Frog Virus 3 in Eastern Box Turtles: Agents seen with Coinfections

James F.X. Wellehan Jr., DVM, PhD, DACZM, DACVM (Virology, Bacteriology/Mycology), Natalie H. Hall, DVM,

DACZM, Gregory J Fleming, DVM, DACZM, April L. Childress, Scott P. Terrell, DVM, DACVP

North American Box TurtlesTerrapene sp.

• Low Fecundity• Low Juvenile Survival Rate• Long Lifespan• Cryptic• Frog Virus 3 Mortality Events Well

Documented

Coinfections

• Koch’s Postulates easily misinterpreted as dichotomous pathogen/nonpathogen

Host

Pathogen Environment

Coinfections

• Coinfections with Rotavirus and other enteric pathogens are synergistic (Bhavnani et al, 2012)

• Coinfections with Marek’s disease and Cryptosporidium baileyi in chickens synergistic (Abbassi et al, 2000)

Iridoviruses

• Enveloped, but infective without envelope– Stable in environment

• Cytoplasmic• Less host specific than herpes/adeno

Iridoviruses

• Genus Ranavirus– Signs:

• Stomatitis,Hepatitis, Splenitis,Enterocolitis– Frog Virus 3 is the best studied pathogen of

box turtles• Also found in amphibians,sturgeon, other

turtles.

Eastern Box Turtles

• Confiscated• Placed at quarantine of large well-run zoo• High mortality rate• 8 turtles submitted for testing

Herpesviruses

• Enveloped virus, not stable in environment• Diverse, coevolved with hosts

– Often high infection rates in endemic hosts– 8 species endemic in one primate species

• Intranuclear• Latency

– Typically infected for life• One genus reported in turtles- Scutavirus

Box Turtle Scutaviruses

• Terrapene HV1– Seen in Eastern Box Turtles– Commonly seen in coinfections with Frog Virus 3– Role in disease under investigation

• Terrapene HV2– Seen in Eastern Box Turtle– Identified in fibropapillomatous lesion

Scutavirus

Iltovirus

Simplexvirus

Varicellovirus

ProboscivirusCytomegalovirusMuromegalovirusRoseolovirus

Lymphocryptovirus

Rhadinovirus

Percavirus

Macavirus

Mardivirus

Adenoviruses

• Non-enveloped– Very stable in environment

• Intranuclear• Diverse, coevolved with hosts

– 6 species endemic in one primate species– Generally host specific, may jump to close

relatives• Eublepharid AdV1 - leopard & fat tailed geckos,

Helodermatid AdV2 – Gila monsters & Pogona

Adenoviruses

• Novel chelonian genus– Box turtles, Red eared sliders, Pancake tortoises– Signs:

• Depression, weight loss

Siadenovirus

Aviadenovirus

Mastadenovirus

Atadenovirus

Novel Turtle Genus

Ichtadenovirus

Tenericutes

• Important bacterial phylum• Mycoplasma, Ureaplasma, Acholeplasma

– Have lost cell wall– More difficult to grow– Dependent on host cells– Range from relatively benign to significant

pathogens• Not beneficial

Mycoplasma

• Mycoplasma sp.– Associated with upper respiratory disease in

box turtles– First reported by Feldman et al, 2006– Distinct from M. agassizii seen in Gopherus sp.– Additional species recently discovered, clinical

significance still under investigation

Confiscated turtlesTurtle Ranavirus Herpes Adeno Mycoplasma

1 - TerHV1 Ornate BTAdV1 Mycoplasma sp. BT

2 - TerHV1 Ornate BTAdV1 Mycoplasma sp. BT

3 - TerHV1 Ornate BTAdV1 Mycoplasma sp. BT

4 FV3 TerHV1 Ornate BTAdV1 Mycoplasma sp. BT

5 - - Ornate BTAdV1 Mycoplasma sp. BT

6 FV3 - Ornate BTAdV1 Mycoplasma sp. BT

7 FV3 - Ornate BTAdV1 Mycoplasma sp. BT

8 - - Ornate BTAdV1 Mycoplasma sp. BT

Future Directions

• Quantitative assays for measurement of agent loads

• Surveillance of wider populations

Thanks