Zoonoses and Exotic Pets

What are zoonoses?

A World Health Organization (WHO) Expert Committee on Bacterial and Viral Zoonoses in 1982 defined zoonoses as:

"those diseases and infections (the agents of) which are naturally transmitted between (other) vertebrate animals and man"

How are zoonoses acquired?

Humans acquire zoonoses by either coming into contact with the vertebrate animal (or its excrement) that is carrying the disease via touch, bite or scratch. Acquisition of a specific infection does vary on the zoonosis.

The WHO Expert Committee does acknowledge that the spread of some zoonoses are partially or fully dependent on arthropod vectors for example fleas and Yersinia pestis and Plasmodium spp via Anopheles mosquitoes respectively. Murphy (1998) therefore describes zoonoses as "the transmission of the etiological agent to humans from an ongoing reservoir life cycle in animals or arthropod, without the permanent establishment of a new life cycle in humans".

Zoonoses can be acquired from a number of domesticated animals and wild animals many of which are killed for bushmeat, they include chimpanzees (Leedertz et al. 2004), reptiles (Sanyal et al. 1997), Japanese deer (Tei et al. 2003), praire dogs (Lewis-Jones, 2004), birds (Mohan, 1984) and civets (Xu et al. 2004).

The emergence and re-emergence of zoonoses is becoming a global concern because they will increase the number of fatalities globally. There are a number of factors that contribute to the emergence of zoonoses for example a rise in the human population globally along with deforestation is bringing humans into a closer proximity with wild animals (Murphy 1998 and Peres 2000). Humans are increasingly traveling to remote regions around the world therefore bringing them into contact with zoonoses (Murphy 1998 and Weber 2001).

Exotic Pets

There are four primary types of etiological agent that cause zoonotic diseases in humans; bacteria, helminthes, protozoa and viruses. The majority of the protozoa diseases are endemic within certain regions of the world and are unlikely to spread via the consumption of bushmeat or exotic pets for example Plasmodium spp that are the etiological agent of malaria. Therefore I will not be discussing protozoa diseases in this dissertation. Nor will I be discussing helminth infection because they usually arise from eating poorly cooked food and poor hygiene around domesticated animals, therefore this group of zoonotic diseases will not be discussed further either.

Bacterial Zoonoses

Anthrax:
Bacillus anthracis is the cause of anthrax, it is a gram positive spore forming bacteria. It is an enzoonotic disease (transmitted between animals) in Africa and Asia and is usually acquired from contaminated soil or water by ruminants. Infection can occur via ingestion of spores. Humans can also become infected via inhalation of spores from the hair, carcass and even bones of an infected or vector animal (Weber et al. 2001). There are three types of anthrax infections cutaneous, respiratory and intestinal. Pathology of anthrax in humans includes black scabs, fever, swelling of lymph nodes and can lead to pneumonia, septicemia and generalized haemorrhaging and if not treated can result in a high fatality rate (Bell et al. 1988 and Leedertz et al. 2004).

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Leedertz et al. (2004) documented that eight chimpanzees from three communities in the Tai National Park, Ivory Coast had died due to anthrax infections. This is a worry because chimpanzees are a source of bushmeat (Thiabault et al. 2003 and De Merode et al. 2004) and theoretically if an infected carcass is eaten a small epidemic could occur with hunters, transporters and street vendors as well as consumers all being infected.

Plague:
The plague (the Black Death) is caused by a member of the Yesinia genus all cause disease in humans, the three species are Y. pseudotuberculosis, Y. enterolitica and Y. pestis. Y. pestis is a gram negative coccobacillus and is the etiological agent of plague. Y. pestis is one of the most feared zoonotic diseases because of the devastating pandemics it has caused throughout history and because of recent epidemics. Perry et al. (1997) estimated that plague has caused the death of 200 million people through out history. From 1345 to 1360 the Black Death caused the death of 24 million people just in Europe, at the time this was a quarter of the world"s population (Fritz et al. 1996).

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One of the most documented plague epidemics to occur in the last century was in India. The plague was first identified in Maharastra state in August 1994, in October (1994) there were 300 suspected cases of plague and 36 deaths in Surat, Gujarat state. This prompted the fleeing of an estimated 600, 000 people. Reports of plague came from other regions of India via the spread of pneumonic plague by humans. A number of countries shut their border with India and a number of commercial flights were cancelled (Fritz et al. 1996 and Perry et al. 1997).

Global distribution of plague (WHO Plague 2002). WHO have stated that in 1999 there were 2,603 cases of plague globally with 212 fatalities. The last large epidemic in a western country was in America, Los Angeles in 1924-1925 (Centers for Disease Control and Prevention Plague Website, 2004). More recent outbreaks of plague include Madagascar in 2000, this outbreak was important because the strain of Yersinia isolated was found to be multiresistant to a number of antibiotics (Ratsitorahina et al. 2000 and Raoult 1998). Other countries that had outbreaks include Zambia in 2001, Malawi in 2002 and Algeria in 2003 (WHO Plague outbreaks).

Humans can contract plague from three sources; from the bite of a flea (Xenopsylla cheopis) from an infected animal. There are a number of animals that are susceptible to plague and act as reservoirs for the disease, plague can therefore act also as an enzoonotic disease. Examples of these animals include rats, prairie dogs, ground squirrels and rabbits (Orloski et al. 2003, Perry et al. 1997). Plague can be acquired from the consumption of infected animal tissue (Perry et al. 1997 and WHO Plague, 2002). There are three forms of plague manifestations; bubonic, septicemic and pneumonic. The third mode of transmission of plague is via the inhalation of infected aerosol droplets sneezed or coughed out by infected humans (patients with pneumonic plague).

After being bitten by an infected flea the patient shows signs of fever and displays swollen lymph nodes (buboes) because this is where the bacteria reside and proliferate, this clinical form is known as bubonic plague and takes 2-8 days to develop after the initial exposure. The bacteria can then infect the blood and cause secondary septicemia, which could in turn lead to death without treatment. Septicemic plague develops without the development of buboes and causes primary septicemia, here the bacteria infect the blood causing headaches, abdominal pain and death without treatment. The Yersinia bacteria can infect the lungs this can occur after bubonic or septecemic plague forms but also manifests as a disease itself in susceptible people. Patients with pneumonic plague have flu-like symptoms and cough up bloody sputum. Pneumonic plague is the most contagious form of plague due to the spread of infectious droplets.

Salmonella:
As well as Salmonella being a common cause of food poisoning it is also a zoonotic disease. There are a number of Salmonella spp that are zoonotic for example S. chameleon, S. rubislaw and S. newport. Woodward et al. (1997) identifies S. arizonae as a serotype that is associated with exotic pets and it has been found in the stool samples of exotic pet (snakes) owners (Sanyal et al. 1997).

In the United States 7.3 million reptiles were kept as pets and in 1996 there were 93,000 cases of Salmonella attributed to reptiles (United Kingdom Department of Health, 2000). The "at risk" populations for contracting salmonellosis are; the pet owners (who oftern touch the pets and clean out cages and terrariums), children under the age of five, immuno-suppressed, the elderly and pregnant women (Geue et al. 2002 and Sanyal et al. 1997). Professor Liam Donaldson, Chief Medical Officer for England issued a warning to pet reptile owners of the possibility of acquiring Salmonella. Geue et al. (2002) stated that 90% of reptiles harbour Salmonella as an intestinal commensal and it is shed in their faeces and Worell (2003) stated more specifically that 90% of green iguanas are carriers of Salmonella. 11-12% of turtles carry Salmonella in their intestines in western countries (Stam et al. 2003). But it is not just cold blooded animals that harbour this bacteria a number of warm blooded exotic pet animals also act as reservoirs (as shown above) for example ferrets (Worell 2003), African pygmy hedgehogs (Avashia et al. 2004 and Woodward et al. 1997) and the Australian marsupials sugar gliders (Woodward et al. 1997).

As well as contracting Salmonella from exotic pets it can also be contracted from bushmeat. Sanyal et al. (1997) documents a case where a 6 year old Hispanic boy from Arizona contracted S. arizonae after consuming sundried rattlesnake meat, a type of folklore medicine. Clinical features of salmonellosis include fever and diarrhea (Bell et al. 1988).

Tuberculosis:
WHO estimated that between 1990 and 1998 there were 88 million cases of tuberculosis and 30 million deaths from this disease the majority of which were in developing countries (Cosivi et al. 1998). In 2000 there were 36 million people infected with HIV and 12 million were co-infected with M. tuberculosis (Godfrey-Faussett et al. 2002).The highest rate of infection is occurring within the age group (15-59) that constitute the workforce of every country, if this workforce is depleted the country on a whole will suffer economically. This is occurring because humans who contract tuberculosis are usually immunosupressed individuals, HIV patients. Therefore tuberculosis is an opportunistic disease.

A number of Mycobacterium spp are the cause of tuberculosis in humans and animals, birds and fish. The most common form of tuberculosis in humans is caused by Mycobacterium tuberculosis. The zoonotic serotypes of tuberculosis are M. bovis, which is acquired from cattle, M. avian, birds are the reservoirs of this serotype, contraction occurs via inhalation of faeces or via an infected carcass and M. marinum is the serotype that infects fish but it can be acquired via a fish bite or consumption or swimming in infected water (Bell et al. 1988, Cosivi et al. 1998, Michalak et al. 1998 and Worell 2003). M. bovis is primarily acquired from cattle but it has been documented that M. bovis has been contracted from seals and elk. M. avian and M. marinum are serotypes of tuberculosis that can be acquired from exotic pets. M. tuberculosis can also infect a number of different mammalian species humans, elephants and tigers (Michalak et al. 1998).

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Michalak et al. (1998) documented the first case whereby M. tuberculosis was a zoonotic disease. On an exotic animal farm in Illinois, California (1996) where both elephants and tigers were kept, a number of elephants had died. Post-mortem discovered "short, fat, relatively scant numbers of acid-fast bacilli". The animal handlers on the farm were tested for tuberculosis via purified protein derivative (PPD) skin prick tests. 50% of the handlers were PPD positive indicating that they had tuberculosis, chest x-rays and sputum samples did confirm this. Horizontal zoonotic transmission of M. tuberculosis between humans and elephants is possible. None of the animal handlers were immunosuppressed but this study uncovered the fact that tuberculosis can be contracted via prolonged exposure with an animal or human with active tuberculosis (Michalak et al. 1998). Earlier, elephants were documented as a type of bushmeat (Thibault and Blaney 2003).

Tularemia:
The causative agent of tularemia is Francisella tularensis. There are two forms of tularemia type A and B. Type A is prevalent in North America whilst type B can be found in Asia, Europe and North America. It is contracted via coming into contact with infected animals such as rabbits, squirrels, prairie dogs and muskrats as well as other rodents. Ticks of the infected animals also carry F. tularensis and are therefore also reservoirs of the disease (Deutz et al. 2003 and Luvesque et al. 1995). Some of the clinical features associated with tularemia include fever, head aches, swollen lymph nodes, pneumonia and vomiting and diarrhea (Avashia et al. 2004 and Bell et al. 1988).

Tularemia is a commonly acquired zoonosis amongst trappers and hunters. Luvesque et al. (1995) in their study of zoonoses among trappers in Canada discovered that 27% of trappers that capture over one hundred muskrats per year had antibodies against F. tularensis in their blood samples. Also an epidemic of tularemia in Vermont, near the United States-Canada boarder was attributed to muskrats. Avashia et al. (2004) documented the first prairie dog-to-human transmission of tularemia. It occurred in Texas where a 24 year old male animal handler contracted F. tularensis from infected black-tailed prairie dogs at an exotic pet distributorship. Before the man had become infected a large number of the prairie dogs died, their deaths were attributed to tularemia due to the isolation of F. tularensis. Before the discovery of tularemia among the prairie dogs a number of them were shipped for sale in other American states and abroad.

The numbers of prairie dogs exported to the various states and countries. Of the hundred prairie dogs that were sent to the Czech Republic 30 were already dead on arrival to the country and 30 were ill, all of the animals were culled (Avashia et al. 2004). But the above incident shows how easy a zoonosis can travel around the world in an exotic pet and potentially infect someone.

Chlamydia:
Chlamydia psittaci is the cause of chlamydia and Bell et al. (1988) describe it as an "obligate intracellular bacterium". C. psittaci is commonly acquired by humans coming into contact with infected birds (Worell 2003). A number of birds can act as reservoirs for the disease they range from ducks to macaws (Mohan 1984). Takahashi et al. (1997) identified a number of serotypes of C. psittaci found in different mammalian and bird species. Birds intermittently shed C. psittaci in their faeces and it is the inhalation of dried faeces or even aerosols (from birds) that cause infection in humans (Worell 2003). Between 1988 and 1998 70% of the 800 cases of C. psittaci were associated with pet birds (Morrison 2001). Clinically C. psittaci is difficult to diagnose because its features are similar to influenza. But features of this zoonosis include fever, coughs and headaches and could lead to an enlarged spleen, endocarditis and hepatitis. Fatalities are rare but if pregnant women become infected neonatal death is a possibility.

Leptospirosis:
Leptospirosis caused by Leptospira interrogans is a sporadic disease and is acquired by wounds and abrasions coming into contact with infected urine from a number of animals for example rats, foxes and raccoons. Luvesque et al. (1995) and Deutz et al. (2003) identified zoonoses amongst trappers in Canada and Austria respectively and identified a number of Leptospira serotypes. Some of the clinical features of the disease include fever, headaches, nausea, pneumonia and even jaundice and nephritis (Bell et al. 1988 and Bharti et al. 2003). Meslin (1997) documented that leptospirosis infected hundreds of people and killed 16 in the Achuapa region in Nicaragua. What was unusual about the leptospirosis infections was that the fatalities during autopsy showed severe respiratory haemorrhaging, leptospirosis is usually associated with kidney and liver infection (Bell et al. 1988). Therefore the samples from the bodies were tested for dengue fever but were negative but found positive for leptospirosis.

Q Fever:
The causative agent of Q fever is an obligate, intracellular gram negative bacterium Coxiella burnetii (rickettsia). It is contracted via the handling of infected carcasses, the inhalation of infected dust or the consumption of infected milk. It can also be acquired from tick bites because arthropods as well as mammals (cats, sheep, goats and cattle) act as reservoirs for this disease. Q fever produces a number of clinical features which include fever, chronic hepatitis and chronic endocarditis (Bell et al. 1988 and Weber et al. 2001). Luvesque et al. (1995) in their seroepidemiological study of zoonoses among trappers in Canada discovered that 15% of trappers and even a control were seropositive for C. burnetii, this high percentage was a cause for concern for the trappers and the scientists.

Other Bacterial Zoonoses:
Deutz et al. (2003) stated that blood tests of hunters in Austria were positive for brucellosis, brucellosis is caused by a species from the Brucella genus and is usually acquired from infected material from an infected animal for example urine or blood. Symptoms include fever, fatigue, joint pains and even depression (Bell et al. 1988). Worell (2003) mentioned that one can also contract Campylobacter spp from reptiles. Other microbial zoonoses mentioned by Morrison (2001) are Cryptococcus neoformans, which can be acquired from birds and causes meningoencephalitis. Streptobacillus moniliformis and Spirillum minus are causes of rat bite fever. Burkholeria pseudomellei is contracted from the water in which exotic fish are transported in. Edwardsiella spp and Plesiomonas spp cause gastroenteritis via contact with infected snakes.

Summary

Many of these zoonoses discussed here can be treated with antibiotics or there is a vaccine available to prevent disease acquisition. But there are millions of people who can neither travel large distances to see a doctor for treatment or can afford to pay for their treatment because they are in extreme poverty i.e. earn an income of <US$1 a day (Davies 2002). Therefore it is theoretically possible to have a large epidemic even a pandemic of a microbial zoonosis for example plague.

The rapidness of world travel, the extremely large global population and deforestation are bringing animals and their infectious etiological agents into closer proximity with humans. The large global population also means that humans are in close contact with each other therefore making the spread of pneumonic plague for example very possible.

© MicrobiologyBytes 2007.