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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 Turtles
Terrapene 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
Proboscivirus
Cytomegalovirus
Muromegalovirus
Roseolovirus
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 turtles
Turtle 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

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Frog virus 3 in eastern box turtles: agents seen with coinfections