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  • Emerging and Contagious Diseases in Captive and Wild Chelonians

    by Heather A. Bjornebo, DVM, DABVP(Reptile-Amphibian Practice), CertAqV

    Introduction:

    The risk of spreading disease amongst both captive and wild populations continues to rise as tortoises and turtles continue increase in popularity in the pet trade. A number of important contagious diseases have already been identified and can cause significant morbidity and mortality in these species. A better understanding of these illnesses will allow better population management and more prompt initiation of appropriate veterinary intervention leading to improved animal care, survivability, captive breeding, and repopulation efforts. This article will discuss clinical signs of illness, prevention, and the diagnostic modalities available in confirming cause of illness and identifying carriers of contagious disease.

    Contagious diseases in chelonians can be broken up within 4 categories: bacterial, viral, internal parasites, and ectoparasites (external parasites).

    Bacterial Diseases:

    Mycoplasma spp.

    • Causes: Mycoplasma agassizii & M. testudinum
    • Species affected:
      • Terrapene spp.
      • Gopherus spp.
      • Testudo spp.
      • Geochelone spp.
      • Indotestudo spp.
      • Pyxis spp.
    • Clinical signs:
      • Upper respiratory tract disease
      • Conjunctivitis
      • Anorexia
      • Lethargy
    • Treatment:
      • Appropriate prescription antibiotics
      • Supportive care
      • Prognosis generally good
      • Choanal flushes
    • Treated animals remain lifelong carriers and recurrence of illness common, stress

    Pasteurella testudinis

    • Often associated with respiratory disease
    • May be found concurrently with Mycoplasma infections
    • Significance unknown
    • Affects Gopherus and Geochelone spp.

    Chlamydia & Chlamydiophila spp.

    • Obligate intracellular pathogens
    • Contagious to a number of vertebrate species
    • Zoonotic
    • Clinical signs
      • Upper and lower respiratory disease
      • Anorexia, lethargy
      • Inability to dive
      • Necrotic foci in the heart, spleen, and liver
      • Hepatic lipdiosis
    • Diagnosis – PCR
    • Treatment – supportive care and appropriate prescription antimicrobial therapy.
    • Prognosis – fair depending on severity of illness

    Salmonella spp.

    • Appears to be a component of the normal GI flora of reptiles
    • Zoonotic
    • Often asymptomatic
      • Has caused death in isolated cases in captive tortoises and turtles
    • Suspect opportunistic infection
    • Clinical signs
      • Emaciation
      • Erosions of the plastron
      • Sloughing scutes
      • Discolored carapace
      • Death
    • Diagnosis – culture
    • Treatment – supportive care and appropriate prescription antimicrobial therapy

    Borrelia  & Rickettsia spp.

    • Borrelia burgdorferi
      • Zoonotic – Lyme disease
      • Spread by ticks Ixodes spp. & Hyalomma aeyptium
      • Isolated from ticks on Testudo spp. in Europe
    • Borrelia turcica
      • No human cases documented
      • Spread by ticks Hyalomma aeyptium
      • Primary host is Testudo spp.
    • Rickettsia spp.
      • Zoonotic – spotted fevers and typhus
      • Spread by ticks Ixodes spp.
      • Isolated from ricks on Testudo spp. in Europe

    Viral Diseases:

    Herpesviruses

    • At least 12 herpesviruses identified that infect chelonians
      • Marine Turtles
        • Chelonid fibropapilloma-associated herpesvirus (ChHV-5)
        • Lung-eye-trachea disease virus (ChHV-6)
        • Loggerhead genital herpesvirus
        • Loggerhead orocutaneous herpesvirus
        • Greypatch Disease
      • Freshwater turtles
        • Emydidae – lethargy, anorexia, subcutaneous edema, hepatomegaly, pulmonary edema, hepatic necrosis
        • Chelidae & Pelomedusidae (Side-neck turtles) – ulcerative skin and shell
      • Tortoises
        • Testudinid herpesvirus 1, 2, 3, 4, and n (TeHV-1, -2, -3, -4, -n)
          • TeHV1 – Europe: Russian, pancake
            • low morbidity/mortality
          • TeHV2 – USA: desert tortoises
          • TeHV3 – Europe, USA, Africa: Testudo and Russian
            • high morb/mort
          • TeHV4 – Bowsprit tortoise
            • clinically healthy
          • TeHVn – leopard, pancake, Argentine, Russian, other…
    • Clinical signs:
      • Rhinitis
      • Conjunctivitis
      • Stomatitis
      • Glossitis
      • Diphtheroid membranes
      • Edema of the neck
      • CNS lesions
      • Hepatitis
      • Pneumonia
    • Diagnosis
      • PCR
      • Serology – latent infections
      • Virus isolation
      • Histopathology
    • Treatment
      • Prescription antivirals
        • Reduce virus replication in laboratory settings, limited success in patients
      • Considered carriers for life
    • Disinfection
      • 10% bleach
      • Inactive in environment after 24 weeks
        • Sun more quickly

    Adenoviruses

    • Increasing cases reported since 2009
      • Documented cases in
        • Red-foot tortoises
        • Leopard tortoises
        • Ornate box turtles
        • Sulawesi tortoises
        • Impressed tortoises
        • Burmese star tortoises
    • Transmission – fecal oral or direct contact
      • Disease most often seen in immunocompromised or young individuals
      • Concurrent disease common
      • Results in: Hepatitis, Enteritis, Esophagitis, Splenitis, Encephalopathy
    • Clinical signs
      • Sudden death
      • Anorexia
      • Lethargy
      • Mucosal ulceration
      • Palatine erosions of the oral cavity
      • Nasal and ocular discharge
      • Diarrhea
      • Adenoviruses
    • Diagnosis
      • PCR
      • Histopathology
    • Treatment – very limited success
      • Mortality rate in Sulawesi tortoises was 87.6%
      • Poor prognosis
      • Recovered animals asymptomatic carriers for life (Red-foot tortoises)
    • Environmentally persistent and disinfection challenging

    Iridoviruses/Ranaviruses

    • Highly contagious cause of morbidity and mortality with increasing cases worldwide since 2003
    • Clinical disease has been described in
      • Hermann’s tortoises
      • Gopher tortoises
      • Soft-shelled turtles (“Red-neck disease”)
      • Eastern box turtles
      • Florida box turtles
      • Red-eared sliders
      • Burmese star tortoises
    • Mechanism of transmission unknown
      • Observed in wild and captive populations in the US and Europe
    • Clinical signs
      • Upper respiratory tract disease
      • Respiratory distress
      • Nasal discharge
      • Oral ulceration
      • Cutaneous abscessation
      • Subcutaneous edema
      • Anorexia
      • Lethargy
      • Red skin lesions (soft-shelled turtles)
      • Conjunctivitis
      • Cellulitis of the neck
    • Diagnosis
      • PCR analysis
        • Needs to be specific and sequencing important as false positives can occur from insect viruses
    • Treatment – limited success

    Paramyxoviruses

    • Well documented cause of disease in snakes
      • Fewer cases documented in tortoises
      • 2013 study of prevalence in Europe and Madagascar
        • 202 tortoises from 6 countries and 9 different species – 5.5% had antibodies
        • Spain and UK had highest percentage at ~10% positive
    • Clinical signs
      • Lethargy
      • Rhinitis
      • Conjunctivitis
      • Emaciation
      • Respiratory distress
      • Death

    Picornaviruses

    • First detected in juvenile Testudo spp. Tortoises in Europe and Sulawesi tortoises in 2014.
      • Previously referred to as “Virus X”
    • Clinical signs: Soft shells, kidney disease, and death
    • Little is known at this point about transmission
      • Koch’s postulates recently experimentally fulfilled
    • Often mistaken for Nutritional Secondary Hyperparathyroidism
      • Metabolic Bone Disease

    Internal Parasites:

    Cryptosporidium spp.

    • Most commonly recognized in snakes and lizards
      • Being reported with increasing frequency in chelonians
        • Sonoran desert tortoises
        • Indian star tortoises
        • Pancake tortoises
        • Russian tortoises
        • Radiated tortoises
        • Gopher tortoises
        • Indotestudo spp  and Testudo spp.
      • Italy, Germany, Spain, Switzerland, Czech Republic, Ghana, Australia, & US
    • Suspect transmission similar to that of Cryptosporidium in other host species – Highly contagious!
    • Clinical Signs
      • Chronic Diarrhea
      • Decreased appetite
      • Pica
      • Decreased growth rate
      • Weight loss
      • Lethargy
      • Softer than normal shells in juveniles
      • Passing undigested feed
    • Diagnosis
      • PCR with sequencing
      • Acid Fast examination of fecal smears
    • Treatment
      • Currently no data for treatment in chelonians
        • Paromomycin (Rx) shows promise in some reptile species but all recovered individuals should be considered asymptomatic carriers
    • Disinfection
      • Resistant to disinfection
      • Temperatures greater than 150F (steam or flame thrower)
      • Formalin (10%)
      • Glutaraldehyde (2.65%)
      • Ammonia (5-10%)
      • Rescue Disinfectant at 1:16 for 15 minutes

    Intranuclear Coccidiosis

    • First identified in 1990
      • Clinical disease has been described in a number of species
        • Radiated tortoises
        • Impressed tortoises
        • Leopard tortoises
        • Forsten tortoises
        • Bowsprit tortoises
        • Spider tortoises
        • Galapagos tortoises
        • Flat-tailed tortoises
        • Eastern box turtles
        • Arakan forest turtles
        • More…
    • Reported in US and Germany
    • Most commonly occurs in captive tortoises
    • Life cycle and route of transmission not fully understood
    • Morbidity and mortality variable within groups
    • Clinical signs – non-specific/variable
      • Anorexia
      • Lethargy
      • Lack of normal diurnal behavioral patterns
      • Increased respiratory effort
      • Mouth breathing
      • Rapid weight loss or gain
      • Mild conjunctival or nasal erythema
      • Ocular or nasal discharge
      • Gasping
      • Subcutaneous edema
      • Ulceration of the cloacal mucosa
      • Death can occur within days of clinical signs or after months of treatment
    • Stress and thermoregulatory changes enhance progression of disease
    • Reduced immune response
    • Animals that recover with treatment become asymptomatic carriers
    • Diagnosis
      • Identification by cytologic examination of nasal discharge
      • Biopsy and histologic examination of affected tissues
      • Quantitative PCR on swabs of the conjunctiva, oral and choanal mucosa, and cloaca
    • Treatment
      • Focused on optimal husbandry
      • Isolation
      • Supportive care
      • Hospitalization
      • Prescription coccidiostats
    • Prognosis
      • Guarded to poor as even recovered individuals may have permanent organ damage and succumb months after treatment

    Hexamita spp.

    • Contagious flagellated protozoal parasite that effects the digestive and urinary tracts, including the kidneys, and liver.
    • Parasite invades kidneys causing damage to the filtration apparatus (glomeruli and renal tubules)
      • Affected kidneys are enlarged and pale
      • Leads to kidney failure and death
    • Documented in cases in numerous freshwater turtle and tortoise species.
    • Most common cases in practice seen in recently imported Russian Tortosies
    • Clinical Signs
      • Failure to thrive
      • Anorexia
      • Weight Loss
      • Death
    • Treatment
      • Prescription antiprotozoals
      • Supportive Care
      • Environmental decontamination
      • Cleansing feces off shells to prevent reinfection
    • Prognosis depends on degree of damage to the kidneys prior to treatment

    Nematodes & Trematodes

    • Nematodes – Hookworms, Roundworms
    • Trematodes – Flukes
    • Clinical signs non-specific
    • Treatment – Prescription antiparasitics

    Ectoparasites:

    Ticks & Mites

    • Vectors for other diseases
    • Anemia with high parasite loads
    • Treatment
      • Antiparasitics – not ivermectin!
      • Physical Removal
    • Prevention

    Disease Prevention:

    • Establish effective quarantine protocols.
    • Decontamination and disinfection is very important.
    • Careful animal health monitoring
      • Annual veterinary examinations
      • Fecal parasite screenings
      • PCR screenings

    Conclusion:

    Diseases in turtles and tortoises are emerging and popularity of these species are increasing. Understanding the prevalence of these diseases both in natural and captive populations is important in preventing the spread of disease between and within collections.

    References:

    •Braun, J. et. al. Molecular methods to detect Mycoplasma spp. and Testudinid herpesvirus 2 in desert tortoises (Gpherus agassizii) and implications for disease management. Journal of Wildlife Diseases. 2014. 50(4): 757-766.

    •Gibbons, PM. And ZJ Steffes. Emerging Infectious Diseases of Chelonians. Vet Clin Exot Anim. 2013. 303-317.

    •Hepner, S. et. al. First investigations on serum resistance and sensitivity of Borrelia turcica. Ticks and Tick-borne Diseases. 2019. 10(5): 1157-1161.

    •Heuser, W, et. al. 2014. Soft plastron, soft carapace with skeletal abnormality in juvenile tortoises. Histopathology and isolation of a novel picornavirus from Testudo graeca and Geochelone elegans. Tierärztliche Praxis. Ausgabe K, Kleintiere/Heimtiere. 42. 310-20. 10.1055/s-0038-1623777.

    •Kar, S. et. al. Presence of Zoonotic Borrelia burgdorferi sl. and Rickettsia spp. in Ticks from Wild Tortoises and Hedgehogs. Journal of Marmara University Institute of Health Sciences. 2011. 1(3):166-170.

    •Origgi, FC. Testudinid Herpesviruses: A Review. Journal of Herpetological Medicine and Surgery. 2012. 22(1):42-54.

    •Origgi, FC. et. al. A genomic Approach to Unravel Host-pathogen Interaction in Chelonians: The Example of Testudinid Herpesvirus 3. PLoS ONE. 2015. 10(8):e0134897. doi:10.1371/journal.pone.0134897

    •Ng TF, Wellehan JF, Coleman JK, et al. 2015. A tortoise-infecting picornavirus expands the host range of the family Picornaviridae. Arch Virol. 160(5):1319–1323.

    •Reavill, DR, and RE Schmidt. 2010. Urinary Tract Diseases of Reptiles. Journal of Exotic Pet Medicine. 19(4): 280-289.

    •Rideout, B. Transmissible Infections and Desert Tortoise Translocation: A Comprehensive Disease Risk Analysis. A report of the U.S. Fish and Wildlife Service. June 2015.

    •Rosler, R. et. al. Detection of antibodies against Paramyxoviruses in tortoises. J Zoo Wildl Med. 2013. 44(2): 333-339.

    •Papp, T. et. al. Paramyxovirus infection in a leopard tortoise (Geochelone pardalis babcocki) with respiratory disease. Journal of Herpetological Medicine and Surgery. 2010. 20(2-3):64-68.

    •Johnson, AJ, et. Al. 2008. RANAVIRUS INFECTION OF FREE-RANGING AND CAPTIVE BOX TURTLES AND TORTOISES IN THE UNITED STATES. Journal of Wildlife Diseases. 44(4):851-863.

    •Stilwell, JM, et. al.  “EXTENSION OF THE KNOWN HOST RANGE OF INTRANUCLEAR COCCIDIOSIS: INFECTION IN THREE CAPTIVE RED-FOOTED TORTOISES (CHELONOIDIS CARBONARIA),” Joural of Zoo and Wildlife Medicine 48(4), 1165-1171.

    •Wellehan, JFX, et al. 2005. Reptile virology. Veterinary Clinics: Exotic Animal Practice. 8(1):27-52.

    •Zwart, P, and Truyens, EHA. 1975. Hexamitiasis in Tortoises. Veterinary pathology. 1:175-183.

  • Cerenia – What is it and why is it used so wildly in veterinary medicine?

    Maropitant (a.k.a Cerenia)

    Cerenia, generically known as Maropitant, is a neurokinin-1 receptor antagonist. It mediates effects of central and peripheral substance P, an excitatory neurotransmitter and is in a class of peptides known as neurokinins. Substance P binds neurokinin-1 receptors which are G protein coupled receptors. As an antagonist, maropitant and others like it, blocks the action of substance P.

    Where are neurokin-1 receptors located?

    They are located in the central nervous system, heart and blood vessels, genitourinary system, immune system , and gastrointestinal tract.

    What are the effects of Cerenia in the body?

    These neurokin-1 receptors are involved in blood cell production, wound healing, neurogenic inflammation, cell survival, cell proliferation, pain transmission, endocrine and paracrine secretions, dilation of blood vessels. They are involved with neuronal transmission associated with depression, stress. Cerenia antagonizes the affects in these areas as well as acts on two areas in the central nervous system to stop vomiting: area postrema and nucleus tractus solitaries.

    So if rabbits and rodents cannot vomit, why is it often used in exotic companion mammals?

    While the anti-vomiting effects in rabbits and rodents not seem as important since they cannot vomit, it does not necessarily mean they cannot feel nausea. Efficacy of maropitant for preventing vomiting is also associated with pmotion sickness in dogs where it blocks final common pathway in the vomiting center of the brain. Studies showed it was very effective in preventing vomiting in dogs premedicated with hydromorphone, an opioid drug often associated with nausea and vomiting in patients. There are reports on Veterinary Information Network as well about its use with rabbits during head tilt and it is thought to maybe be helpful to reduce nausea from vestibular disease. It is also used in ferrets and birds as an anti-regurgitation drug.

    What about its use in pain control?

    As a neurokinin-1 receptor antagonist, Maropitant has shown to reduce anesthetic requirements of dogs undergoing surgery and can be used to reduce visceral pain. In rabbits, Maropitant reduced the viscerosensory response caused by colorectal distention and it is often in rabbits and guinea pigs as pain control for gastrointestinal stasis.

    It also has anti-itch effects!

    Since neurokinin-1 receptors are involved in mediating some itch pathways. Substance P is found in nerve fibers in the skin and it plays a significant role in the nerve pathways that are involved in inchiness. antagonizing, or blocking these pathways, can be helpful to reduce itch. Studies have shown similar drugs reducing itch in humans and Maropitant signficantly reduced the itchiness of ulcerative dermtitis lesions in mice.

    It can also reduce the creation of abdominal adhesions forming after surgery!

    Antagonizing neurokinin 1 receptors decreases postoperative adhesion formation and increases peritoneal fibrinolytic activity. Research in a rat model with the use of a neurokinin-1 receptor antagonist (NK-1RA) was found to decrease postoperative peritoneal adhesion formation by up to 53% at higher doses studied compared to saline controls. This research indicated that the antagonist used blocked the binding of substance P to neurokinin receptors. Left unblocked, substance P is proinflammatory and results proliferation of scar tissue and stimulates excessive blood vessel formation. Furthermore, antagonism appears to increase expression of tissue-type plasminogen activator an important enzyme in the production of plasmin, a protein that breaks down fibrin and scar tissue production. Research in rabbits has shown that intestinal adhesions can be reduced compared to controls when tissue-type plasminogen activator is given intraperitoneally.

    But wait… there’s more… how about in respiratory disease

    Maropitant has been used to treat canine chronic bronchitis. Substance P acts on the neurokinin-1 receptor in airway inflammation and the cough reflex. Antagonizing substance P showed a significant decrease in cough frequency and severity but no change in inflammation.

    So are their side effects for Maropitant we should consider?

    Some recommend not giving for more than 5 days in a row since the enzyme responsible for its metabolism, CYP2D15, becomes saturated. It should also be used with caution with highly protein bound drugs as these drugs compete with Maropitant for protein binding and there can be increases in unbound Maropitant in the blood. Also it should be used with caution with calcium channel antagonists as maropitant has an affinity for Ca and K channels. Excessive use may also decrease intestinal motility and it induced intestinal motility disorder in mice.