Clinical, virological and epidemiological characterization of an outbreak of Testudinid Herpesvirus 3 in a chelonian captive breeding facility: Lessons learned and first evidence of TeHV3 vertical transmission

Abstract

Testudinid herpesviruses (TeHVs) have a worldwide distribution among tortoises. However, information such as risk factors promoting the occurrence or the recrudescence of the associated disease and the mid-term sequelae of an outbreak comprising the extent and dynamic of the viral shedding have been only minimally investigated. Critical management information is also lacking or anecdotal. Furthermore, major aspects of the viral pathogenesis including the likelihood of vertical transmission of the virus are virtually unknown. The present study describes the occurrence and the management of an outbreak of Testudinid herpesvirus genotype 3 (TeHV3) in a large, private collection of chelonians. Clinical, pathological, molecular and serological characterization of the outbreak were carried out. Seventy-five percent of the infected tortoises died. Complementation of molecular and serological testing was a critical point for successful management implementations. A case-control study was performed to analyze possible risk factors associated with the infection. Furthermore, a subgroup of six asymptomatic infected tortoises was monitored for two consecutive seasons after the outbreak: all the infected tortoises were determined to be intermittent shedders, except one, which was a persistent shedder. Post-hibernation was associated with the highest number of shedders. Finally, evidence of the most likely vertical transmission of the virus was obtained for the first time.

Fig 1. Epidemic curve of the TeHV3 outbreak, April 2013-March 2014.

The curve was built using only the cases having clinical signs, for which it is possible to estimate an exact date of onset of the clinical signs. Bars represent longer periods of time that were cut in the figure. The pattern of the curve, with its irregular trend of cases reflecting the timing and extent of repeated exposures, is consistent with an intermittent source of infection. An estimation of the incubation period was attempted observing the gaps between the peaks of the curve that could represent tortoise-to-tortoise transmission events, followed by a possible incubation period. After the initial period, the outbreak waned, perhaps because of the successful and rapid implementation of control measures.

Fig 2. Tortoise no. 7: Oral cavity, glottis.

Mucosal erosion and ulceration with marked spongiosis (intercellular oedema). Note the presence of intranuclear amphophilic inclusions in the epithelial cells (arrows) associated with margination of the nuclear chromatin. H&E, 400X.