Shell Lesions Associated With Emydomyces testavorans Infection in Freshwater Aquatic Turtles

Abstract

A newly described onygenalean fungus, Emydomyces testavorans, has been isolated from ulcerative shell and skin lesions of freshwater aquatic chelonians. To investigate the shell lesions associated with infection and determine if any lesional features were unique to E. testavorans, tissues from turtles housed in zoological institutions ( n = 45) in the United States and free-living turtles ( n = 5) submitted for diagnostic biopsy or necropsy were examined. Free-living turtles were from geographically distinct habitats in Florida ( n = 1) and Washington ( n = 4) at the time of sampling. Histologic shell sections were evaluated for the presence or absence of specific lesional features. Infection with E. testavorans was evaluated in all cases by screening GMS (Grocott-Gomori’s methenamine silver)-stained histologic sections for the presence of morphologically consistent fungi and by quantitative PCR (polymerase chain reaction) on representative frozen tissue or formalin-fixed paraffin-embedded sections. Additionally, culture was performed for 15 cases with available fresh/frozen tissue. In total, there were 17 PCR-confirmed E. testavorans cases, 29 cases with morphologically consistent fungi on GMS-stained sections, and 21 cases of shell lesions without histologic or molecular evidence of E. testavorans infection. Epithelial inclusion cysts, defined as cystic structures within the dermis lined by keratinized stratified squamous epithelium and containing necrotic bone and keratin debris, were significantly ( P < .01) associated with E. testavorans infection. Other significantly associated shell lesions included squamous metaplasia, hyperkeratosis, inflammation, and osteonecrosis ( P < .05). This study identified characteristic shell lesions associated with E. testavorans infection. Further studies to prove causality are needed.

Major Emerging Fungal Diseases of Reptiles and Amphibians

“…had only been reported in captive lizards until 2020; detection in symptomatic wild Australian lizards has since been a major cause of concern given the trajectory of global emergence seen with Oo . With new pathogenic members of the Onygenales order being discovered, most recently in aquatic turtles in the United States [ 13 , 187 ], surveillance of fungal pathogens of reptiles and amphibians is paramount, and control measures aimed at preventing geographic spread and spillover between captive and wild populations need to be urgently enhanced [ 106 , 186 ].…”

Bioencapsulation is a feasible method of terbinafine administration in Emydomyces testavorans-infected western pond turtles (Actinemys marmorata)

“…concentration (MIC) data for ET. 2,5,13 Broth dilution terbinafine susceptibility testing from 3 clinical ET isolates has demonstrated MICs between 15 and 60 ng/mL. 2 However, oral medication administration in chelonians can be challenging due to the ability of individuals to pull their heads into their shells and the challenges associated with manually opening their beaks.…”

“…1,2 There is currently a strong association between ET and ulcerative shell disease, resulting in morbidity and mortality. [2][3][4][5] To date, infection has been confirmed in a wide variety of chelonians under human care, including the western pond turtle (Actinemys marmorata). 2,[4][5][6][7] Western pond turtles are classified as vulnerable or endangered across their home range and are designated as a priority species for conservation under the Association of Zoos and Aquariums (AZA) Saving Animals From Extinction (SAFE) program.…”

“…[2][3][4][5] To date, infection has been confirmed in a wide variety of chelonians under human care, including the western pond turtle (Actinemys marmorata). 2,[4][5][6][7] Western pond turtles are classified as vulnerable or endangered across their home range and are designated as a priority species for conservation under the Association of Zoos and Aquariums (AZA) Saving Animals From Extinction (SAFE) program. [8][9][10] While Bioencapsulation is a feasible method of terbinafine administration in Emydomyces testavorans-infected western pond turtles (Actinemys marmorata…”

Estado sanitario de tortugas dulceacuícolas de la familia <i>Chelidae</i> en arroyos pampásicos de llanura y serranos con distinto impacto de contaminación

“…En el proceso están implicadas una variedad de bacterias Gram negativas, e incluso podría existir una relación sinérgica entre ellas. En estudios recientes se logró aislar varias especies de hongo asociadas a ulceraciones caparaciales en tortugas cautivas y silvestres de distintas especies (Woodburn et al 2019, Woodburn et al 2021. Sin embargo, no habría un consenso claro acerca de si la SCUD es un estado avanzado que se inicia con la presencia de úlceras en el caparazón o si se trata de dos patologías diferentes (Granados et al 2013).…”