European Association of Zoo and Wildlife Veterinarians - Transmissible Diseases Handbook 2019

DEVRIESEA AGAMARUM IN LIZARDS

B02.03 OIE BALAI EU AHL

BACTERIA Devriesea agamarum ZOONOSIS

SUSCEPTIBLE PREVENTION TRANSMISSION CLINICAL SIGNS SEVERITY TREATMENT ANIMAL GROUPS AND CONTROL

Lizards (Agamidae, Direct contact Cheilitis Chronic disease in Antimicrobial Detection of Iguanidae, (scratching, biting Uromastyx spp. therapy asymptomatic Peri-cloacal Eublepharidae) lesions) and Crotaphytus (ceftiofur, carriers dermatitis spp. ceftazidime) Indirect contact Environmental Localized dermal (decreased skin Acute septicemia Environmental disinfection granulomas integrity and high disinfection Treatment of predisposes to Dermato- mortality has Optimize affected animals infection) septicemia been noted in husbandry Agama spp. Exposure to

asymptomatic

carriers, such as Pogona vitticeps

FACT SHEET COMPILED BY LAST UPDATE La’Toya Latney, DVM, DECZM (ZHM), DABVP Reptile & Amphibian Practice February 2018

FACT SHEET REVIEWED BY Tom Hellebuyck, DVM, PhD, Dipl ECZM (Herpetology)

DISEASE AGENT Devriesea agamarum is a gram-positive, short rod in the phylum Actinobacteria. Measuring approximately 1 to 2 mm in length, D. agamarum organisms are non-spore-forming, non-motile, non-acid-fast rods that occur singly, in pairs, or in short chains. This bacterial agent has been previously identified as a part of the oral microbiota in a variety of species. It has emerged as a primary pathogen of captive Uromastyx, Crotaphytus, Physignathus, Agama spp. and wild Iguana delicatissima with increased virulence in other agamid, iguanid and euphlebarid species. There are 8 AFLP strains currently recognized in free-ranging and captive lizards. The predominant AFLP type found in wild I. delicatissima has until now exclusively been demonstrated in captive Uromastyx lizards.

SUSCEPTIBLE ANIMAL GROUPS Infections have been described in many species including: spiny-tailed lizards (Uromastyx spp.), free-ranging endangered Lesser Antillean Iguanas (Iguana delicatissima), jewelled curly-tailed lizard (Leiocephalus personatus), frilled lizard (Chlamydosaurus kingii), Philippine sailfin lizard (Hydrosaurus pustulatus), Eastern collared lizard (Crotaphytus collaris), leopard gecko (Eublepharis macularius), Bibron’s agama (Agama impalearis), plumed Basilisk (Basciliscus plumifrons), Chinese water dragon (Physignathus cocincinus), one case report of infection in an Inland bearded dragon (Pogona vitticeps). In addition to a variety of lizards species, inland bearded dragons (Pogona vitticeps) however are primarily considered to be asymptomatic carriers.

ZOONOTIC POTENTIAL None.

DISTRIBUTION Worldwide.

Devriesea Agamarum in Lizards - Fact Sheet B02.03 European Association of Zoo and Wildlife Veterinarians - Transmissible Diseases Handbook 2019

TRANSMISSION The route of transmission has been proven via Koch’s postulates by Hellebuyck et al. (2009). The bacterium can be dermally inoculated and/or primarily infect abraded skin in susceptible species. The organism can survive over 5 months in humid sand and distilled water, and was detected in dermal crusts removed from affected animals for up to 57 days. Transmission can occur from contact with asymptomatic carriers. Long-term environmental survival as well as the presence of asymptomatic carriers are important factors that contribute to persistence of devrieseasis in captive collections.

INCUBATION PERIOD Experimental transmission studies have demonstrated that dermal inoculation of D. agamarum induced dermatitis as early as 5-9 days after exposure. Distinctive dermal crusts are noted on the lips and other dermal sites in affected species. Asymptomatic Pogona vitticeps can be reservoirs causing persistent clinical disease in susceptible lizard species.

CLINICAL SIGNS Clinical signs typically include hyperkeratotic lesions of the skin, presenting as distinctive cheilitis and peri-cloacal dermatitis, however lesions have been also noted along the lateral body wall, medial side of hindlegs and distal extremities in affected species, and less frequently localized dermal granulomas have been reported in e.g. Uromastyx spp. and Physignathus cocincinus. The disease can progress rapidly to cause septicemia in e.g. Agama species.

PATHOLOGY AND POST MORTEM FINDINGS Gross findings: Localized dermal granulomas, dermatitis, and cheilitis, may be noted, with additional microabscessation noted in various organs in septic animals. Concurrent infections with other pathogens has been reported in a single case, which included Chrysosporium guarroi, another pathogen that can also cause a severe dermatitis and dermatosepticemia. In this case, D.agamarum may have been a contaminant, however mixed infections are possible. Histologic findings: For dermal lesions, epidermal hyperplasia, orthokeratotic hyperkeratosis, spongiosis as well as adjacent epidermal edema and/or granuloma formation. In systemic cases, granulomatous lesions with gram-positive rod colonization may also be visible in the liver and muscle.

DIAGNOSIS Microbiology: Microbiological examination of samples from infected tissue or the inside of dermal crusts is the most important. Oral and cloacal swabs can help in the detection of asymptomatic carriers. Histopathologic evaluation of lesions: Epidermal hyperplasia, orthokeratotic hyperkeratosis, spongiosis as well as adjacent epidermal edema and/or granuloma formation may be present in biopsied lesions. Histologic Stains: Gram stained sections may reveal colonization with Gram-positive bacteria in the superficial corneal layers and throughout biopsied granulomas. Hyperemia, moderate edema and the perivascular influx of heterophils may also be present in the dermis. PCR: Morphological and biochemical identification of suspected isolates is possible but species confirmation requires 16S rRNA PCR.

SAMPLES REQUIRED FOR LABORATORY ANALYSIS Swabs or biopsy specimens of oral and other lesions. Oral and cloacal samples are collected mostly in asymptomatic carriers, animals that have no skin lesions. Dead animals or skin of dead animals for necropsy and bacterial detection.

TREATMENT In severe cases, surgical debridement of dermal lesions may be indicated and concurrent parenteral antibiotic therapy is necessary. Ceftiofur, a third-generation cephalosporin, administered intramuscularly at 5 mg/kg every 24 hours for an average of 18 days in Pogona vitticeps and 12 days in Uromastyx spp. has been described as an effective treatment. Enrofloxacin at 5 mg/kg IM q24h did not eliminate bacterial infection. One case series in clinically affected Uromastyx spp. revealed that D. agamarum was inhibited by ceftazidime, erythromycin, and tetracycline, and that the highest resistance was shown to enrofloxacin, penicillin, and gentamicin on individual culture and sensitivity. Ceftazidime, 10 mg/kg IM q72h for 15 days, proved clinically effective in the aforementioned report for clinical Uromastyx species. The importance of susceptibility testing of any isolate can not be overly emphasized.

Devriesea Agamarum in Lizards - Fact Sheet B02.03 European Association of Zoo and Wildlife Veterinarians - Transmissible Diseases Handbook 2019

PREVENTION Bacteriology needs to be performed on newly acquired animals and suspected isolates can be submitted for 16S rRNA PCR to confirm the species being D. agamarum. Microbiological examination of oral and cloacal swabs should also be carried out during quarantine, especially to allow the detection of asymptomatic carriers. Enclosures and all equipment should be disinfected regularly.

CONTROL Environmental control of the pathogen can be obtained by using following common agents to disinfect hard surfaces with a minimum contact time of 5 minutes: sodium hypochlorite (0.05% - 0.5%), chlorhexidine (0.05%–0.5%), boric acid (0.01%), and ethanol (70%). Disinfectants are listed at the minimal concentrations needed to inactivate the pathogen.

LEGISLATIVE REQUIREMENTS Not notifiable under OIE 2019, BALAI (Council Directive 92/65/ECC) or AHL (Regulation EU 2016/429).

RELEVANT DIAGNOSTIC LABORATORIES In general, laboratories offering standard microbiological diagnostic testing with some experience with reptile samples. Contact the lab to make sure they are aware of D. agamarum as a differential and are able to identify this bacterium.

REFERENCES 1. Martel, A. et al. 2008. Devriesea agamarum gen. nov., sp. nov., a novel actinobacterium associated with dermatitis and septicaemia in agamid lizards. Int. J. Syst. Evol. Microbiol. 58(9): 2206-2209. 2. Devloo, R. et al. 2011. Bearded dragons (Pogona vitticeps) asymptomatically infected with Devriesea agamarum are a source of persistent clinical infection in captive colonies of dab lizards (Uromastyx sp.). Vet Microbiol 150: 297–301. 3. Hellebuyck T. et al. 2009. Designing a successful antimicrobial treatment against Devriesea agamarum infections in lizards. Vet Microbiol 139(1):189–192. 4. Hellebuyck T. et al. 2009. Devriesea agamarum causes dermatitis in bearded dragons (Pogona vitticeps). Vet Microbiol 134(3):267–271. 5. Hellebuyck T. et al. 2011. Prolonged environmental persistence requires efficient disinfection procedures to control Devriesea agamarum associated disease in lizards. Lett Appl Microbiol 52(1):28–32. 6. Schmidt‐Ukaj, S. et al. 2014. Infection with Devriesea agamarum and Chrysosporium guarroi in an inland bearded dragon (Pogona vitticeps). Vet dermatol 25(6): 555-e97. 7. Lukac, M. et al. 2013. Findings of Devriesea agamarum associated infections in spiny-tailed lizards (Uromastyx sp.) in Croatia. Journal of zoo and wildlife medicine 44(2): 430-434. 8. Hellebuyck, Tom, et al. 2014. Autovaccination confers protection against Devriesea agamarum associated septicemia but not dermatitis in bearded dragons (Pogona vitticeps). PloS one 9(12): e113084. 9. Bauwens, L. et al. 2014.Prevalence of Devriesea agamarum in the lizard collection of The Royal Zoological Society of Antwerp. J Aquarium Res 2: 88-91. 10. Hellebuyck, T, et al. 2017. A virulent clone of Devriesea agamarum affects endangered Lesser Antillean iguanas (Iguana delicatissima). Scientific reports Nature 7.1: 12491-12497. 11. Rossier, C. et al. 2016. Devriesea in a Plumed basilisk (Basiliscus pulmfrons) and Chinese water dragons (Physignathus cocincinus) in a zoological collection. J Zoo and Wildl Med 47(1): 280-285. 12. Haesendonck, R. et al. 2017. Genome sequence of Devriesea agamarum, isolated from agamid lizards with dermatitis." Genome announcements 3(4): e00949-15.

Devriesea Agamarum in Lizards - Fact Sheet B02.03