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Several million people in the United States have compromised immune systems, including an estimated 1 million people infected with human immunodeficiency virus (HIV).¹ Immunocompromised persons are susceptible to a number of opportunistic infections. However, although opportunistic infections may be acquired from pets, and although 30 to 40% of immunocompromised persons may own pets,² few immune-suppressed individuals are offered information about zoonoses prevention. In this report, we provide veterinarians with guidelines for a zoonoses prevention program for their immunocompromised clients.

Conditions Compromising the Immune System in Human Beings

The immune system may become suppressed by underlying diseases, treatments, or infectious diseases. Systemic diseases associated with immune suppression in people include congenital immunodeficiencies, diabetes mellitus, chronic renal failure, alcoholism and liver cirrhosis, malnutrition, and certain types of cancers. Persons likely to receive immunosuppressive treatments are cancer patients, organ- or bone marrow-transplant recipients, and patients with autoimmune diseases. Other immunosuppressive treatments include splenectomy and long-term hemodialysis. Although many infectious diseases may cause immune suppression, the most profound suppression is caused by HIV.

Persons infected with HIV may be free of clinical signs or symptoms for many years. The acquired immunodeficiency syndrome is a severe, life-threatening condition that represents the late clinical stage of HIV infection. The median time from HIV infection to development of acquired immunodeficiency syndrome is approximately 10 years, although some individuals have remained asymptomatic 15 years after infection.³

Severity of the immunologic damage in HIV-infected persons is usually monitored through measurement of T-lymphocyte counts, especially absolute CD4 lymphocyte counts.⁴ Trends in CD4 counts are commonly used to make decisions regarding treatment, including prophylaxis against several opportunistic infections, in HIV-infected individuals. The risk of developing opportunistic infections increases as CD4 counts decrease, especially when counts are <200 cells/µl. When CD4 counts are >500 cells/µl, routine veterinary care is probably adequate for companion animals of HIV-infected clients. However, as CD4 counts decrease, implementing an expanded zoonoses prevention program becomes increasingly important.⁵

Public Health Role for Veterinarians

Through monitoring the health of companion animals and educating pet owners on zoonoses prevention, veterinarians can help reduce the likelihood of an immunosuppressed person acquiring certain zoonotic opportunistic infections and can help their clients make more informed decisions about the risks and benefits of owning a pet.^6,7 However, few veterinarians routinely discuss ways to minimize transmission of zoonoses with their clients⁸ and we believe even fewer inquire about the general health of persons who live in the household with the pet. Not surprisingly, although many immunocompromised persons own pets, few apparently receive information from veterinarians about preventing transmission of opportunistic infections from their animals; in one survey,⁶ <1% of persons infected with HIV had obtained such information from a veterinarian.

Despite receiving training about zoonoses, many veterinarians may be reluctant to discuss this topic, perhaps because they view educating people about zoonoses as a role for physicians. Our experience, however, is that few physicians provide immunocompromised persons with information about zoonoses and safe practices for pet ownership. In addition, when pets are thought to pose a health risk, overly cautious recommendations are often made, such as giving up pets altogether.⁹

Although a high proportion of immunocompromised pet owners have been advised to give up their pets, it is our experience that few part with their pets,¹⁰ suggesting a strong emotional attachment between many owners and their pets. Companion animals apparently provide psychological benefits for some immunocompromised persons, many of whom have feelings of isolation and rejection.¹¹ A recent study^a of HIV-infected persons revealed that pet ownership was associated with a decreased prevalence of depressive symptoms, particularly in persons with less human social support.

In recent years, several nonprofit groups have organized to help HIV-infected persons care for their pets. Over 3,000 HIV-infected clients currently receive services for their companion animals from such organizations in the United States (Appendix). Several veterinarians have been active in these organizations, particularly with the Education Committee of Pets Are Wonderful Support (PAWS) in San Francisco, which has published several brochures for HIV-infected and other immunocompromised pet owners. These brochures include Safe Pet Guidelines, Toxoplasmosis and Your Cat, Zoonoses and Your Bird, and Cat Scratch Disease.

Although we encourage all veterinarians to offer an expanded zoonoses prevention program for their immunocompromised clients, we believe such a program requires special commitment of the veterinarian. The veterinarian should be knowledgeable about animal-associated opportunistic infections and be willing to educate immunocompromised clients about zoonoses prevention. He or she should have access to a laboratory that uses appropriate tests to detect the most common opportunistic pathogens. The veterinarian also should recognize that the increased financial costs of an expanded zoonoses prevention program may be a hardship for some immunocompromised individuals.

Veterinarians should inform their clients of the existence of an expanded zoonoses prevention program, while respecting the client's privacy.¹² This may best be accomplished by announcing the program in a sign, brochure, or newsletter (Figure 1). If a client inquires about the program, the veterinarian then could ask, in the privacy of the examination room, if someone in the household has an immunosuppressive condition and if so, offer the program to the client.

Veterinarians should also educate their staff about conditions that cause immune suppression, including HIV infection and acquired immunodeficiency syndrome.¹³ The need for confidentiality should be emphasized. Because some people confuse feline and human immunodeficiency viruses, or mistakenly believe animals can transmit HIV, the role of pets in HIV-associated disease and opportunistic infections should be explained. Personnel should understand how to use universal precautions when administering first aid to clients or staff.¹⁴

Guidelines

Although the health risk of owning a companion animal is thought to be low for a person with an impaired immune system, the risk can be further reduced with simple precautions.¹⁵ If someone with a compromised immune system elects to own a companion animal, he or she should be more vigilant of the pet's health than other pet owners are expected to be. Immunocompromised pet owners should be willing to seek veterinary care early in the clinical course of illness in their pet. They also should recognize that an expanded zoonoses prevention program may be more expensive than routine veterinary care.

Many of the opportunistic infections that infect immunocompromised persons also infect animals, but the extent to which infected pets contribute to the transmission of these diseases to immunocompromised persons varies widely.¹⁵ The most common infections associated with animals include Toxoplasma gondii, Cryptosporidium spp, Salmonella spp, Campylobacter spp, Giardia sp, Rhodococcus equi, Bartonella (Rochalimaea) spp, Mycobacterium marinum, and Bordetella bronchiseptica. Each of these infections, except for possibly Bartonella spp, may be acquired from sources other than pets.¹⁵ The proportion of these infections acquired from pets is not known, but is thought to be small.¹⁵ When considering their prevalence and the proportion of cases originating from pet sources, the most common infections acquired by immunocompromised persons from pets apparently are those caused by Salmonella and Campylobacter spp.

General recommendations--Immunosuppressed pet owners should be particularly careful about what their pets eat and drink. We recommend they feed their pets only high-quality commercial pet foods. If immunocompromised persons insist on supplementing their pets' diets, they should ensure that all egg, poultry, and meat products have been adequately cooked before feeding. Only pasteurized dairy products should be used. Tap water is adequate for most pets, unless it has been shown to be unhealthy for human consumption, in which case commercial bottled water is preferred. Pets should not be allowed to drink out of toilet bowls or have access to garbage. They should be closely supervised while outside, unless they are in their own fenced yard. Pets should not be allowed to scavenge, hunt, or eat other animals' feces. Immunocompromised persons should wash their hands after handling pets, especially before eating, and should avoid contact with their pet's feces.

Cats and dogs should receive routine annual veterinary care, including a physical examination, standard immunizations, and a fecal examination for intestinal parasites. Pets owned by immunocompromised persons should receive veterinary care early in course of the pet's illness. In animals with diarrhea, a fecal sample should be obtained for Salmonella and Campylobacter culture and should be examined for Cryptosporidium and Giardia spp (screening for Cryptosporidium and Giardia spp is not necessary for birds). Animals with diarrhea should not be allowed contact with immunocompromised persons.

Veterinarians should submit fecal samples to a clinical laboratory that performs the specific procedures necessary to detect these pathogens. Salmonella spp are isolated by culturing on standard selective media, then determining biochemical reactions. Selective media and appropriate incubation conditions, including a micro aerobic atmosphere, must be used to isolate Campylobacter spp.¹⁶ An acid-fast test may identify Cryptosporidium spp, but the indirect fluorescent antibody test is more sensitive and specific.^17,18 The preferred concentration technique for detection of Giardia sp is the zinc sulfate method,¹⁹ but additional examinations may be required for diagnosis.²⁰ Sample transportation requirements, including transport media and preservatives, may differ among laboratories, emphasizing the need for advance coordination with the laboratory.

If a Campylobacter sp is isolated from dogs or cats, treatment with erythromycin is recommended to eliminate shedding of organisms in feces.²¹ Fecal samples for Campylobacter culture should be obtained after treatment because shedding may recur in some animals.²² Treatment of pets with salmonellosis is usually not recommended unless clinical signs of bacteremia are evident, because treatment may prolong the usually transient shedding period.²³ Pathogens should not be found on culture of fecal samples, collected at least 24 hours apart when the pet is not receiving antibiotics, before introducing or returning a pet infected with Salmonella or Campylobacter spp to the home of a person with impaired immune function. Giardiasis should be treated with metronidazole²⁴ or possibly albendazole, which has recently been shown to be an effective alternative treatment for giardiasis in dogs.²⁵ There is no effective treatment for cryptorporidiosis, although shedding in otherwise healthy pets is thought to be transient, often lasting <2 weeks.^26-27

Obtaining a pet--When obtaining a new pet, immunocompromised persons should choose a healthy adult pet and avoid young animals, especially those with diarrhea, since young animals with diarrhea are more likely to be shedding Salmonella,²³ Campylobacter,²⁸ Cryptosporidium,²⁹ or Giardia spp.³⁰ Because the hygienic and sanitary conditions in facilities of pet breeders, pet stores, and animal shelters are highly variable, immunocompromised persons should exercise caution if obtaining a pet from these sources.

Immediately after a pet is obtained, it should be examined by a veterinarian. If the pet's health is questionable, it should not be allowed contact with an immunosuppressed person. Examination of fecal samples from healthy animals for pathogens may be advisable if the client's immune suppression is severe (eg, an HIV-infected client with a CD4 count below 200 cells/µl).

Birds--Pet birds pose a low risk to immunocompromised persons. A high proportion of HIV-infected persons have heard they should avoid owning pet birds,¹⁰ apparently because of concerns about infections with Cryptococcus neoformans or M avium, but these concerns are largely unwarranted. We do not recommend screening healthy birds for C neoformans or M avium.

Cryptococcus neoformans does not cause disease in birds because of their high body temperature. Cryptococcus neoformans is commonly isolated from soil and droppings of wild birds, especially pigeons, but seldom from droppings of pet birds.³¹ Transmission to human beings is by inhalation of airborne organisms, but even in highly contaminated areas, only a small number of organisms of the appropriate size to reach the alveoli are aerosolized.³² Pet birds are therefore an unlikely source of Cryptococcus infection for human beings.¹⁵

Pet birds are also an unlikely source of M avium infections in human beings because M avium isolates from birds differ in antibiotic susceptibility, serovars, and genetic sequencing from human isolates.^33-35 Mycobacterium avium causes avian tuberculosis, an enteric granulomatous infection characterized by chronic weight loss and high WBC counts. Pet birds rarely develop avian tuberculosis, although the infection may be more common in gray-cheeked parakeets and Amazon parrots.³⁶ Diagnosis is by positive results on acid-fast staining of a direct fecal smear. Treatment of birds with M avium infection may be possible with long-term antituberculous drugs.³⁶ Although increased risk is not documented, persons with impaired immune function probably should not have contact with pet birds with clinical M avium infections.

Immunocompromised persons should avoid contact with bird droppings, although an increased incidence of suitcases has not been reported among immunosuppressed persons, and enteric pathogens, such as Salmonella and Campylobacter spp, apparently are rarely acquired from birds.¹⁵ To further reduce the risk of salmonellosis and campylobacteriosis, immunocompromised persons should feed their birds only a high-quality diet, avoiding old seed that may become contaminated during storage. A reliable pet store may be helpful in selection of good-quality feed. Ideally, an immune-competent person should clean the cage, or the immunocompromised person should wear gloves during cleaning and immediately wash afterwards. In ill birds, samples of droppings should be obtained for culture of Salmonella and Campylobacter spp.

Immunocompromised persons should avoid handling wild birds because they are more likely than pet birds to shed Salmonella and Campylobacter spp.¹⁵ In addition, because C neoformans is transmitted via inhalation and is commonly found in pigeon excreta, these persons should avoid places where pigeon droppings are abundant.

Cats--Many immunocompromised persons have been told they should not own cats to avoid developing cerebral toxoplasmosis, a common opportunistic infection among immunosuppressed persons.¹⁰ However, in 1 study of HIV-infected persons,³⁷ an association between cerebral toxoplasmosis and cat ownership was not found. Most cases of cerebral toxoplasmosis are caused by reactivation of a previously latent infection, and not by an acute infection.³⁸ In addition, most acute infections apparently are acquired through eating undercooked meats.³⁹ Nevertheless, immunosuppressed persons should take precautions to prevent ingestion of infective oocysts from cat feces.³⁷

Cats are the definitive host of Toxoplasma gondii; they are the only animals that pass oocysts in their feces. Once oocysts are shed, they require 1 to 5 days to sporulate and become infective.⁴⁰ Although shedding has been suggested to be prolonged or recurrent in some cats,⁴¹ cats pass oocysts for only 2 to 3 weeks following primary infection.⁴⁰ Cats experimentally infected with feline immunodeficiency virus and T gondii⁴² or FeLV and T gondii⁴³ did not have prolonged oocyst shedding. Oocyst shedding also did not recur in adult cats following repeated infections,^44,45 administration of clinical doses of glucocorticoids,⁴⁶ or infection with feline immunodeficiency virus.⁴⁷

We do not recommend examination of feces for Toxoplasma oocysts or testing of serum for Toxoplasma antibodies in healthy cats. Fecal examination is seldom rewarding, because oocysts are shed only transiently and are so small they are easily missed. Current serologic tests cannot accurately predict which cats are shedding oocysts. Most, but not all infected cats have completed oocyst shedding by the time antibodies are detectable in their serum.⁴⁰ Thus, a small proportion of seropositive cats may still be shedding oocysts. In contrast, a seronegative cat may be uninfected or may be recently infected and currently shedding oocysts. Given the uncertainties in the interpretation of these laboratory tests and the relative ease in implementing measures to prevent zoonotic disease, these tests should not be used to modify recommended precautions.

Preventing transmission of toxoplasmosis from cats should focus on litter box hygiene.³⁷ Litter boxes should be cleaned daily and not placed in kitchen or dining areas. An immune-competent person should clean the litter boxes. If an immunocompromised person must clean the litter box, he or she should wear gloves during cleaning and immediately wash afterwards. Direct contact with cats is unlikely to result in transmission of toxoplasmosis because most cats do not leave feces on their fur for the 1 to 5 days required for oocyst sporulation.

To prevent infection with T gondii, cats should not be allowed to hunt and should not be fed raw or undercooked meat. Because outdoor cats frequently defecate in gardens and T gondii oocysts may survive for months under appropriate conditions,³⁹ immunosuppressed persons should wear gloves when gardening or working with soil and should immediately wash their hands afterwards.

Although infrequently acquired from cats, salmonellosis and campylobacteriosis may be the most common infections acquired from cats in immunocompromised persons.¹⁵ The previously mentioned litter box and feeding guidelines for preventing transmission of toxoplasmosis also will help prevent transmission of these enteric pathogens.

Bacillary angiomatosis is a newly recognized disease syndrome that has been diagnosed primarily among immunocompromised persons.^48-53 Much remains to be learned regarding the spectrum of human disease, prevalence of infection, and methods for prevention. Disease signs among immunocompromised persons are variable and include undiagnosed febrile disease, serious skin lesions, and life-threatening systemic disease. Although antibiotic treatment appears to be effective for immunocompromised patients, such treatment may need to be prolonged.^53,54

Bacillary angiomatosis is caused by Bartonella (formerly Rochalimaea) quintana or B henselae infections.⁵⁴ Bartonella quintana infections have not been associated with cat contact, and a zoonotic reservoir for B quintana has not been described.⁵⁴ In contrast, infections with B henselae, which is also the etiologic agent of cat scratch disease in immunocompetent persons, are associated with cat contact.^55-59 Cat scratch disease is diagnosed in an estimated 22,000 persons/year in the United States⁶⁰; however, the prevalence of B henselae infections among immunocompromised persons has not yet been determined.

Domestic cats appear to be common reservoirs for B henselae. Risk factors for humans acquiring B henselae infections include owning a cat (especially a kitten), being scratched by a cat, and having a cat with fleas.^51,58,59 Bartonella henselae also has been isolated from the blood samples of 41% of apparently healthy cats, and from fleas from some of the same cats. However, the potential role of fleas as effective vectors of B henselae has not yet been established.^56,61 Likewise, typically 40 to 50% of healthy cats have evidence of past or current Bartonella infection, and antibody prevalence is higher among cats associated with infected human beings.⁵⁹

Because the mechanisms of B henselae transmission are not yet known, recommendations for prevention are limited to common-sense precautions.⁶² Kittens appear to pose a greater risk for disease than adult cats do. Flea control may be beneficial in preventing transmission, but this has not been proven. Persons with immune suppression should avoid activities that may result in cat scratches or bites. All cat scratches or bites should be washed immediately with soap and water. The effect of declawing of cats on the likelihood of B henselae transmission is unknown. Similarly, the effect of claw covers for reducing transmission has not been evaluated, but may be beneficial. Treating cats with antimicrobial agents has been suggested to clear the infection, but further controlled studies are necessary⁵⁶; reinfection after the organism has been cleared has not been evaluated. Cats may have concurrent B henselae bacteremia and Bartonella-specific IgG antibodies, and the relationship between antibody status and potential infectivity is still being investigated. For all these reasons, the value of Bartonella antibody testing in cats for individuals making decisions regarding cat ownership remains unclear, especially in environments where the prevalence of infection and rate of transmission in cats are high. Because early antimicrobial treatment is effective in bacillary angiomatosis, all immunocompromised persons should inform their physician about the presence of cats in the household.

Cats may develop cutaneous C neoformans infections, but these are not considered public health hazards because the organism is not aerosolized from these sites.⁶³ Cats also may develop cutaneous or disseminated M avium infections, but these organisms are ubiquitous in the environment and human infections have not been associated with infected cats.⁶⁴

Dogs--Bordetella bronchiseptica infections have been reported in several immunocompromised persons,⁶⁵ but routine use of the B bronchiseptica vaccine is not recommended except for dogs entering kennels or on show circuits.⁶⁶ In lieu of having their dogs vaccinated, immunocompromised persons, especially those with advanced disease, should avoid exposing themselves and their dogs to environments known to represent a source of B bronchiseptica (eg, boarding kennels, dog shows, or any situation in which dogs from several sources are housed together).

Although infrequently acquired from dogs, salmonellosis and campylobacteriosis may be the most common infections acquired from dogs in immunocompromised persons.¹⁵ Dogs are probably more likely than cats are to transmit these enteric infections to human beings, because rates of shedding of Salmonella, Campylobacter, Cryptosporidium, and Giardia organisms in feces are usually higher in dogs, and dogs are generally less fastidious about grooming themselves.

Other animals--Immunocompromised individuals should not own reptiles because of the high rates of carriage and shedding of Salmonella organisms in reptiles.⁶⁷ Persons who insist on keeping reptilian pets should wear gloves when cleaning the cages and handling the pet, and should feed it a diet specifically processed for reptiles (without raw meat or egg products). Treatment of reptiles for Salmonella infection is not effective.⁶⁷

Small rodents, such as hamsters and gerbils, can also transmit Salmonella, Campylobacter, Cryptosporidium, and Giardia infections.⁶⁸ Immunocompromised persons should be diligent about washing their hands after handling the animals or cleaning cages.

A small number of Mycobacterium marinum infections have been reported among HIV-infected persons.¹⁵ All of these patients acquired their infection from contact with pet fish usually when cleaning the aquarium.¹⁵ Gloves should be worn when cleaning an aquarium or when handling fish. Fish infected with M marinum should be killed and the aquarium should be disinfected before new fish are introduced.⁶⁹

Immunocompromised persons should avoid contact with young farm animals, especially animals with diarrhea, because farm animals can act as a reservoir for several infective agents, including Cryptosporidium spp.¹⁵ Immunocompromised persons also should avoid exposure to swine, which are a known source of B bronchiseptica.⁶⁶ Although Rhodococcus equi infection has been reported in several immunosuppressed people,^70,71 most patients do not report a history of recently visiting farms or rural areas, and risk does not seem to be increased by having contact with adult horses.¹⁵

Footnote

(a) Angulo FJ. Association of pet-ownership and prevention of depressive symptomology among HIV-infected persons (abstr), in Proceedings. Delta Soc 12th Annu Conf 1993;19.

Figure 1- Example of a poster that veterinarians could use to encourage clients to discuss the need for an expanded zoonoses prevention program. Free copies of this poster (12 x 17 in) may be obtained by sending $3 for shipping and handling to the Humane Society of the United States, Department PA, 2100 L Street, NW, Washington, DC 20037.

Appendix

Nonprofit organizations providing assistance to pet owners infected with human immunodeficiency virus

Companion Animal Support and Assistance Network (CASAN), 810 Barret Ave, 266B, Louisville, KY 40204; (502)574-5490.

Hawaiian Humane Society: Pets Are Loving Support(PALS) Program, 2700 Waialae Ave, Honolulu, HI 96826; (808)955-5122.

Marin Humane Society: Share Program, 171 Bel Marin Keys Blvd, Novato, CA 94949;(415)883-4621.

Pet Pals, PO Box 190869, Dallas, TX 75219; (214)521-5124.

Pet Patrol, PO Box 980255, Houston, TX 77O98; (713)522-1954.

PALS, 1438 Peachtree St, Atlanta, GA 30309;(404)876-7257.

PALS: Guerneville, PO Box 1539, Guerneville, CA 95446; (707)887-2729.

Pets Are Wonderful Support (PAWS), 539 Castro St, San Francisco, CA 94114; (415)241-1460.

PAWS: Los Angeles, 7221 Santa Monica Blvd, Ste B, West Hollywood, CA 90046;(213)876-7297

PAWS: Chicago, 1153 N Dearborn 321, Chicago, IL 60610;(312)465-3741.

PAWS: Orange County, 3111 Via Santo Tomas, San Jaun Capistrano, CA 92675; (714)489-2898.

PAWS: Philadelphia, 1234 Locust, Philadelphia, PA 19107; (215)985-0206.

PAWS: St Louis, 3952 S Grand Ave, St Louis, MO 63118; (314)865-0188.

PAWS: San Diego, 1278 University Ave San Diego, CA 92103; (619)234-7297.

PETS: Washington DC, 2001 O St NW, Washington, DC 20009; (202)234-7387.

Pet Support Network, 1824 12th Ave, Seattle, WA 98122; (206)322-5444.

Pet Owners With AIDS/ARC Resource Service (POWARS), PO Box 1116, Madison Square Station, New York, NY 10159; (212)744-0847.

POWARS: Baltimore, PO box 39364, Baltimore, MD 21212; (410)783-8823.

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