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

MYCOPLASMA IN TESTUDINES

B10.06 OIE BALAI EU AHL

BACTERIA Mycoplasma agassizii, M. testudineum ZOONOSIS

SUSCEPTIBLE PREVENTION TRANSMISSION CLINICAL SIGNS SEVERITY TREATMENT GROUPS AND CONTROL

All Testudines Direct contact Nasal and ocular Fatal, species Clarithromycin, Quarantine through nasal or discharge, dependent enrofloxacin, Testing oral secretions palpebral edema, tylosin and conjunctivitis tetracyclines Separation

FACT SHEET COMPILED BY LAST UPDATE Matt Allender, DVM, MS, PhD, DACZM, Wildlife Epidemiology Lab, February 2018 University of Illinois, Urbana, IL 61802, United States of America

FACT SHEET REVIEWED BY Carol Bradford, DVM, MS, DACZM, ABQ BioPark, Albuquerque, NM 87102, United States of America

DISEASE AGENT Mycoplasma agassizii, Mycoplasma testudineum, and an unnamed box Mycoplasma.

SUSCEPTIBLE ANIMAL GROUPS Probably all Testudines. Infections have been described in many species including spp., spp., Terrapene spp., spp., Pyxis spp., spp., spp. and spp.

ZOONOTIC POTENTIAL No.

DISTRIBUTION North America and Europe, likely worldwide.

TRANSMISSION The route of transmission is likely direct contact through nasal or oral secretions.

INCUBATION PERIOD Four to eight weeks in experimental transmission.

CLINICAL SIGNS Lesions are restricted to the upper respiratory tract and include nasal discharge, ocular discharge, palpebral edema, conjunctivitis. Oral plaques can be present in emydids.

PATHOLOGY AND POST MORTEM FINDINGS Histopathology: chronic proliferative rhinitis, the respiratory epithelium becomes hyperplastic and there are diffuse accumulations of mixed inflammatory cells in the lamina propria.

DIAGNOSIS Histopathologic evaluation of lesions. Swabs from the nasal cavity or choanae for culture or PCR. A PCR targeting the 16S

Mycoplasma in Testudines - Fact Sheet B10.06 European Association of Zoo and Wildlife Veterinarians - Transmissible Diseases Handbook 2019 rRNA gene has been used to detect many positive samples. A qPCR targeting Mycoplasma agassizii and M. testudineum exists. ELISA for antibodies to M. agassizii and M. testudineum.

SAMPLES REQUIRED FOR LABORATORY ANALYSIS Swabs for culture or PCR. Serum or plasma for ELISA to detect antibodies. Dead for necropsy and Mycoplasma detection.

TREATMENT Clarithromycin at 15 mg/kg twice weekly. Enrofloxacin at 5 mg/kg (Gopher ) q24-48 hr, or 10 mg/kg (Hermann’s tortoises) q24 hr, or 0.2 mg/ml nasal flush. Tylosin at 5 mg/kg q24 hr. Tetracyclines have also been anecdotally effective.

PREVENTION Quarantine and testing of new acquisitions. Consider positive animals as persistently infected, and restrict access to naive individuals.

CONTROL Suggested disinfectants for housing facilities: alcohol and hydrogen peroxide, but not quaternary ammonium, based cleaners have been shown to be effective. Wash facilities well after disinfection.

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

RELEVANT DIAGNOSTIC LABORATORIES 1. Dr. Rachel E. Marschang, Laboklin GmbH & Co. KG, Bad Kissingen, GERMANY 2. Dr. Silvia Blahak, Chemisches und Veterinäruntersuchungsamt OWL, Detmold, GERMANY It is best to contact the laboratory before collecting and sending the samples to optimise chances of success.

REFERENCES 1. Aiello CM, Nussear KE, Esque TC, Emblidge PG, Sah P, Bansal S, Hudson PJ. 2016. Host contact and shedding patterns clarify variation in pathogen exposure and transmission in threatened Gopherus agassizii: implications for disease modelling and management. J Anim Ecol. 2016 May;85(3):829-42. 2. Brown, M.B., G.S. McLaughlin, P.A. Klein, B.C. Crenshaw, I.M. Schumacher, D.R. Brown, E.R. Jacobson. 1999. Upper respiratory tract disease in the is caused by Mycoplasma agassizii. Journal of Clinical Microbiology 37:2262-2269. 3. Brown, D.R., B.C. Crenshaw, G.S. McLaughlin, I.M. Schumacher, C.E. McKenna, P.A. Klein, E.R. Jacobson, M.B. Brown. 1995. Taxonomic analysis of the tortoise mycoplasmas Mycoplasma agassizii and Mycoplasma testudinis by 16S rRNA gene sequence comparison. International Journal of Systematic Bacteriology 45:348–350. 4. duPre, S.A., C.R. Tracy, K.W. Hunter. 2011. Quantitative PCR method for detection of mycoplasma spp. DNA in nasal lavage samples from the (Gopherus agassizzi). Journal of Microbiological Methods 86:160-165. 5. Farkas SL, Gál J. 2009. Adenovirus and mycoplasma infection in an ornate ( ornata) in Hungary. Vet Microbiol. 2009 Jul 2;138(1-2):169-73. 6. Feldman, S.H., J. Wimsatt , R.E. Marchang, A.J. Johnson, W. Brown, J.C. Mitchell, J.M. Sleeman. 2006. A novel mycoplasma detected in association with upper respiratory disease syndrome in free-ranging eastern box (Terrapene carolina carolina) in Virginia. Journal of Wildlife Diseases 42:279-289. 7. Gauvin J, 1993. Drug therapy in . Semin Avian Exotic Pet Med. 2:48-59. 8. Jacobson E.R., J.M. Gaskin, M.B. Brown, R.K. Harris, C.H. Gardiner, J.L. LaPointe, H.P. Adams, C. Reggiardo. 1991. Chronic upper respiratory tract disease of free-ranging desert tortoises (Xerobates agassizii). Journal of Wildlife Diseases 27 9. Kinney ME, Lamberski N, Wack R, Foster R, Neely M, Tell L, Gehring R. 2014. Population pharmacokinetics of a single intramuscular administration of tulathromycin in adult desert tortoises (Gopherus agassizii). J Vet Pharmacol Ther. 2014 Oct; 37(5):500-7.

Mycoplasma in Testudines - Fact Sheet B10.06 European Association of Zoo and Wildlife Veterinarians - Transmissible Diseases Handbook 2019

10. Kolesnik E, Obiegala A, Marschang RE. 2017. Detection of Mycoplasma spp., herpesviruses, topiviruses, and ferlaviruses in samples from chelonians in Europe. J Vet Diagn Invest. 2017 Nov;29(6):820-832. 11. Lecis R, Paglietti B, Rubino S, Are BM, Muzzeddu M, Berlinguer F, Chessa B, Pittau M, Alberti A. 2011. Detection and characterization of Mycoplasma spp. and Salmonella spp. in free-living European tortoises (Testudo hermanni, Testudo graeca, and Testudo marginata). J Wildl Dis. 2011 Jul;47(3):717-24. 12. Salinas M, Francino O, Sánchez A, Altet L. 2011. Mycoplasma and herpesvirus PCR detection in tortoises with rhinitis- stomatitis complex in Spain. J Wildl Dis. 2011 Jan;47(1):195-200. 13. Silbernagel C, Clifford DL, Bettaso J, Worth S, Foley J. 2013. Prevalence of selected pathogens in western pond turtles and sympatric introduced red-eared sliders in California, USA.Dis Aquat Organ. 2013 Nov 25;107(1):37-47. 14. Wendland, L.D., D.R. Brown, P.A. Klein, M.B. Brown. 2006. Upper respiratory tract disease (Mycoplasmosis) in tortoises. In: Medicine and Surgery, D. Mader (ed.). Saunders, Elsevier Inc., Philadelphia, PA. Pp. 931-938. 15. Wimsatt J, Tothill A, Offermann CF, Sheehy JG, Peloquin CA. 2008. Long-term and per rectum disposition of Clarithromycin in the desert tortoise (Gopherus agassizii). J Am Assoc Lab Anim Sci. 2008 Jul;47(4):41-5. 16. Seimon TA, Horne BD, Tomaszewicz A, Pruvot M, Som S, In S, Sokha C, Platt S, Toledo P, McAloose D, Calle PP. 2017. Disease screening in southern river terrapins ( affinis edwardmolli) in Cambodia. J Zoo Wildl Med. 2017 Dec; 48(4):1242-1246.

Mycoplasma in Testudines - Fact Sheet B10.06