Zoonoses in Exotic Species
American Association of Zoo Veterinarians Conference 2008
R. Scott Larsen, DVM, MS, DACZM
Wildlife Health Center and Department of Medicine & Epidemiology, University of California, Davis, CA

 Roughly 75% of emerging infectious diseases are of zoonotic origin

 The CDC has authority under the Public Health Service Act to prohibit importation of animals and animal products. They also have the authority to regulate foreign quarantine in order to prevent introduction of zoonoses.

 Currently banned: Non-human primates, African rodents, civets, and Asian birds

 Protect the public against: Ebola virus, Simian Immunodeficiency Virus, monkey pox, Sudden Acute Respiratory Syndrome virus, and avian influenza

 Compendium of Measures to Prevent Disease Associated with Animals in Public Settings7

 Hand washing is the single-most important prevention step

 Education of owners regarding risk of disease transmission

Zoonoses of Domestic Rabbits and Rodents

Despite the recent outbreak of monkey pox in pet rodents, overall there have been relatively few zoonotic diseases documented to have been transmitted from pet rabbits or rodents.2,4 The most common causes of disease from these species are infections from animal bites and immunologic reactions to rabbit scratches.2,4 Cutaneous and respiratory allergies are common and are incited by exposure to dander, salivary, or urinary proteins. Owners can try to reduce exposure to allergens by minimizing animal handling (particularly direct contact), by housing the animal on newspaper for easy cleaning and disposal, and by using room air-filtration systems.2

Monkey Pox Virus

African rodents appear to be the most likely natural hosts of monkey pox. The disease can affect primates, rodents, and lagomorphs, although some rodents are asymptomatic. In people, it is characterized by rashes that are similar to those of smallpox, along with fever, headache, backache and lymphadenopathy. The 2003 U.S. outbreak was associated with prairie dogs that had contracted monkey pox from imported African rodents.8 Affected prairie dogs developed necrotizing bronchopneumonia, conjunctivitis, and tongue ulceration.3 In mid-2008, in order to help stop the spread of monkey pox, prairie dogs and African rodents were prohibited from sale or interstate commerce. This ban became permanent in late 2003 and made it illegal to collect prairie dogs from the wild for the purposes of keeping them in captivity.

Lymphocoriomeningitis (LCM) virus

The LCM virus is found in many rodent species and the natural host is the domestic mouse, which is usually an asymptomatic carrier.2 The virus spreads among rodents via saliva, urine, and feces; it can also be transmitted vertically. Mice infected in the embryo develop persistent infections and shed the virus most of their lives.2 LCM can spread to people via direct contact, rodent bites, or aerosolization. Outbreaks of disease in people have been associated with pet hamsters, as species that is usually asymptomatic. People may develop flu-like signs with fever and headache. Rarely patients may develop aseptic meningitis or meningoencephalitis. Infection during pregnancy may result in abortion. Because of the risk of LCM virus infection, representatives of the CDC have recommended against pregnant women and immunocompromised people owning pet rodents.1

Pasteurella multocida

Pasteurella organisms are carried commonly by rabbits and may infect wounds inflicted by rabbit bites or scratches.4 Some people have a stronger immunologic reaction to this organism, and these individuals develop swelling, erythema, and pruritis. Wounds inflicted by rabbits should be thoroughly washed and disinfected; in some cases, wounds may require antibiotics. Elimination of Pasteurella in rabbits is not feasible, due to the high prevalence of infection and environmental exposure. In rabbits, Pasteurella may cause abscesses, respiratory infections, or other diseases.

Francisella Tularensis

Tularemia is most commonly found in wild rabbits, although domestic rabbits can also be affected. Tularemia is often transmitted by tick or flea bits, so flea and tick control are important, particularly for rabbits housed outdoors.

Dermatophytes

There are multiple species of fungal organisms that may cause dermatophytosis, but the most common skin fungal pathogen of both rabbits and rodents is Trichophyton mentagrophytes. Infections with Microsporum spp. also sometimes occur. Affected animals typically have dermatologic lesions such as scaling; sub-clinical infections occasionally occur.9 Diagnosis of dermatophytosis can be made by direct microscopy of wet-mount microscopy of hair or flaked skin. Some dermatophytes fluoresce when a Wood's lamp is used.4 Positive identification may be achieved using fungal culture. Animals suspected of dermatophytosis should be handled with gloves and direct contact should be avoided. There should be good environmental sanitation and the animals should be carefully monitored to insure complete disease resolution.

Mites

Sarcoptes sp. of rodents can infect humans and cause intense itching. The rabbit fur mite, Cheyletiella parasitovorax, can also infect humans, causing a pruritic, papular dermatitis on the thorax, abdomen, arms, and thighs. Rabbits infected with Cheyletiella may be asymptomatic, have mild clinical signs, or have severe alopecia with erythema, scaling and pruritis. Lesions often involve hair loss and a scaly, oily dermatitis. Diagnosis in rabbits may be performed by skin scraping. The life cycle of Cheyletiella is 35 days, with adult females and eggs surviving off the host for up to 10 days.2 Treatment of both the affected rabbit and the environment is needed; this may be accomplished using carbaryl, permethrin, or pyrethrin-based ectoparasiticides.4 Ivermectin has been used successfully to resolve Cheyletiella in rabbits, although many practitioners now prefer the use of selamectin as it is longer-acting and is applied topically. Fipronil is not recommended for rabbits due to severe adverse side effects, including dramatic neurologic disease.

Other organisms of potential zoonotic importance are Balantidium (guinea pigs), tapeworms (hamsters and gerbils), Yersinia pseudotuberculosis (rabbits), and Salmonella spp. (all species).2,4

Zoonoses of Domestic Ferrets

Influenza

Influenza is the major zoonotic disease of ferrets, with documented ferret-to-human disease transmission.6 Both ferrets and humans are susceptible to influenza types A and B. People with severe colds or influenza-like symptoms should avoid direct or indirect contact with pet ferrets. Ferrets with influenza may develop conjunctivitis, nasal discharge, sneezing, fever, and anorexia4 in some cases, they may develop pneumonia. Symptomatic and supportive care is warranted; antibiotics may be given to minimize secondary infection of the respiratory tract. As in humans, the most effective preventive treatment for ferrets is elimination of contact with potential sources of infection - including infected people and other ferrets.

Other organisms that may be carried by ferrets that have the potential to cause disease in people include Campylobacter, Helicobacter, Listeria, Mycobacterium avium, M. bovis, M. tuberculosis, Salmonella, Microsporum, Trichophyton, Ancylostoma caninum, Cryptosporidium, Dipylidium caninum, Dirofilaria immitis, Giardia, Sarcoptes scabiei, Toxocara, and rabies virus.

Zoonoses of Captive Primates

TNTC (Too Numerous To Count)

Zoonoses of Birds

Chlamydophila Psittaci

Psittacines, passerines, and columbiformes may all carry and transmit Chlamydophila psittaci. Birds may be asymptomatic or acutely ill. Birds with clinical disease from Chlamydophila often have leukocytosis and may have elevations in aspartate aminotransferase (AST). Radiographs may demonstrate an enlarged spleen or indistinct air sacs (air sacculitis), but neither finding is patho-pneumonic for Chlamydophila infection. Polymerase chain reaction (PCR) is a very useful tool in determining whether a bird is shedding Chlamydophila organisms; samples may be taken, using a single swab, from the conjunctiva, choana, and cloaca (in that order). Other diagnostics tests should as ELISA and elementary body agglutination assays may also be used to evaluate infection status. Treatment of birds for chlamydiosis requires a 6-week course of an appropriate antibiotic. Tetracyclines are typically used to treat chlamydiosis. There are many different tetracycline preparations that may be used, depending on the circumstances. For individual birds, the use of a long-acting (once per week) injectable tetracycline can be very useful. Quaternary ammonia compounds can be used to eliminate environmental organisms.

Mycobacterium Avium-complex and Mycobacterium Genavense

There are four organisms within the M. avium-complex: M. avium avium; M. a. hominissuis; M. a. paratuberculosis;and M. a. silvaticum.Historically, sub-speciation has been uncommon so most human infections have been diagnosed as M. avium-complex. Before 1981, there were <3,000 worldwide M. avium-complex infections in people per year, and these were mostly immunocompromised patients (organ transplants, leukemia, etc.).5 In humans, disseminated M. avium-complex infection most commonly occurs late in the course of disease of patients with acquired immune deficiency syndrome (AIDS).5 Now, about 40% of AIDS patients will develop M. avium complex if not given preventative treatment. Clinical signs of M. avium-complex in people include fever, weight loss and anemia. For most people, the source of infection is most likely environmental (food, water, soil) via ingestion.5

M..avium-complex and M. genavense are unlikely to be a health risk to people with normal immune systems, but those that are immunocompromised are likely at increased risk. The CDC does not list pet bird contact as a possible risk for infection with M. avium-complex. There are occasional reports of infection in people that are not immunocompromised - usually due to overwhelming exposure such as water vapor from hot tubs.5

Mycobacterial infections appear to be the particularly common in gray-cheeked parrots and African gray parrots.4 Birds with clinical mycobacteriosis typically have a persistent leukocytosis, wasting or other gastrointestinal signs, caseous nodules, non-specific lameness (bone lesions), or granulomas. Swabs of lesions may be acid-fast stained for diagnosis, but this in relatively insensitive requiring high numbers of organisms. Mycobacterial culture and PCR can be used to identify infection as well, although culture typically requires several weeks.

There is considerable discussion about treating birds for Mycobacterial infection. Concerns exist about zoonotic transmission and potential creation of drug-resistant strains.

Salmonella

The risk of contracting Salmonella from pet birds seems to be quite low. Salmonella is discussed more extensively in regard to reptiles.

Avian Influenza

The risks of contracting avian influenza (particularly highly pathogenic AI (HPAI)) from pet birds in North America currently appear to be very small. Respiratory and/or gastrointestinal disease in birds would be expected.

Zoonoses of Reptiles

Always wash hand well after handling any patient, but reptiles in particular. Disposable gloves are often recommended. Any reptile scratches or bites should be washed and disinfected thoroughly, as infection with gram-negative organisms is likely (Proteus, Pseudomonas, Klebsiella, Aeromonas). People can be infected with pentastomids (Armillifer spp.) from exposure to snake feces, but these infections are typically asymptomatic.2

Salmonella

Most reptiles should be considered carriers or potential carriers of Salmonella. Some practitioners advocate performing fecal or cloacal cultures to test for Salmonella. However, Salmonella can be intermittently shed, so even serial cultures can have false-negative results. Along the same lines, it is questionable as to whether reptiles can be definitively cleared of Salmonella if treated and re-infection from the environment is also possible. Salmonella strains can be nonpathogenic to the reptile host, but may be pathogenic to human handlers. Owners of pet reptiles should be given information about the possibility of Salmonella, with pertinent information regarding risks to children and immunocompromised individuals. Salmonella may cause a range of symptoms in people, from mild gastrointestinal disease to life-threatening sepsis. Red-eared slider turtles that are < 4 inches long have banned for commercial distribution within the U.S. since 1975.2 Recent research has developed techniques to eliminate Salmonella on the egg shell, thus theoretically being able to provide a Salmonella-free turtle. As a result, legislation has been introduced into Congress petitioning to lift the ban on the sale of small red-eared sliders. To date this ban has not been lifted.

References

1.  Center for Disease Control. Lymphocytic choriomengitis (LCMV). http://www.cdc.gov/ncidod/dvrd/spb/mnpages/dispages/lcmv.htm. Accessed 1 September 2008.

2.  Chomel, B.B. 1992. Zoonoses of household pets other than dogs, cats and birds. Ped. Infect. Dis. J. 11: 479-487.

3.  Guarner, J., B.J. Johnson, C.D. Paddock, W.J. Shieh, C.S. Goldsmith, M.G. Reynolds, I.K. Damon, R.L. Genery, S.R. Saki, Veterinary Monkeypox Virus Working Group. 2004. Monkeypox transmission and pathogenesis in prairie dogs. Emerg. Infect. Dis. 10(3): 426-431.

4.  Johnson-Delaney, C.A. 1993. Potential zoonoses from nontraditional pets with particular attention to the immunosuppressed pet owner. J. Small Exotic Anim. Med. 2(2): 103-111.

5.  Lennox, A.M. 2007. Mycobacteriosis in companion psittacine birds: a review. J. Avian Med. Surg. 21(3): 181-187.

6.  6. Marini, R.P., J.A. Adkins, and J.G. Fox. 1989. Proven or potential zoonotic diseases of ferrets. J. Amer. Vet. Med. Assoc. 195: 990-994.

7.  National Association of State Public Health Veterinarians. 2007. Compendium of Measures to Prevent Disease Associated with Animals in Public Settings, 2007. http://www.nasphv.org/Documents/AnimalsInPublicSettings.pdf

8.  Reed, K.D., J.W. Melski, M.B. Graham, R.L. Genery, M.J. Sotir, M.V. Wegner, J.J. Kazmierczak, E.J. Stratman, Y. Li, J.A. Fairley, G.R. Swain, V.A. Olson, E.K. Sargent, S.C. Kehl, M.A. Frace, R. Kline, S.L. Foldy, J.P. Davis, and I.K. Damon. 2004. The detection of monkeypox from humans in the Western Hemisphere. N. Engl. J. Med. 350(4): 342-350.

9.  Vangeel, I. F. Pasmans, M. Vanrobaeys, P. De Herdt, and F. Haesebrouck. 2000. Prevalence of dermatophytes in asymptomatic rabbits and guinea pigs. Vet. Rec. 146: 440-441.

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

R. Scott Larsen, DVM, MS, DACZM
Wildlife Health Center
and Department of Medicine & Epidemiology
School of Veterinary Medicine
University of California-Davis
Davis, CA, USA


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