What Is Your Diagnosis? Author(s): Source: Journal of Avian Medicine and Surgery, 28(4):343-347. Published By: Association of Avian Veterinarians DOI: http://dx.doi.org/10.1647/2013-009 URL: http://www.bioone.org/doi/full/10.1647/2013-009
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Avian Medicine and Surgery 28(4):343–347, 2014 Ó 2014 by the Association of Avian Veterinarians
What Is Your Diagnosis? thoracic air sacs were slightly opaque, and the pleural surfaces were diffusely thickened with sticky, yellow mucoid material. Multiple nodular masses were attached to the mesentery and mesovarium, and a large (6 3 2 3 1-cm) mass extended from the infundibulum of the oviduct (Fig 2). On cut section, the masses contained caseous material. The ovary contained 3, dark redbrown, 2–4-cm masses (Fig 3). A 4-mm-diameter, yellow-tan, caseous plug was present within both external ear canals, extending toward the middle ear. At necropsy, various tissue samples were fixed in neutral-buffered 10% formalin, routinely processed, embedded in paraffin, sectioned, and stained with hematoxylin and eosin. On histologic examination, inflammatory infiltrate was present within the mesentery and mesovarium consisting of
History Multiple cases of upper respiratory disease developed in a free-range flock of Brahma chickens. The flock consisted of 70 hens and 4 roosters; approximately 40 birds became ill or died. Clinical signs were sneezing, coughing, and mucoid nasal and ocular discharge. A subset of birds also developed torticollis, with most of the animals dying within 1 week of developing clinical disease. The entire flock had been recently treated for 7 days with tetracycline (211 mg/L in the drinking water q24h). The owner had reported a problem with raccoons (Procyon lotor) on the property. The carcass of a hen with signs of torticollis (Fig 1), ataxia, and general unresponsiveness to stimuli was submitted to the Diagnostic Center for Population and Animal Health at Michigan State University for necropsy. The hen that was presented for a pathologic evaluation weighed 1.95 kg and had very poor body condition, as evidenced by a prominent keel. The oral cavity and trachea contained a moderate amount of yellow-white mucoid material. The
Figure 2. The hen described in Figure 1 at necropsy. The thoracic air sacs were slightly opaque, and the pleural surfaces were diffusely thickened with sticky, yellow mucoid material. Multiple nodular masses were present throughout the coelom and within the mesentery and mesovarium.
Figure 1. A hen exhibiting clinical signs of severe torticollis, ataxia, and upper respiratory disease. The hen was from a flock of 74 birds; 40 of which had become ill or died.
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Figure 3. The hen described in Figure 1 at necropsy. The ovary contained 3 dark-brown hemorrhagic masses (lower right). The mesovarium extending from the infundibulum contained a large 6 3 2 3 1-cm, caseous mass (left).
Figure 5. Higher magnification of oviduct described in Figure 4, highlighting numerous bacterial colonies (arrow) within the necrotic exudate. Note the adjacent, tall, columnar epithelium (arrowhead) (hematoxylin and eosin, 320).
heterophils and histiocytes with aggregates of basophilic coccobacilli. The sections of ovary, infundibulum, and magnum were characterized by a large amount of amorphous, granular, hypereosinophilic necrotic debris, surrounded by granulation tissue and inflammatory infiltrate with intralesional basophilic coccobacilli (Fig 4). The inflammatory infiltrate consisted primarily of epithelioid macrophages and heterophils with occasional lymphocytes and plasma cells. A segment of cerebellar leptomeninges was expanded by a large focus of caseous debris and enveloped by
aggregates of heterophils surrounded by epithelioid macrophages (Figs 5 through 7). The lumen of the trachea contained wispy, basophilic mucoid material and debris, admixed with basophilic coccobacilli. Sections of cecum and colon contained numerous ascarid nematodes (200–300 lm in diameter) with prominent lateral alae, lateral cords, coelomyarian musculature, and uninucleate intestinal epithelium, consistent with Heterakis species. The feathered skin around the vent contained moderate perifollicular lymphoplasmacytic inflammation.
Figure 4. Photomicrograph of the oviduct from the hen described in Figure 1. The oviduct contains a large focus of hypereosinophilic, amorphous necrotic debris (*). Note the glandular epithelium (arrowhead) (hematoxylin and eosin, 34).
Figure 6. Higher magnification of the oviduct described in Figure 4, highlighting bacterial colonies, and variously degenerate heterophils (hematoxylin and eosin, 340).
WHAT IS YOUR DIAGNOSIS?
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Figure 7. High magnification of a section of the cerebellum from the hen described in Figure 1. A large mat of amorphous, hypereosinophilic debris and degenerate heterophils is present within the meninges (arrow), and a focus of necrosis (adjacent to *) is within the molecular layer of the cerebellum (arrowhead) (hematoxylin and eosin, 320).
Please evaluate the history, physical condition findings, and Figures 1–7. Formulate a list of differential diagnoses and consider other diagnostic tests before proceeding.
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Diagnosis At necropsy, the gross and histologic findings were chronic, granulomatous, heterophilic, and necrotizing oophoritis; salpingitis; peritonitis; otitis; and meningitis, as well as endoparasitism by Heterakis species. In chickens, differential diagnoses for salpingitis and peritonitis are infection with avian pathogenic Escherichia coli, Salmonella enterica, Mycoplasma gallisepticum, Pasteurella multocida, and Gallibacterium anatis. In this case, a choanal swab sample and mucoid discharge collected from the trachea and upper airways at necropsy were submitted to the bacteriology department at the Diagnostic Center for Population and Animal Health for culture. The culture and susceptibility test results revealed numerous G anatis. This isolate was distinguished from other Pasteurella species and was noted to be resistant to oxytetracyclines. The final diagnosis in this case was G anatis septicemia. Discussion The clinical signs and course of disease on this farm are most consistent with fowl cholera caused by P multocida. This gram-negative, bipolarstaining bacillus enters the body through mucus membranes of the pharynx or conjunctiva. Fowl cholera is characterized by acute upper respiratory disease and septicemia. Birds that survive the acute phase may develop chronic disease, typically characterized by localized caseous reaction in the wattle, joints, pharynx, reproductive tract, or middle ear. Turkeys are most susceptible, but outbreaks have occurred in chickens older than 16 weeks. Pasteurella multocida will disseminate in a flock through oral and nasal secretions that contaminate the environment. Sources of infection include chronically infected birds and wildlife reservoirs, such as free-flying birds, cats, and raccoons.1 Gallibacterium anatis biovar haemolytica is a recently characterized bacterium of the Pasteurellaceae family. Previously grouped as [Pasteurella haemolytica]-‘‘Actinobacillus salpingitidis’’ complex, a new genus was established following genetic and morphologic description.2–4 It has been proposed that G anatis has a role in peritonitis and salpingitis in chickens concurrently infected with avian pathogenic E coli.3,5,6 Gallibacterium anatis has been isolated from the respiratory and reproductive tracts of healthy birds and is thought to be part of the normal flora.7 Studies involving intravenous injection with a well-characterized, virulent strain
of G anatis in immunosuppressed chickens resulted in 73% mortality.7 In healthy chickens, this experiment resulted in severe septicemic lesions. Intraperitoneal injection of the same strain resulted in local and diffuse peritonitis in healthy and immunosuppressed birds, respectively.7 A separate study documented bacteremia following instillation of G anatis through the nasal passages of healthy chickens.8 Virulent strains of G anatis have been shown to express an atypical RTX toxin (GtxA), which may be responsible for its hemolytic activity. They also express iron transporters, capsular proteins, and matrix metalloproteinases shown to degrade chicken immunoglobulin G; all of which may contribute to pathogenicity.9–11 Additionally, 65% of field strains of G anatis demonstrated multidrug resistance, with resistance to tetracyclines (92% of strains) and sulfamethoxazole (96%) as the most common findings.12,13 The isolate in this case was resistant to oxytetracycline and sulfadimethoxine. Bacterial respiratory infection in live birds may be diagnosed by culture of nasal swabs or nasal discharge. Definitive diagnosis at necropsy is best accomplished in acutely affected birds that have not been previously treated with antibiotics. The best clinical outcome follows prompt diagnosis, culture, and appropriate antibiotic selection. We propose that this flock may have had a prior outbreak of disease because of a primary infection of P multocida (with or without avian pathogenic E coli) and a secondary infection with G anatis. The P multocida infection may have been successfully treated with the 7-day course of tetracycline administered by the owner, which allowed the concurrent G anatis infection to perpetuate clinical signs in these birds. This case demonstrates the importance of appropriate submission of fresh tissue samples or live, untreated birds for the best diagnostic outcome and supports a potential role of G anatis as a secondary pathogen in chickens. Plans for this farm include collection of antemortem samples and necropsy of acutely affected birds in an attempt to definitively diagnose fowl cholera. This case was submitted by Rebecca Kohnken, DVM, College of Veterinary Medicine, Ohio State University, 1900 Coffey Road, Columbus, OH 43210, USA; and David B. Needle, DVM, Stephanie J. French, DVM, MS, and Jon S. Patterson, DVM, PhD, Dipl ACVP, Diagnostic Center for Population and Animal Health, 4125 Beaumont Road, Michigan State University, Lansing, MI 48910, USA.
WHAT IS YOUR DIAGNOSIS?
References 1. Saif YM, ed. Diseases of Poultry. 11th ed. Ames, IA: Iowa State Press; 2003. 2. Christensen H, Bisgaard M, Bojesen AM, et al. Genetic relationships among avian isolates classified as Pasteurella haemolytica, ‘Actinobacillus salpingitidis’ or Pasteurella anatis with proposal of Gallibacterium anatis gen. nov., comb. nov. and description of additional genomospecies with Gallibacterium gen. nov. Int J Syst Evol Microbiol. 2003;53(pt 1):275–287. 3. Johnson TJ, Nolan LK, Trampel DW. Understanding Gallibacterium-Associated Peritonitis in the Commercial Egg-Laying Industry. St Paul, MN: Midwest Poultry Research Program; 2007–2008. 4. Kristensen BM, Sinha S, Boyce JD, et al. Natural transformation of Gallibacterium anatis. Appl Environ Microbiol. 2012;78(14):4914–4922. 5. Castellanos L, Vazquez M, Carrillo A, Campogarrido R. Protection Conferred by a Commercial Gallibacterium anatis Vaccine in Commercial Layers. Jalisco, Mexico: Poultry Technical Department, Boehringer Ingelheim; 2006. 6. Neubauer C, De Souza-Pilz M, Bojesen AM, et al. Tissue distribution of haemolytic Gallibacterium anatis isolates in laying birds with reproductive disorders. Avian Pathol. 2009;38(1):1–7.
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7. Bojesen AM, Nielsen OL, Christensen JP, Bisgaard M. In vivo studies of Gallibacterium anatis infection in chickens. Avian Pathol. 2004;33(2):145–152. 8. Zepeda VA, Calder´on-Apodaca NL, Paasch ML, et al. Histopathologic findings in chickens experimentally infected with Gallibacterium anatis by nasal instillation. Avian Dis. 2010;54(4):1306–1309. 9. Garcia-Gomez E, Vaca S, Perez-Mendez A, et al. Gallibacterium anatis-secreted metalloproteases degrade chicken IgG. Avian Pathol. 2005;34(5):426– 429. 10. Kristensen BM, Frees D, Bojesen AM. Expression and secretion of the RTX-toxin GtxA among members of the genus Gallibacterium. Vet Microbiol. 2011;153(1–2):116–123. 11. Kristensen BM, Frees D, Bojesen AM. GtxA from Gallibacterium anatis, a cytolytic RTX-toxin with a novel domain organization. Vet Res. 2010;41(3):25. 12. Bojesen AM, Bager RJ, Ifrah D, Aarestrup FM. The rarely reported tet(31) tetracycline resistance determinant is common in Gallibacterium anatis. Vet Microbiol. 2011;149(3–4):497–499. 13. Bojesen AM, Vazquez ME, Bager RJ, et al. Antimicrobial susceptibility and tetracycline resistance determinant genotyping of Gallibacterium anatis. Vet Microbiol. 2011;148(1):105–110.
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Avian Medicine and Surgery 28(4):343–347, 2014 Ó 2014 by the Association of Avian Veterinarians
What Is Your Diagnosis? thoracic air sacs were slightly opaque, and the pleural surfaces were diffusely thickened with sticky, yellow mucoid material. Multiple nodular masses were attached to the mesentery and mesovarium, and a large (6 3 2 3 1-cm) mass extended from the infundibulum of the oviduct (Fig 2). On cut section, the masses contained caseous material. The ovary contained 3, dark redbrown, 2–4-cm masses (Fig 3). A 4-mm-diameter, yellow-tan, caseous plug was present within both external ear canals, extending toward the middle ear. At necropsy, various tissue samples were fixed in neutral-buffered 10% formalin, routinely processed, embedded in paraffin, sectioned, and stained with hematoxylin and eosin. On histologic examination, inflammatory infiltrate was present within the mesentery and mesovarium consisting of
History Multiple cases of upper respiratory disease developed in a free-range flock of Brahma chickens. The flock consisted of 70 hens and 4 roosters; approximately 40 birds became ill or died. Clinical signs were sneezing, coughing, and mucoid nasal and ocular discharge. A subset of birds also developed torticollis, with most of the animals dying within 1 week of developing clinical disease. The entire flock had been recently treated for 7 days with tetracycline (211 mg/L in the drinking water q24h). The owner had reported a problem with raccoons (Procyon lotor) on the property. The carcass of a hen with signs of torticollis (Fig 1), ataxia, and general unresponsiveness to stimuli was submitted to the Diagnostic Center for Population and Animal Health at Michigan State University for necropsy. The hen that was presented for a pathologic evaluation weighed 1.95 kg and had very poor body condition, as evidenced by a prominent keel. The oral cavity and trachea contained a moderate amount of yellow-white mucoid material. The
Figure 2. The hen described in Figure 1 at necropsy. The thoracic air sacs were slightly opaque, and the pleural surfaces were diffusely thickened with sticky, yellow mucoid material. Multiple nodular masses were present throughout the coelom and within the mesentery and mesovarium.
Figure 1. A hen exhibiting clinical signs of severe torticollis, ataxia, and upper respiratory disease. The hen was from a flock of 74 birds; 40 of which had become ill or died.
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JOURNAL OF AVIAN MEDICINE AND SURGERY
Figure 3. The hen described in Figure 1 at necropsy. The ovary contained 3 dark-brown hemorrhagic masses (lower right). The mesovarium extending from the infundibulum contained a large 6 3 2 3 1-cm, caseous mass (left).
Figure 5. Higher magnification of oviduct described in Figure 4, highlighting numerous bacterial colonies (arrow) within the necrotic exudate. Note the adjacent, tall, columnar epithelium (arrowhead) (hematoxylin and eosin, 320).
heterophils and histiocytes with aggregates of basophilic coccobacilli. The sections of ovary, infundibulum, and magnum were characterized by a large amount of amorphous, granular, hypereosinophilic necrotic debris, surrounded by granulation tissue and inflammatory infiltrate with intralesional basophilic coccobacilli (Fig 4). The inflammatory infiltrate consisted primarily of epithelioid macrophages and heterophils with occasional lymphocytes and plasma cells. A segment of cerebellar leptomeninges was expanded by a large focus of caseous debris and enveloped by
aggregates of heterophils surrounded by epithelioid macrophages (Figs 5 through 7). The lumen of the trachea contained wispy, basophilic mucoid material and debris, admixed with basophilic coccobacilli. Sections of cecum and colon contained numerous ascarid nematodes (200–300 lm in diameter) with prominent lateral alae, lateral cords, coelomyarian musculature, and uninucleate intestinal epithelium, consistent with Heterakis species. The feathered skin around the vent contained moderate perifollicular lymphoplasmacytic inflammation.
Figure 4. Photomicrograph of the oviduct from the hen described in Figure 1. The oviduct contains a large focus of hypereosinophilic, amorphous necrotic debris (*). Note the glandular epithelium (arrowhead) (hematoxylin and eosin, 34).
Figure 6. Higher magnification of the oviduct described in Figure 4, highlighting bacterial colonies, and variously degenerate heterophils (hematoxylin and eosin, 340).
WHAT IS YOUR DIAGNOSIS?
345
Figure 7. High magnification of a section of the cerebellum from the hen described in Figure 1. A large mat of amorphous, hypereosinophilic debris and degenerate heterophils is present within the meninges (arrow), and a focus of necrosis (adjacent to *) is within the molecular layer of the cerebellum (arrowhead) (hematoxylin and eosin, 320).
Please evaluate the history, physical condition findings, and Figures 1–7. Formulate a list of differential diagnoses and consider other diagnostic tests before proceeding.
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JOURNAL OF AVIAN MEDICINE AND SURGERY
Diagnosis At necropsy, the gross and histologic findings were chronic, granulomatous, heterophilic, and necrotizing oophoritis; salpingitis; peritonitis; otitis; and meningitis, as well as endoparasitism by Heterakis species. In chickens, differential diagnoses for salpingitis and peritonitis are infection with avian pathogenic Escherichia coli, Salmonella enterica, Mycoplasma gallisepticum, Pasteurella multocida, and Gallibacterium anatis. In this case, a choanal swab sample and mucoid discharge collected from the trachea and upper airways at necropsy were submitted to the bacteriology department at the Diagnostic Center for Population and Animal Health for culture. The culture and susceptibility test results revealed numerous G anatis. This isolate was distinguished from other Pasteurella species and was noted to be resistant to oxytetracyclines. The final diagnosis in this case was G anatis septicemia. Discussion The clinical signs and course of disease on this farm are most consistent with fowl cholera caused by P multocida. This gram-negative, bipolarstaining bacillus enters the body through mucus membranes of the pharynx or conjunctiva. Fowl cholera is characterized by acute upper respiratory disease and septicemia. Birds that survive the acute phase may develop chronic disease, typically characterized by localized caseous reaction in the wattle, joints, pharynx, reproductive tract, or middle ear. Turkeys are most susceptible, but outbreaks have occurred in chickens older than 16 weeks. Pasteurella multocida will disseminate in a flock through oral and nasal secretions that contaminate the environment. Sources of infection include chronically infected birds and wildlife reservoirs, such as free-flying birds, cats, and raccoons.1 Gallibacterium anatis biovar haemolytica is a recently characterized bacterium of the Pasteurellaceae family. Previously grouped as [Pasteurella haemolytica]-‘‘Actinobacillus salpingitidis’’ complex, a new genus was established following genetic and morphologic description.2–4 It has been proposed that G anatis has a role in peritonitis and salpingitis in chickens concurrently infected with avian pathogenic E coli.3,5,6 Gallibacterium anatis has been isolated from the respiratory and reproductive tracts of healthy birds and is thought to be part of the normal flora.7 Studies involving intravenous injection with a well-characterized, virulent strain
of G anatis in immunosuppressed chickens resulted in 73% mortality.7 In healthy chickens, this experiment resulted in severe septicemic lesions. Intraperitoneal injection of the same strain resulted in local and diffuse peritonitis in healthy and immunosuppressed birds, respectively.7 A separate study documented bacteremia following instillation of G anatis through the nasal passages of healthy chickens.8 Virulent strains of G anatis have been shown to express an atypical RTX toxin (GtxA), which may be responsible for its hemolytic activity. They also express iron transporters, capsular proteins, and matrix metalloproteinases shown to degrade chicken immunoglobulin G; all of which may contribute to pathogenicity.9–11 Additionally, 65% of field strains of G anatis demonstrated multidrug resistance, with resistance to tetracyclines (92% of strains) and sulfamethoxazole (96%) as the most common findings.12,13 The isolate in this case was resistant to oxytetracycline and sulfadimethoxine. Bacterial respiratory infection in live birds may be diagnosed by culture of nasal swabs or nasal discharge. Definitive diagnosis at necropsy is best accomplished in acutely affected birds that have not been previously treated with antibiotics. The best clinical outcome follows prompt diagnosis, culture, and appropriate antibiotic selection. We propose that this flock may have had a prior outbreak of disease because of a primary infection of P multocida (with or without avian pathogenic E coli) and a secondary infection with G anatis. The P multocida infection may have been successfully treated with the 7-day course of tetracycline administered by the owner, which allowed the concurrent G anatis infection to perpetuate clinical signs in these birds. This case demonstrates the importance of appropriate submission of fresh tissue samples or live, untreated birds for the best diagnostic outcome and supports a potential role of G anatis as a secondary pathogen in chickens. Plans for this farm include collection of antemortem samples and necropsy of acutely affected birds in an attempt to definitively diagnose fowl cholera. This case was submitted by Rebecca Kohnken, DVM, College of Veterinary Medicine, Ohio State University, 1900 Coffey Road, Columbus, OH 43210, USA; and David B. Needle, DVM, Stephanie J. French, DVM, MS, and Jon S. Patterson, DVM, PhD, Dipl ACVP, Diagnostic Center for Population and Animal Health, 4125 Beaumont Road, Michigan State University, Lansing, MI 48910, USA.
WHAT IS YOUR DIAGNOSIS?
References 1. Saif YM, ed. Diseases of Poultry. 11th ed. Ames, IA: Iowa State Press; 2003. 2. Christensen H, Bisgaard M, Bojesen AM, et al. Genetic relationships among avian isolates classified as Pasteurella haemolytica, ‘Actinobacillus salpingitidis’ or Pasteurella anatis with proposal of Gallibacterium anatis gen. nov., comb. nov. and description of additional genomospecies with Gallibacterium gen. nov. Int J Syst Evol Microbiol. 2003;53(pt 1):275–287. 3. Johnson TJ, Nolan LK, Trampel DW. Understanding Gallibacterium-Associated Peritonitis in the Commercial Egg-Laying Industry. St Paul, MN: Midwest Poultry Research Program; 2007–2008. 4. Kristensen BM, Sinha S, Boyce JD, et al. Natural transformation of Gallibacterium anatis. Appl Environ Microbiol. 2012;78(14):4914–4922. 5. Castellanos L, Vazquez M, Carrillo A, Campogarrido R. Protection Conferred by a Commercial Gallibacterium anatis Vaccine in Commercial Layers. Jalisco, Mexico: Poultry Technical Department, Boehringer Ingelheim; 2006. 6. Neubauer C, De Souza-Pilz M, Bojesen AM, et al. Tissue distribution of haemolytic Gallibacterium anatis isolates in laying birds with reproductive disorders. Avian Pathol. 2009;38(1):1–7.
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7. Bojesen AM, Nielsen OL, Christensen JP, Bisgaard M. In vivo studies of Gallibacterium anatis infection in chickens. Avian Pathol. 2004;33(2):145–152. 8. Zepeda VA, Calder´on-Apodaca NL, Paasch ML, et al. Histopathologic findings in chickens experimentally infected with Gallibacterium anatis by nasal instillation. Avian Dis. 2010;54(4):1306–1309. 9. Garcia-Gomez E, Vaca S, Perez-Mendez A, et al. Gallibacterium anatis-secreted metalloproteases degrade chicken IgG. Avian Pathol. 2005;34(5):426– 429. 10. Kristensen BM, Frees D, Bojesen AM. Expression and secretion of the RTX-toxin GtxA among members of the genus Gallibacterium. Vet Microbiol. 2011;153(1–2):116–123. 11. Kristensen BM, Frees D, Bojesen AM. GtxA from Gallibacterium anatis, a cytolytic RTX-toxin with a novel domain organization. Vet Res. 2010;41(3):25. 12. Bojesen AM, Bager RJ, Ifrah D, Aarestrup FM. The rarely reported tet(31) tetracycline resistance determinant is common in Gallibacterium anatis. Vet Microbiol. 2011;149(3–4):497–499. 13. Bojesen AM, Vazquez ME, Bager RJ, et al. Antimicrobial susceptibility and tetracycline resistance determinant genotyping of Gallibacterium anatis. Vet Microbiol. 2011;148(1):105–110.
