Introduction

A zoonotic disease or zoonosis (plural zoonoses) is defined as a disease that can be transmitted between non-human animals and humans. Zoonoses can be further classified by their epidemiology:

  Anthropozoonosis - a zoonosis maintained in nature by non-human animals that is transmissible to humans, i.e., rabies and brucellosis.²

  Zooanthroponosis - a zoonosis maintained by humans that can also infect animals; also called a reverse zoonosis, i.e., protozoal infection in pets, tuberculosis in cattle, and some instances of methicillin-resistant Staphylococcus aureus (MRSA).³

Zoonotic agents are often contracted via the fecal-oral route associated with poor hand hygiene and/or inadequate personal protective equipment (PPE). Appropriate hand-washing before and after handling animals or their associated items is essential to reduce the risk of transmission. Transmission can also occur via contact with wounds or mucous membranes, or inhalation.^6,7 Humans that are immune compromised, due to chemotherapy, chronic illness, or extremes in age, are at increased risk for contracting zoonoses. Finally, a risk for zoonotic disease that each veterinarian and owner face is the increased exposure to these animals.³ Many zoonoses are well known, including Salmonella, tuberculosis, rabies, and influenza. Zoonotic diseases may be reportable to the state or federal government. Excellent resources on specific diseases, transmission, prevention, and reporting requirements exist at the Center for Food Security and Public Health (www.cfsph.iastate.edu/Zoonoses/zoonotic-disease-resources.php, accessed 1 August 2013) and in the AAZV's Infectious Disease Manual (www.aazv.org/?page=754, accessed 10 August 2013) (VIN editor: Link updated Dec 17, 2013).

Bacterial Zoonoses

The most common bacterial zoonoses are enteric bacterial diseases. Transmission generally occurs when bacteria are accidentally ingested through contaminated food or poorly washed hands.

Salmonellosis

Salmonella causes two distinct disease processes, but only nontyphoidal salmonellosis, the gastrointestinal illness is zoonotic. In healthy individuals, these symptoms, including nausea, vomiting, diarrhea, cramps and fever, are often self-limiting.^6,8-10 Nontyphoidal salmonellosis is of particular importance as it affects nearly all animals seen by an exotic animal practitioner, and outbreaks are associated with exotic pets.^8,9,12 Reptiles are an important taxon when discussing animal associated salmonellosis for pet owners and veterinarians.^5,10

  Evidence suggests captive reptiles shed Salmonella more commonly than wild counterparts, and can appear healthy while shedding the bacteria intermittently in their feces.¹⁰

  Bacteria are picked up during handling of animal or cleaning of animal's environment and accidentally ingested, with fecal-oral transmission especially high risk in children.^8,10,12

  Culture remains the gold standard for diagnosis and identification.

  Genetic identification of certain high-risk serotypes from pure culture possible

  Most often traditional serotyping performed by national labs.¹²

  Any animal shedding Salmonella should be considered a risk to human health.^3,6,9,10,12

  Destiny of Salmonella-positive animal is complicated: attempted treatment may be unsuccessful as chronic carriage and intermittent shedding is common, and reinfection is possible.

  Positive animals should be handled with caution: high risk groups may want to consider PPE.³ Hand washing is a must. CDC advises parents to keep their children under 5 years of age away from reptiles.¹²

Other Enteric Bacteria

E. coli is part of normal ruminant livestock flora, with cattle, sheep, goats, deer, and New World camelids as possible asymptomatic carriers. Many nonruminant animals exhibit gastrointestinal signs similar to humans when infected. As these are fecal bacteria, all mammal feces could be a source of these bacteria, including pocket pets and nonhuman primates.^6,9

Bacteria in the genus Yersinia cause important zoonoses of two forms.^1,15

  Yersinia pestis causes the plague, a zoonosis transmitted by the rat flea, Xenopsylla cheopis.

  Small wild mammals in rural and semi-rural areas of the desert Southwest, California, and Oregon serve as reservoirs. Pets can bring the infected flea into the home or clinic to infect humans.

  Human exposure mostly comes from contact with rat flea, but inhalation of aerosolized particles is possible, leading to pneumonic plague.¹⁵

  Y. pseudotuberculosis and Y. enterocolitica are important pathogens of birds that also affect mammals.

  Rodents are considered the reservoir; agent transmitted via fecal-oral route.

  These bacteria can cause gastrointestinal disease in humans and other mammals, including nonhuman primates, pocket pets, pigs, and hoofstock.¹

  Canaries and toucans are highly susceptible to disease, often presenting with peracute mortality or fulminant hepatitis.⁶

  Diagnosis can be difficult; fecal shedding is intermittent. Culture of the affected organ (such as the liver) is often done at necropsy for diagnosis. Treatment of in-contact animals with broad spectrum antibiotics appears to be successful without appearance of antimicrobial resistance.¹

Nonenteric Bacterial Pathogens

Tuberculosis and nontuberculous mycobacteria (NTM) are zoonotic diseases caused by bacteria in the genus Mycobacterium. Important highlights for this audience come from an excellent review of the mycobacterial diseases important to zoo practitioners.

  M. tuberculosis in psittacines often presents with mucocutaneous lesions or lesions of the head or neck, and the source is often an infected human in the household.

  M. avium-intracellulare complex (MAC) can occur in any bird. Contaminated environment, generally from a chronically infected bird, is the most likely source. Treatment is generally unsuccessful.

  MAC is an important and common cause of clinical disease in immunocompromised humans.

  M. avium paratuberculosis, which causes Johne's disease in domestic hoofstock, can affect nondomestic ruminants, and there is speculation that it is linked to Crohn's disease in humans.

  M. genavense affects both humans and birds as an emerging pathogen.

  M. leprae causes leprosy or Hansen's disease in humans with a similar presentation in nonhuman primates. Natural infection of armadillos in the southeastern US has been documented, although zoonotic risk is believed to be minimal.

  M. marinum, M. fortuitum, and M. chelonae are important pathogens in fish that can be zoonotic, with common presentation in reptiles and amphibians. Treatment in veterinary species is generally unsuccessful.⁵

Psittacosis

Caused by Chlamydophila psittaci, this important pathogen of birds that can cause severe disease in humans. Clinical signs in birds can be nonspecific or nonexistent, and shedding may be intermittent, so diagnosis can be challenging. The gold standard for diagnosis is culture and isolation of the organism. Three case definitions exist based on the type of diagnostic performed and the presence of illness that can assist in interpreting diagnostic testing. PCR is the recommended screening test, performed on blood, serum, or a choanal/cloacal swab. Even prior to testing results, treatment should be initiated if the disease is suspected.¹⁴ Treatment with doxycycline (25–50 mg/kg PO q12–24h; 25–50 mg/kg IM q5–7d x 5–7 treatments) is recommended.¹¹

Other important pocket-pet bacterial zoonoses include:

  Tularemia, caused by Francisella tularensis, affects lagomorphs, rodents and people. Transmission can be via vectors like ticks and deer flies, or via contact with infected animals, inhalation of aerosolized bacteria, or ingestion of infected animals or contaminated water. Tularemia is reportable in most areas, and if you have a suspicion of this disease, you should alert the proper authorities.^3,8

  Leptospirosis, caused by serovars of the genus Leptospira, affects mammals worldwide. Transmission can occur via ingestion or via the mucous membranes or damaged skin. Generally the source of infection is water or food contaminated with urine from a maintenance host, such as a rodent, raccoon, opossum, or skunk. Diagnosis can be challenging, with serology commonly used, but treatment may begin empirically based on clinical signs, including elevated renal or hepatic enzymes.⁷ Penicillins and tetracyclines are the backbone of treatment in acute leptospirosis.³

  Rat bite fever is caused by Streptobacillius moniliformis, part of the normal respiratory rodent flora. It can occur as the name suggests via a bite, scratch or consumption of contaminated food or water.^6,7

Viral Zoonoses

Many viruses are zoonotic, and many are well known to the clinical practitioner and behave similarly in both the traditional and nontraditional companion animal. Certain viral zoonoses more specific to the exotic animal practitioner include poxviruses, the encephalitides, and herpesviruses.

Poxviruses

Zoonotic poxviruses in mammals include both orthopox- and parapox-viruses. Monkeypox virus causes disease in humans and nonhuman primates. It is an orthopoxvirus enzootic in wild mammals in west and central Africa, including the Gambian pouched rat, which was responsible for an outbreak associated with pets and people. Fever and rash are often the first signs, with progression to pneumonia and severe disease. Isolation of infected and exposed animals and involvement of regulatory officials is recommended if monkeypox is suspected.² Contagious ecthyma is a parapoxvirus commonly known as orf, which affects sheep and goats, and as the name suggests, is transmissible to people via contact or fomites. Orf is generally self-limiting.⁴

West Nile Virus (WNV)

WNV is an important arthropod-borne virus transmitted by mosquitoes. This virus was enzootic throughout much of the eastern hemisphere, and not considered a major human pathogen until its jump to North America in 1999. WNV affects multiple animal species but is most associated with mortalities in birds and horses. Many captive birds are vaccinated with the available equine vaccine, which is a killed vaccine. Variable vaccination protocols exist with marked discrepancies in titers across species.¹³ At the author's institution we recommend vaccination of birds with reasonable suspicion of naïveté to the pathogen, including New World species, species from high altitudes, and all birds from highly susceptible families, including corvids, flamingos, penguins, and raptors. The vaccination regimen includes 3 vaccines administered 3 weeks apart, with the dose amount ranging from 0.5–1 mL per administration, and an annual booster. Mosquito control is the other arm of prevention of all arthropod-borne encephalitides.

Herpesviruses

Given the close relationship between primates - human and non-human - our herpesviruses can be interchanged with disastrous consequences. Veterinary care of any nonhuman primate requires far more education and training than this presentation or most other CE can provide due to the risk of zoonoses, injury, and inadequate preparation. New World primates are extremely susceptible to a reverse zoonosis from the herpes simplex virus, a virus that is carried by a good portion of the human population. A facemask and gloves should be worn at all times when handling these animals. Without PPE, a human during a flare up can easily cause the death of any callitrichid with which he/she comes into contact. The herpes B virus is a traditional zoonosis, carried by macaques and similar primates but deadly to humans. This author cannot underscore the importance of appropriate PPE (facemask, face shield, gloves, at a minimum) and the essential experience and expertise that a practitioner should have prior to treating nonhuman primates of the macaque family. Special human health precautions, including development of a post-exposure kit, relationship with local emergency medical clinicians, and a clinic-wide protocol should be established prior to starting to see any primate that may carry herpes B or herpes B-like virus.^2,7

Other Zoonotic Virus of Note

Lymphocytic choriomeningitis virus (LCMV) is an arenavirus of rodents that can cause disease in humans. LCMV can also infect nonhuman primates, causing an acute hepatitis referred to as callitrichid hepatitis. Feral rodent exposure is generally the source of the infection.^2,6

Parasitic Zoonoses

Zoonotic Protozoa

Toxaplasma gondii is a protozoan parasite that can be food-borne or zoonotic. Transmission is via accidental ingestion, and much is made of the concern regarding cat litter as a source, although food-borne toxoplasmosis is far more common. Toxoplasmosis is transmitted to felids that serve as the definitive host by ingestion of intermediate hosts like rodents and birds. Intermediate hosts pose no risk to humans, as only the cat sheds infective oocysts. Other veterinary patients may become ill after ingesting sporulated oocysts, including rabbits, domestic hoofstock, nonhuman primates, and marsupials. Disease signs range from vague respiratory or gastrointestinal signs to neurologic changes or death.^3,8

Many protozoa of the genus Cryptosporidia affect a wide variety of vertebrates, with many relatively host-specific. A few species, including C. parvum, can infect both humans and other mammals, including domestic cows, deer and New World camelids. Crypto is generally contracted from infected water, as the most important water-borne pathogen in the US, rather than directly from accidental fecal ingestion. Cryptosporidiosis, like toxoplasmosis, is a major pathogen affecting the immunocompromised. Both are recognized as major causes of morbidity and mortality in HIV-positive patients.^3,8,9

Zoonotic Helminthes

Baylisascaris procyonis is a major and possibly deadly ascarid associated with raccoon feces. It causes neurologic disease and can lead to death in humans and other aberrant hosts, due to larval migrans.⁷ Cestodes from the genus Hymenolepis infect humans and other mammals, and some species are zoonotic. Transmitted is through the ingestion of the egg. It can be diagnosed on a fecal parasite check via direct smear or flotation, and the backbone of treatment is praziquantel.⁶

References

1.  Allchurch, A. F. 2003. Yersiniosis in all taxa. In: Fowler, M. E., and R. E. Miller (eds.). Zoo and Wild Animal Medicine. 5th ed. W. B. Saunders Co., Philadelphia, Pennsylvania. Pp. 724–727.

2.  Burgos-Rodriguez, A. G. 2011. Zoonotic diseases of primates. Vet. Clin. Exot. Anim. 14: 557–575.

3.  Glaser, C. A., E. L. Powers, and C. E. Greene. 2012. Zoonotic infections of medical importance in immunocompromised humans. In: Greene, C. E. (ed.). Infectious Diseases of the Dog and Cat. 4th ed. Elsevier Saunders, St. Louis, Missouri. Pp. 1141–1162.

4.  Greenwood, A. 2003. Pox disease in all taxa. In: Fowler, M. E., and R. E. Miller (eds.). Zoo and Wild Animal Medicine. 5th ed. Elsevier, Philadelphia, Pennsylvania. Pp. 737–741.

5.  Isaza, R. 2003. Tuberculosis in all taxa. In: Fowler, M. E., and R. E. Miller (eds.). Zoo and Wild Animal Medicine. 5th ed. W. B. Saunders Co., Philadelphia, Pennsylvania. Pp. 689–696.

6.  James, S. B. Children's zoo medicine: zoonoses. In: Fowler, M. E., and R. E. Miller (eds.). Fowler's Zoo and Wild Animal Medicine: Current Therapy. Vol. 7. Elsevier, Inc., St. Louis, Missouri. Pp. 115–124.

7.  Johnson-Delaney, C. A. 2005. Safety issues in the exotic pet practice. Vet. Clin. Exot. Anim. 8: 515–524.

8.  Lampel, K. A., S. Al-Khaldi, and S. M. Cahill. 2012. Bad Bug Book, Foodborne Pathogenic Microorganisms & Natural Toxins. 2nd ed. Food and Drug Administration. www.fda.gov/downloads/Food/FoodborneIllnessContaminants/UCM297627.pdf. Accessed 12 September 2013.

9.  LeJeune, J. T., and M. A. Davis. 2004. Outbreaks of zoonotic enteric disease associated with animal exhibits. J. Am. Vet. Med. Assoc. 224: 1440–1445.

10. Mermin, J., L. Hutwagner, D. Vugia, S. Shallow, P. Daily, J. Bender, J. Koehler, R. Marcus, and F. J. Angulo. 2004. Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin. Infect. Dis. 38: S253–S261.

11. Pollock, C., J. W. Carpenter, and N. Antinoff. 2005. Birds. In: Carpenter, J. W. (ed.). Exotic Animal Formulary. 3rd ed. Elsevier Saunders, Philadelphia, Pennsylvania. Pp. 133–344.

12. Reports of selected Salmonella outbreak investigations. 2013. Center for Disease Control and Prevention. www.cdc.gov/salmonella/outbreaks.html. Accessed 10 August 2013.

13. Travis, D. 2008. West Nile Virus in birds and mammals. In: Fowler, M. E., and R. E. Miller (eds.). Zoo and Wild Animal Medicine: Current Therapy. Vol. 6. Elsevier, Inc., St. Louis, Missouri. Pp. 2–9.

14. Tully, T. N., Jr. 2009. Birds. In: Mitchell, M. A., and T. N. Tully, Jr. (eds.). Manual of Exotic Pet Practice. Saunders Elsevier, St. Louis, Missouri. Pp. 250–298.

15. Williams, E. S. 2003. Plague. In: Fowler, M. E., and R. E. Miller (eds.). Zoo and Wild Animal Medicine. 5th ed. W.B. Saunders Co., Philadelphia, Pennsylvania. Pp. 705–709.