involved in some cases of the disease. GD has become one of the most significant diseases of commercial turkeys in the United States. Several infectious and/or environmental immunosuppressive factors can predispose to GD. Skin lesions are considered to be the main portal of entry of the microorganism(s) involved. GD is characterized by acute onset of mortality associated with gross skin and subcutaneous tissue lesions consisting of variable amounts of serosanguineous exudate together with emphysema and hemorrhages. The underlying skeletal muscle can also be involved. Ulceration of the epidermis may be also noticed in cases complicated with S. aureus. Microscopically, necrosis of the epidermis and dermis, and subcutaneous edema and emphysema are commonly observed. Gram-positive rods can be identified within the subcutis and skeletal muscles, usually associated with minimal inflammatory infiltrate. A presumptive diagnosis of GD can be made based on history, clinical signs, and gross anatomic and microscopic lesions. However, confirmation should be based on demonstration of the causative agents by culture, PCR, immunohistochemistry, and/or fluorescent antibody tests.

Keywords

Chickens gangrenous dermatitis turkeys

Introduction

Gangrenous dermatitis (GD) is a disease that affects primarily commercial broiler chickens and turkeys, and it is responsible for severe economic losses in the poultry industry worldwide.⁴² The disease is also called blue wing disease in chickens and cellulitis in turkeys. The condition is characterized by congestion, hemorrhage, and necrosis of the skin and subcutaneous tissue, associated with edema and/or emphysema, which sometimes extends into the underlying musculature. The most significantly affected areas include breast, back, abdomen, thighs, tail and wings (USDA-APHIS, 2011, Clostridial dermatitis in U.S. commercial broilers and turkeys, https://goo.gl/Xnirdc).^10,53,68,73

GD is primarily caused by Clostridium septicum and Clostridium perfringens type A, acting singly or in combination (Table 1).^{8,53,68,71,73} However, cases of GD may also be caused by a myriad of anaerobic and aerobic bacteria including Clostridium sordellii, Clostridium novyi, Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus xylosus, Escherichia coli, Enterococcus faecalis, Pasteurella multocida, Gallibacterium anatis biovar haemolytica, Proteus spp., Pseudomonas aeruginosa, Bacillus spp., and Erysipelothrix rhusiopathiae (Table 1; Andrada M, et al. Dermatitis gangrenosa en pollos de engorde: caso clínico [Gangrenous dermatitis in broilers: a clinical case]. Proc XVIII Reunión de la Sociedad Española de Anatomía Patológica Veterinaria; 2006 Jun 28–30; Rabat, Morocco. Spanish, https://goo.gl/DwKifa; https://goo.gl/Xnirdc).^{1,9,10,17,53,55,56,67,68,73}

Table 1.

Anaerobic and aerobic bacterial species involved in gangrenous dermatitis of chickens and turkeys.

Organism involved	Chickens	Turkeys
Clostridium septicum	FI	FI
Clostridium perfringens type A	FI	FI
Clostridium sordellii	II	II
Clostridium novyi	II	ND
Staphylococcus aureus	II	II
Staphylococcus xylosus	II	ND
Staphylococcus epidermidis	II	ND
Escherichia coli	II	II
Pasteurella multocida	ND	II
Pseudomonas aeruginosa	II	II
Enterococcus faecalis	II	II
Proteus spp.	II	II
Bacillus spp.	II	II
Erysipelothrix rhusiopathiae	II	II
Gallibacterium anatis var. haemolytica	II	II

FI = frequently isolated; II = infrequently isolated; ND = no data available.

Although GD has been recognized for many years as a sporadic disease,⁷³ the prevalence and severity of this condition has increased over the past two decades in the United States and elsewhere. GD is currently considered one of the 3 most significant diseases of commercial turkeys in the US (USDA-APHIS, 2012, Role of intestinal pathology and clostridial species in clostridial dermatitis on U.S. turkey-grower farms, https://goo.gl/tiuETr), and it was listed among the most frequently diagnosed diseases in commercial broiler chickens in California in January 2010–December 2012 (Carnaccini S, et al. Summary of diseases diagnosed in broiler chickens submitted to the California Animal Health and Food Safety Laboratory System, 2010–2012. Proc 62nd West Poult Dis Conf; 2013 Mar 25–27; Sacramento, CA, https://goo.gl/vg4Xwf).

GD was first reported in the United States in the early 1930s⁴⁸; Clostridium welchii (now C. perfringens) was isolated from heart blood and liver of 2 chickens. The disease was reproduced experimentally in chickens by intramuscular inoculation of this isolate, causing severe necrosis of the skeletal muscles and subcutaneous tissue.⁴⁸ Later, GD was diagnosed in chickens suffering heavy mortality. C. welchii, C. septicum, and C. novyi were isolated from the tissues of the dead birds.¹³

GD has received different names over the years, including necrotic dermatitis, gangrenous cellulitis, gangrenous dermatomyositis, spontaneous clostridial myonecrosis, poultry gangrene, avian malignant edema, gas edema disease, subcutaneous emphysema, tailitis, blue wing disease, and wing rot.^{32,35,53,68,73} However, as of 2017, gangrenous dermatitis is the preferred and most widely used name (https://goo.gl/Xnirdc; https://goo.gl/tiuETr).^10,35

Etiology

Clostridia

Genus Clostridium, which belongs to phylum Firmicutes, class Clostridia, order Clostridiales, family Clostridiaceae,⁵⁹ is composed of anaerobic, mostly gram-positive, spore-forming rods.^12,53,59

C. perfringens type A is the most frequently reported toxinotype of this bacterial species involved in GD outbreaks.^53,68 All type A isolates produce alpha toxin (CPA); some strains may also produce one or more additional toxins including necrotic enteritis B–like toxin (NetB) and enterotoxin (CPE).⁵⁸ The phylogenetic relation of 139 C. perfringens strains isolated from chickens and turkeys with necrotic enteritis or GD was studied by multilocus sequence typing (MST).³² The study demonstrated that GD-associated C. perfringens isolates are significantly different from isolates obtained from cases of necrotic enteritis.³² The role of specific toxins in the pathogenesis of GD is still unknown, although CPA has been suggested to play the most critical role.⁶⁸

The main virulence factor of C. septicum is alpha toxin (ATX), a necrotizing pore-forming toxin (PFT), which is unrelated to the alpha toxin of C. perfringens. ATX induces increased membrane permeability, which leads to cell necrosis. C. septicum also produces septicolysin, another PFT, which is thought to have a synergistic effect with ATX in the pathogenesis of gas gangrene lesions.⁵⁷ C. septicum isolates (n = 109) obtained from turkeys and chickens with GD were analyzed by MST. Most of the C. septicum isolates belonged to a predominant clonal population composed of 2 clusters with little genetic diversity.⁴⁷ Based on this finding, it has been hypothesized that only certain strains of C. septicum are implicated in cases of GD in poultry. Several authors have suggested that ATX plays a critical role in the pathogenesis of GD.^10,53,68 This is supported by the ATX effect on endothelial cells, causing fluid extravasation, and the possible synergistic effect that septicolysin has with ATX.⁵⁷

C. sordellii produces 2 main toxins, namely lethal toxin (TcsL) and hemorrhagic toxin (TcsH); both of which are glycosylating. In addition, most strains of this microorganism produce sordellilysin, phospholipase, neuraminidase, and collagenase.⁵⁷ No information is currently available on the role that any of the C. sordellii toxins have in the pathogenesis of GD.

Staphylococcus spp

Genus Staphylococcus is composed of gram-positive, coccoid-shaped, aerobic bacteria, which are commonly seen as clusters when grown in solid media and short chains when cultured in liquid media.² S. aureus is the most common non-clostridial bacterial species associated with GD.² This microorganism is able to cause GD alone or in combination with one or more clostridial species. Other species of this genus that have been found in outbreaks of GD in broiler chickens include S. xylosus and S. epidermidis (Andrada M, et al. Dermatitis gangrenosa en pollos de engorde: caso clínico [Gangrenous dermatitis in broilers]. Proc XVIII Reunión de la Sociedad Española de Anatomía Patológica Veterinaria; 2006 Jun 28–30; Rabat, Morocco. Spanish).⁷³ However, these microorganisms can also be found in skin and nares of healthy chickens, and isolation from chickens with GD does not necessarily confirm a causative role in this disease.² S. aureus can produce several toxins, including hyaluronidase, deoxyribonuclease, fibrinolysin, lipase, protease, leucocidin, hemolysins, epidermolytic toxin, and dermonecrotic toxin.³¹ Following intradermal inoculation in poultry and rabbits,⁹ dermonecrotic toxin induced severe dermal inflammation and skin necrosis at the injection site, which supports a possible role of this toxin in the pathogenesis of GD.

Other aerobic bacteria

E. coli isolates obtained from cases of cellulitis, swollen head syndrome, and colisepticemia in chickens produce a vacuolating cytotoxin. This toxin is specific for avian cells and appears to be similar to the one produced by Helicobacter pylori.⁶⁴ The role of this toxin in cases of GD is unknown. Serogroup D P. multocida have been associated with dermal lesions in poultry with GD. Strains containing a heat-labile protein have been isolated from turkeys. Dermal inoculation of sonicated suspensions of these strains produced necrotic lesions in turkey skin.^61,62 Facial cellulitis associated with P. multocida in turkeys has also been described.³⁷ P. aeruginosa is characterized by a wide virulence repertoire, including extracellular and cellular components. Most strains produce exotoxin A, responsible for tissue necrosis with a mechanism similar to that of diphtheria toxin.¹¹,¹⁹ The most important virulence factor of E. rhusiopathiae is a neuraminidase that promotes adhesion and spreading of the pathogen.⁷⁴ Whether this toxin plays a role in the pathogenesis of GD is not known.

Pathogenesis

The proposed pathogenesis of GD in chickens and turkeys is summarized in Figures 1 and 2, respectively. Several authors suggested that immunosuppression may be the key predisposing factor for GD in chickens and turkeys.^{10,33,53,68,73} A retrospective study of GD in broiler chickens, including cases that occurred in 1995–2006 in Alabama, described severe lymphocytic depletion of the thymus and bursa of Fabricius, associated with the onset of GD (Hoerr F. Case reports from Alabama. Proc 56th West Poult Dis Conf; 2007 Mar 26–29; Las Vegas, NV, https://goo.gl/vg4Xwf). Experimentally, intramuscular administration of dexamethasone successfully predisposed to the development of GD after subcutaneous challenge with C. septicum or C. perfringens in turkey poults.⁷²

Figure 1.

Proposed pathogenesis of gangrenous dermatitis in chickens.

Figure 2.

Proposed pathogenesis of gangrenous dermatitis in turkeys.

Under natural conditions, immunosuppression can be triggered by a wide range of infectious and environmental factors in both chickens and turkeys.^{10,33,53,68,73} Immunosuppressive viral agents that may predispose to GD in chickens and turkeys include Marek’s disease virus, infectious bursal disease virus, chicken anemia virus, several reoviruses, and reticuloendotheliosis virus.^{10,20,33,34,53,67,68,73} Other viral infectious agents such as inclusion body hepatitis virus^53,73 in chickens and hemorrhagic enteritis virus in turkeys have also been suggested as possible immunosuppressive agents that may trigger GD.^10,33

Environmental factors that can predispose chickens and turkeys to GD^10,33,53 are: 1) traumatic lesions of the skin associated with cannibalism and/or fighting (the latter being more common in turkeys); overcrowding; feed outages; deficient diets; and 2) wet and poor litter conditions; contaminated feed, water, equipment, and vaccines; high ammonia levels; and mycotoxins (e.g., aflatoxins, trichothecenes, fumonisins, and ochratoxins) in feed.^{10,16,33,44,53,68}

In broiler chickens, GD is mainly predisposed to by traumatic damage of the skin, usually associated with cannibalism and overcrowding. Such skin lesions provide a port of entry for bacteria.^49,53,65,75 However, GD was also reported, albeit infrequently, in heavy broiler chickens with grossly intact skin. In those cases, the predisposing factor was considered to be anaerobiosis generated by subcutaneous tissue necrosis associated with trauma of the pectoral region, as a result of prolonged ventral recumbency. Chaotic multiplication of the intestinal flora followed by absorption into the bloodstream promoted bacteremia, which was thought to be the origin of some of the GD lesions.^34,66 There is anecdotal evidence of a similar pathogenesis of GD in broiler chickens as a result of the use of ionophores in the feed associated with toxic muscle damage (authors’ unpublished observations).

The pathogenesis of GD in turkeys is not fully understood.^10,43,68 As of 2017, 2 models are being investigated in this species. The first model is the so-called “inside-out” model, which considers that the first step in pathogenesis is intestinal overgrowth and/or loss of integrity of the intestinal mucosa allowing the clostridia responsible for GD to reach the bloodstream. These organisms then reach the muscle and subcutaneous tissue hematogenously (https://goo.gl/tiuETr).^10,43 Transmission of these microorganisms from one animal to another would occur via the orofecal route. The second model, the so-called “outside-in” model, resembles the pathogenesis of GD in chickens, and suggests the entry of microorganisms into the subcutaneous tissue through moist or damaged skin.^10,68

Several experimental challenge models have been used to clarify the role of C. septicum, C. perfringens, and S. aureus in the pathogenesis of GD.^70,71,76 Four-wk-old broiler chickens were inoculated simultaneously by subcutaneous and intramuscular routes with C. septicum and/or S. aureus; mortality rates were much higher in chickens challenged with both microorganisms than in those inoculated with either isolate separately.⁷⁶ GD lesions and death were reproduced in 10-wk-old breeder turkeys by intravenous administration of C. septicum or C. perfringens (untyped). Three- and 7-wk-old turkeys were challenged subcutaneously with C. septicum and C. perfringens type A, separately or in combination.⁷¹ Although both C. perfringens and C. septicum caused cellulitis and mortality when inoculated combined or separately, C. septicum was found to be more effective than C. perfringens in causing cellulitis and mortality.⁷¹ Oral challenge with either C. septicum or C. perfringens showed only limited success reproducing GD, supporting the idea that skin lacerations are the main port of entry for most or all of the microorganisms involved in GD.⁴³

Epidemiology and clinical signs

GD has been described in chickens in several countries, including Argentina,⁷ Australia,⁵,⁶⁰ Bulgaria,¹⁶ Egypt,⁴ Hungary,³⁶ India,³⁹ Japan,⁶⁶ New Zealand,⁴⁴ Nigeria,⁵¹ Spain (Andrada M, et al. Gangrenous dermatitis in broilers; a clinical case), United Kingdom,²² and the United States (https://goo.gl/Xnirdc; https://goo.gl/vg4Xwf).^{23,30,33,34,42,65,75,77} In turkeys, GD has been reported only in the United States (https://goo.gl/Xnirdc)^8,43

GD is commonly observed in close-to-market age (>35 d) broiler chickens and turkeys (>13–16 wk).⁶⁸ GD has been associated with increased condemnation rates and downgrading of chicken and turkey carcasses at slaughter.⁶⁸ Affected flocks typically show daily mortality ranging from a few birds to 3%.⁶⁸ However, mortality of up to 60% was reported in some flocks.^53,68

The disease can occur without clinical signs being observed. However, high fever, depression, anorexia, ataxia, leg weakness, and lateral recumbency are usually seen in both chickens and turkeys.⁶⁸ The lower abdomen and inner thighs are frequently affected by the accumulation of subcutaneous edema.⁶⁸ The skin over affected areas is usually featherless and can show dark-red, purple, green, or green-blue discoloration (Fig. 3). The most frequently affected areas of the body are breast, abdomen, back, thighs, legs, and wings (Fig. 4).^{10,16,42,53,68}

Figure 3.

Affected featherless and wet skin area showing diffuse dark-red to purple discoloration in a chicken with gangrenous dermatitis.

Figure 4.

Unilateral blue wing disease showing wet, edematous, hyperemic skin and caking feathers in a chick with gangrenous dermatitis.

Gross anatomic lesions

Rapid autolysis is a common and predominant feature of carcasses affected by GD, particularly in cases of sudden death. Feathers can be easily removed from the affected skin areas.⁶⁷ Extensive amounts of edema mixed with gas, and multifocal-to-coalescent hemorrhages can be present in the subcutaneous tissue (Fig. 5).^{10,16,42,53,68} Abrasions are usually present in the overlying skin of affected birds, although cases without obvious pre-existing skin lesions have also been reported.⁵³ The underlying skeletal muscle can show gray or tan discoloration, hemorrhages, edema, and gas between muscle bundles (Fig. 6).^42,53 Vesicle-like lesions and edema, together with soft, blood-filled or broken feather shafts, have been described in the tail region of turkeys.⁵³

Figure 5.

Severe subcutaneous edema, emphysema, and hemorrhage in a turkey with gangrenous dermatitis.

Figure 6.

Pale areas of discoloration and multifocal-to-coalescing hemorrhagic areas in breast muscles in a turkey with gangrenous dermatitis.

Microscopic lesions

In uncomplicated cases of GD associated with C. perfringens, necrotic changes are usually seen in the epidermis and dermis.⁶⁷ Cases coinfected with S. aureus are usually characterized by ulceration of the epidermis and necrosis in dermis and subcutis (Fig. 7).⁶⁸ Subcutaneous tissue has accumulations of serofibrinous exudate and emphysema (Figs. 8, 9).^5,67,68 Examination of the underlying skeletal muscle reveals variable degrees of degeneration and necrosis together with congestion, hemorrhages, and mild inflammatory cell infiltrates (Fig. 10).^53,68 Uncomplicated cases are characterized by the presence of numerous gram-positive, usually non-sporulated, bacilli, singly or in clusters, which are commonly observed within the areas of hemorrhage and subcutaneous edema (Fig. 11). The lack of a prominent inflammatory cell response is characteristic of such cases.⁶⁸ In cases of GD complicated with S. aureus coinfection, gram-positive cocci mixed with variable numbers of heterophils can be observed.⁶⁸ The liver and spleen of affected birds can show randomly scattered, small foci of coagulative necrosis associated with intralesional bacterial colonies secondary to hematogenous spread of bacteria from the skin, subcutis, and muscle.^{10,42,43,53,55,67,68}

Figure 7.

Focal necrosis of epidermis (E) and dermis (D) with moderate infiltration of mixed inflammatory cells in a chicken with gangrenous dermatitis. H&E. Bar = 50 μm.

Figure 8.

Focal necrosis of epidermis (E) and dermis (D) with inflammatory exudate and edema extending to subcutis in a chicken with gangrenous dermatitis. H&E. Bar = 50 μm.

Figure 9.

Marked fibrinous exudate (F) and emphysema (EM) in the subcutis of a chicken with gangrenous dermatitis. H&E. Bar = 70 μm.

Figure 10.

Skeletal myodegeneration (MD) and inflammatory cell infiltrate (ICI) and edema (ED) in a chicken with gangrenous dermatitis. H&E. Bar = 50 μm. Inset: higher magnification of inflammatory cells. Bar = 20 μm.

Figure 11.

Numerous gram-positive, non-sporulated, bacilli within an area of subcutaneous edema in a chicken with gangrenous dermatitis. Gram. Bar = 10 μm.

Diagnosis

Epidemiology, clinical signs, and gross anatomic and microscopic changes are highly suggestive of GD and allow the establishment of a presumptive diagnosis. The observation of gram-positive rods on smears of the serosanguineous exudate, collected from affected skin and/or subcutaneous tissue, adds certainty to the presumptive diagnosis.^53,68 Confirmation of a diagnosis of GD must be based, however, on demonstration of the microorganism(s) involved. Detection can be done by isolation or PCR demonstration of the bacterial species involved.^10,53,68,73 Immunohistochemistry and fluorescent antibody tests are also helpful ancillary techniques to confirm the involvement of specific microorganisms.⁶⁸ GD must be differentiated from a wide range of infectious and non-infectious skin conditions of chickens and turkeys in which necrosis of the skin, subcutaneous tissues, and underlying skeletal muscles occurs. The most significant skin conditions resembling GD include contact dermatitis²⁶; mycotic dermatitis caused by Candida albicans⁴¹ and Rhodotorula spp. infections³,⁶,⁵⁴; bacterial cellulitis caused by E. coli,^{14,18,38,40,45,50,52} Streptococcus dysgalactiae,^45,52 E. rhusiopathiae,¹⁵ Aeromonas hydrophila,^1,52 and mixed aerobic bacteria²⁴; focal ulcerative dermatitis of turkeys²⁵,⁶⁹; scabby hip dermatitis of broiler chickens²⁹; and skin neoplasms such as squamous cell carcinoma^21,28,46,63 and avian keratoacanthoma.^27,28

Prevention

GD can be prevented or controlled to a great extent by preventing cannibalism, reducing overcrowding, providing a balanced diet, decreasing the intensity of light, good ventilation, controlling humidity, controlling ectoparasites, providing perches and dust bathing on the floor, beak and toe trimming, and cleaning and disinfection of houses between each flock placement. Cannibalism is a natural behavioral trait exhibited by dominant birds, which is influenced by genetics and can therefore be difficult to prevent. A few practices that may help to control cannibalism include removing dead birds from the house 2 to 3 times per day, keeping the litter dry, acidifying drinking water and litter, adding iodine to the drinking water, and minimizing bird stress.

Conclusions

GD is considered a major disease in most poultry production areas of the world.¹⁰ Although previous studies have filled some of the gaps in the knowledge about the pathogenesis of GD, particularly in commercial turkeys (https://goo.gl/tiuETr), more information is required to fully understand the pathogenesis of this complex disease. Our review will be useful for the development of prevention and control strategies for GD.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

Funding for the current review was provided by the California Animal Health and Food Safety Laboratory, School of Veterinary Medicine, University of California, Davis.

References

Abdul-Aziz

Barnes

. Miscellaneous and sporadic bacterial infections. In: Swayne

, et al., eds. Diseases of Poultry. 13th ed. Ames, IA: Wiley-Blackwell, 2013:1017–1027.

Andreasen

. Staphlylococcosis. In: Swayne

, et al., eds. Diseases of Poultry. 13th ed. Ames, IA: Wiley-Blackwell, 2013:971–977.

Aruo

SK.

Necrotizing cutaneous rhodotorulosis in chickens in Uganda. Avian Dis 1980;24:1038–1043.

Awaad

MHH

. A research note on the treatment of naturally induced gangrenous dermatitis in chickens by copper sulfate. Vet Med J Giza Egypt 1986;34:121–124.

Bains

MacKenzie

. An outbreak of gangrenous cellulitis caused by Clostridium septicum in a broiler flock. Aust Vet J 1975;51:106–107.

Beemer

, et al. Rhodotorula mucilaginosa dermatitis in feathered parts of chickens: an epizootic on a poultry farm. Avian Dis 1970;14:234–239.

Bianco

, et al. Dermatitis gangrenosa en pollos parrilleros: dos brotes en Río Cuarto [Gangrenous dermatitis in broilers: two outbreaks in Rio Cuarto]. Vet Arg 1985;2:879–883. Spanish.

Carr

, et al. Excessive mortality in market-aged turkeys associated with cellulitis. Avian Dis 1996;40:736–741.

Cervantes

, et al. Staphylococcus-induced gangrenous dermatitis in broilers. Avian Dis 1988;32:140–142.

10.

Clark

, et al. Clostridial dermatitis and cellulitis: an emerging disease on turkeys. Avian Dis 2010;54:788–794.

11.

Collier

, et al. Structure-activity relationships in diphtheria toxin and exotoxin A from Pseudomonas aeruginosa. Prog Clin Biol Res 1979;31:752–759.

12.

Cooper

, et al. Diagnosing clostridial enteric disease in poultry. J Vet Diagn Invest 2013;25:314–327.

13.

de Blieck

Jansen

. Gasoedeem bij kippen na bloedtappen [Gaseous edema in chickens after blood collection]. Tijdschr Diergeneeskd 1931;58:513–518. Dutch.

14.

Derakhshanfar

Ghanbarpour

. A study on avian cellulitis in broiler chickens. Vet Arhiv 2002;72:277–284.

15.

Derakhshanfar

, et al. A pathologic study on experimental Erysipelothrix rhusiopathiae cellulitis in broiler chickens. Vet Arhiv 2004;74:217–224.

16.

Dinev

. Gangrenous dermatitis. In: Diseases of Poultry: A Color Atlas. 1st ed. Stara Zagora, Bulgaria: CEVA Santé Animale, 2007:57–61.

17.

Dinev

Enzootic outbreak of necrotic gastritis associated with Clostridium perfringens in broiler chickens. Avian Pathol 2010;39:7–10.

18.

Elfadil

, et al. Description of cellulitis lesions and associations between cellulitis and other categories of condemnation. Avian Dis 1996;40:690–698.

19.

Elsayed

MSA

, et al. Virulence repertoire of Pseudomonas aeruginosa from some poultry farms with detection of resistance to various antimicrobials and plant extracts. Cell Mol Biol 2016;62:1.

20.

Engström

, et al. Blue wing disease of chickens: experimental infection with a Swedish isolate of chicken anaemia agent and an avian reovirus. Avian Pathol 1988;17:33–50.

21.

Fallavena

LCB

, et al. Diagnosis of skin lesions in condemned or downgraded broiler carcasses-a microscopic and macroscopic study. Avian Pathol 2000;29:557–562.

22.

Fowler

Hussaini

. Clostridium septicum infection and antibiotic treatment in broiler chickens. Vet Rec 1975;96:14–15.

23.

Frazier

, et al. Gangrenous dermatitis of chickens. Avian Dis 1964;8:269–273.

24.

Gomis

, et al. Histopathologic and bacteriologic evaluations of cellulitis detected in legs and caudal abdominal regions of turkeys. Avian Dis 2002;46:192–197.

25.

Gonder

Barnes

. Focal ulcerative dermatitis (“breast buttons”) in marketed turkeys. Avian Dis 1987;31:52–58.

26.

Greene

, et al. A contact dermatitis of broilers—clinical and pathological findings. Avian Pathol 1985;14:23–38.

27.

Hafner

, et al. Avian keratoacanthoma (dermal squamous cell carcinoma) in broiler chicken carcasses. Vet Pathol 1993;30:265–270.

28.

Hafner

, et al. Other tumors. In: Swayne

, et al., eds. Diseases of Poultry. 13th ed. Ames, IA: Wiley-Blackwell, 2013:604–622.

29.

Harris

Jr , et al. The development of dermatitis (scabby-hip) on the hip and thigh of broiler chickens. Avian Dis 1978;22:122–130.

30.

Helfer

, et al. Case report: Clostridium septicum infection in a broiler flock. Avian Dis 1969;13:231–233.

31.

Hermans

, et al. Staphylococcus. In: Gyles

, et al., eds. Pathogenesis of Bacterial Infections in Animals. 4th ed. Ames, IA: Blackwell, 2010:75–89.

32.

Hibberd

, et al. Multilocus sequence typing subtypes of poultry Clostridium perfringens isolates demonstrate disease niche partitioning. J Clin Microbiol 2011;49:1556–1567.

33.

Hoerr

Clinical aspects of immunosuppression in poultry. Avian Dis 2010;54:2–15.

34.

Hofacre

, et al. Subcutaneous clostridial infection in broilers. Avian Dis 1986;30:620–622.

35.

Huff

, et al. Dexamethasone immunosuppression resulting in turkey clostridial dermatitis: a retrospective analysis of seven studies, 1998–2009. Avian Dis 2013;57:730–736.

36.

Ivanics

, et al. [Gangrenous dermatitis in broiler chickens]. Magy Allatorv Lapja 1996;51:599–601. Hungarian.

37.

Jeffrey

, et al. Facial cellulitis associated with fowl cholera in commercial turkeys. Avian Dis 1993;37:1121–1129.

38.

Jeffrey

, et al. Assessing cellulitis pathogenicity of Escherichia coli isolates of broiler chickens assessed by an in vivo inoculation model. Avian Dis 1999;43:491–496.

39.

Kalita

, et al. Gangrenous dermatitis in a flock of Nagaraja chicken. Indian J Poult Sci 2012;47:112–113.

40.

Kumor

, et al. Cellulitis in broiler chickens: epidemiological trends, meat hygiene, and possible human health implications. Avian Dis 1998;42:285–291.

41.

Kuttin

, et al. Chicken dermatitis and loss of feathers from Candida albicans. Avian Dis 1976;20:216–218.

42.

, et al. An outbreak of gangrenous dermatitis in commercial broiler chickens. Avian Pathol 2010;39:247–253.

43.

Lighty

, et al. Incidence of clostridial dermatitis (cellulitis) and factors for development of the disease in turkeys. J Appl Poult Res 2016;25:104–112.

44.

Martland

. Ulcerative dermatitis in broiler chickens: the effects of wet litter. Avian Pathol 1985;14:353–364.

45.

Messier

, et al. Focal cellulitis and dermatitis in broiler chickens: bacteriological and pathological findings. Avian Dis 1993;37:839–844.

46.

Nakamura

, et al. Pathology and microbiology of dermal squamous cell carcinoma in young brown chickens reared in reused litter. Avian Dis 2010;54:1120–1124.

47.

Neumann

Rehberger

TG.

MLST analysis reveals a highly conserved core genome among poultry isolates of Clostridium septicum. Anaerobe 2009;15:99–106.

48.

Niemann

KW.

Clostridium welchii infection in the domestic fowl. J Am Vet Med Assoc 1930;77:604–606.

49.

Nievas

, et al. Subcutaneous clostridial infection in Adelie penguins in Hope Bay, Antarctica. Polar Biol 2007;30:249–252.

50.

Nolan

, et al. Colibacillosis. In: Swayne

, et al., eds. Diseases of Poultry. 13th ed. Ames, IA: Wiley-Blackwell, 2013:751–785.

51.

Okonkwo

Madubuike

. An outbreak of gangrenous dermatitis in broiler chicken reared on battery cage operation in Umuahia, Abia State, Nigeria. J Vet Adv 2015;5:819–825.

52.

Olkowski

, et al. Cellulitis lesions in commercial turkeys identified during processing. Vet Rec 1999;145:228–229.

53.

Opengart

. Gangrenous dermatitis. In: Swayne

, et al., eds. Diseases of Poultry. 13th ed. Ames, IA: Wiley-Blackwell, 2013:957–960.

54.

Page

, et al. Dermatitis produced by Rhodotorula glutinis in broiler-age chickens. Avian Dis 1976;20:416–421.

55.

Pass

DA.

The pathology of the avian integument: a review. Avian Pathol 1989;18:1–72.

56.

Peterson

EH.

Clostridium novyi isolated from chickens. Poult Sci 1964;43:1062–1063.

57.

Popoff

MR.

Toxins of histotoxic clostridia: Clostridium chauvoei, Clostridium septicum, Clostridium novyi, and Clostridium sordellii. In: Uzal

, et al., eds. Clostridial Diseases of Animals. Ames, IA: Wiley-Blackwell, 2016:23–43.

58.

Prescott

JF.

Brief description of animal pathogenic clostridia. In: Uzal

, et al., eds. Clostridial Diseases of Animals. Ames, IA: Wiley-Blackwell, 2016:13–19.

59.

Prescott

, et al. 2016. Taxonomic relationships among the clostridia. In: Uzal

, et al., eds. Clostridial Diseases of Animals. Ames, IA: Wiley-Blackwell, 2016:3–5.

60.

Reece

, et al. Diseases diagnosed in broiler chicken flocks in Victoria, Australia, 1977 to 1984. Vet Rec 1985;116:315–320.

61.

Rhoades

Rimler

. Capsular groups of Pasteurella multocida isolated from avian hosts. Avian Dis 1987;31:895–898.

62.

Rhoades

Rimler

. Virulence and toxigenicity of capsular serogroup D Pasteurella multocida strains isolated from avian hosts. Avian Dis 1990;34:384–388.

63.

Riddell

Shettigara

. Dermal squamous cell carcinoma in broiler chickens in Saskatchewan. Can Vet J 1980;21:287–289.

64.

Salvadori

, et al. Vacuolating cytotoxin produced by avian pathogenic Escherichia coli. Avian Dis 2001;45:43–51.

65.

Saunders

Bickford

. Clostridial infections of growing chickens. Avian Dis 1965;9:317–326.

66.

Shirasaka

Benno

Isolation of Clostridium septicum from diseased chickens in broiler farms. Jpn J Vet Sci 1982;44:807–809.

67.

Shivaprasad

. Integumentary. In: Fletcher

Abdul-Aziz

, eds. Avian Histopathology. 3rd ed. Madison, WI: American Association of Avian Pathologists, 2008:392–427.

68.

Shivaprasad

HL.

Gangrenous dermatitis in poultry. In: Uzal

, et al., eds. Clostridial Diseases of Animals. Ames, IA: Wiley-Blackwell, 2016:255–264.

69.

St-Hilaire

, et al. Association between cellulitis (enlarged sternal bursa) and focal ulcerative dermatitis in Ontario turkeys at the time of processing. Avian Dis 2003;47:531–536.

70.

Tellez

, et al. Evidence for Clostridium septicum as a primary cause of cellulitis in commercial turkeys. J Vet Diagn Invest 2009;21:374–377.

71.

Thachil

, et al. Role of Clostridium perfringens and Clostridium septicum in causing turkey cellulitis. Avian Dis 2010;54:795–801.

72.

Thachil

, et al. Effects of dexamethasone immunosuppression on turkey clostridial dermatitis. Avian Dis 2014;58:433–436.

73.

Thayer

Miller

. Clostridial diseases. In: Dufour-Zavala

, et al., eds. A Laboratory Manual for the Isolation, Identification and Characterization of Avian Pathogens. 5th ed. Madison, WI: American Association of Avian Pathologists, 2008:47–52.

74.

Wang

, et al. Neuraminidase production by Erysipelothrix rhusiopathiae. Vet Microbiol 2015;107:265–272.

75.

Weymouth

, et al. Report of Clostridium in capons. Avian Dis 1963;7:342–343.

76.

Wilder

, et al. Differences in the pathogenicity of various bacterial isolates used in an induction model for gangrenous dermatitis in broiler chickens. Avian Dis 2001;45:659–662.

77.

Willoughby

, et al. Periodic recurrence of gangrenous dermatitis associated with Clostridium septicum in a broiler chicken operation. J Vet Diagn Invest 1996;8:259–261.

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