Enteric Zoonoses

Michael Lappin United States

Visceral larval migrans can occur in humans following infection by Toxocara canis, Toxocara cati, or Baylisascaris procyonis eggs. Following ingestion of infectious eggs, larvae penetrate the intestinal wall and migrate through the tissues leading to eosinophilic granulomatous reactions involving the skin, lungs, central nervous system, and eyes. Ocular larva migrans most commonly involves the retina and can cause reduced vision, strabismus, uveitis and endophthalmitis. Adult T. cati have been detected in some infected children. Cutaneous larval migrans can be induced with infection by three species of hookworms infecting dogs and cats in the United States: Ancylostoma caninum, Ancylostoma braziliense, and Uncinaria stenocephala. Larvae are released from eggs passed into the environment in feces; infectious larvae infect humans by skin penetration. Larval migration results in the development of an erythematous, pruritic cutaneous tunnel. Occasionally, larvae will reach the lungs and cornea. Ancylostoma caninum has been linked with eosinophilic enteritis in humans. Prevention revolves around control of animal excrement in human environments. Since hookworm and roundworm infections are sometimes occult, anthelmintics such as pyrantel pamoate should be routinely administered to all puppies and kittens at least twice, 14 to 21 days apart. In high-risk puppies, pyrantel could be given every two weeks from two to eight weeks of age. In high-risk kittens, pyrantel could be given at 6, 8, and 10 weeks of age. Fecal flotation should be performed as well to assess for other parasites. Fecal flotation should be performed once or twice yearly on all dogs and cats, particularly if they go outdoors, and even if they are on heartworm preventatives.

Dipylidium caninum, Echinococcus granulosa, and Echinococcus multilocularis are cestodes that can infect humans. Transmission to humans occurs following ingestion of the intermediate host (flea, Dipylidium) or by the ingestion of eggs (Echinococcus). Dogs and cats can be the definitive hosts of Echinococcus spp. Dipylidium infection is most common in children and can lead to diarrhea and pruritis ani. Following human ingestion of eggs, Echinococcus enters the portal circulation and spreads throughout the liver and other tissues. Prevention and/or control is primarily by use of taeniacides and sanitation procedures. Praziquantel has been shown to be effective for the treatment of echinococcosis in pets.

The enteric protozoans infecting dogs and cats that can be zoonotic include Entamoeba histolytica, Balantidium coli (dogs), Cryptosporidium parvum, C. felis, Giardia spp., and Pentatrichomonas hominus. Cysts do not form following infection of cats by Entamoeba or Pentatrichomonas and so these parasites are unlikely to lead to infection of humans following exposure to cats; both genera are rare in dogs as well. Metronidazole may be effective for the treatment of E. histolytica, B. coli (dogs), Giardia spp., and P. hominus in some animals. Some trichomonads are resistant to metronidazole but respond clinically to paromomycin (see cryptosporidiosis).

Giardia is a flagellate with worldwide distribution that causes significant gastrointestinal disease in dogs, cats, and people. The organism is felt to have a wide host range; mammalian isolates are all currently classified as G. lamblia. Using DNA sequences from a number of different genes, there appears to be two or three genotypes of Giardia in people as well as two distinct genetic groups isolated exclusively from dogs. However, whether these genotypes vary in biologic activity including zoonotic potential is for the most part unknown. There have been varying results concerning cross-infection potential of Giardia spp. isolates. In one study, Giardia spp. from humans was inoculated into cats; the cats were relatively resistant to infection. In contrast, evaluation of human and feline Giardia spp. isolates by isoenzyme electrophoresis suggests that cats could serve as a reservoir for human infections. Since it is impossible to determine zoonotic strains of Giardia spp. by microscopic examination, it seems prudent to assume feces from all dogs and cats infected with Giardia spp. to be a potential human health risk. Giardia is a common enteric pathogen in dog and cat studies and can be detected in feces of animals with and without diarrhea. These findings emphasize that fecal examination should be performed on all dogs and cats, at least yearly, and treatment with anti-Giardia drugs like praziquantel-pyrantel-febantel, fenbendazole, or metronidazole should be administered if indicated. Albendazole is also effective for the treatment of giardiasis but has been associated with neutropenia. Vaccination against Giardia could be considered in animals with recurrent infection; this practice is being evaluated as a therapeutic.

Infection of people with the coccidian parasite Cryptosporidium parvum results in severe gastrointestinal tract disease; infection of immunosuppressed individuals may be life threatening. Infection is common in humans; approximately 300,000 people in Milwaukee developed cryptosporidiosis when a water purification system malfunctioned, approximately 10�20% of AIDS patients are infected with C. parvum at some time during their life, and the organism commonly causes diarrhea outbreaks in daycare centers. Many infected individuals require hospitalization for administration of intravenous fluid therapy; people with AIDS may never be cured. Cryptosporidiosis has been documented in people as well as cats or dogs in the same environment suggesting the potential for zoonotic transfer exists. Cryptosporidium parvum oocysts have been documented in feces of many domestic dogs and cats in the United States, Japan, Scotland, Australia, and Spain.

Presence of serum antibodies can be used to estimate numbers of individuals exposed to C. parvum. An enzyme-linked immunosorbent assay for detection of C. parvum IgG was developed and applied to serum of cats. Using this assay, the seroprevalences of C. parvum antibodies in serum of cats in Colorado and the United States are 15.3% and 8.3%, respectively. Oocysts or antigens of C. parvum were detected in feces of 5.4% of cats tested and 6.0% of dogs tested in north-central Colorado. These results suggest that C. parvum infection is common in dogs and cats. It is usually undetermined where people acquire C. parvum infection; contaminated water is the most likely source, but contact with infected dogs or cats is also possible. There have been limited cross-infection studies performed with C. parvum isolates from cats or dogs. In one study, a feline isolate failed to cross infect mice, rats, guinea pigs, or dogs. In another study, a C. parvum isolate from a cat cross-infected lambs. An alternative to cross-infection studies is comparison of isolates genetically. Canine and feline genotypes that vary considerably from human and cattle genotypes have been identified. The feline and canine genotypes were documented in an infected human and the feline genotype was documented in an infected cow suggesting the genotypes can infect other mammals.

As for Giardia, it is impossible to determine zoonotic strains of C. parvum by microscopic examination thus, it seems prudent to assume feces from all dogs and cats infected with C. parvum to be a potential human health risk. Techniques for the detection of C. parvum should be included in the diagnostic evaluation of dogs and cats with diarrhea and all dogs or cats in the homes of immunosuppressed individuals. Infected cats and dogs generally do not shed large numbers of Cryptosporidium oocysts and so acid-fast staining, immunofluorescent antibody staining of feces, or fecal antigen ELISA will aid in the identification of the extremely small oocysts (5 microns).

Paromomycin (Parke-Davis, Morris Plains, NJ) administered at 165 mg/kg q12h PO, for five days is the drug of choice for cryptosporidiosis and is an alternate drug for Pentatrichomonas and Giardia, but has been associated with acute renal failure and deafness in some cats with hemorrhagic diarrhea. Sequential administration of clindamycin (Antirobe, Upjohn Co.) followed by tylosin blocked oocyst shedding and resolved diarrhea in one cat with chronic, clinical cryptosporidiosis. Prevention of these parasites revolves around controlling exposure.

Toxoplasma gondii is one of the most common small animal zoonoses; approximately 30�40% of adult humans in the world are seropositive, suggesting previous or current infection by T. gondii. People are most commonly infected by T. gondii after ingestion of sporulated oocysts or ingestion of tissue cysts. Thus, prevention of toxoplasmosis in people can be achieved by avoiding those two life stages.

Fortunately, clinical disease is generally mild following primary infection of immunocompetent people. Self-limiting fever, malaise, and lymphadenopathy are the most common clinical abnormalities and the majority never realizes when their first T. gondii infection occurred. The disease is potentially confused with infectious mononucleosis. Clinical disease can be much more severe in immunosuppressed individuals. At particular risk: the fetus, people with AIDS, and people treated with immunosuppressive agents for the treatment of cancer and to prevent organ transplant rejection. Toxoplasma gondii is a common opportunistic CNS infection of people with AIDS; as T-helper cells counts decline, toxoplasmic encephalitis from activation of bradyzoites in tissue cysts can result. If a mother has her first T. gondii infection during gestation, stillbirth, CNS disease, and ocular disease are common clinical mani�festa�tions in the fetus. The importance of T. gondii as a zoonotic disease should not be underestimated. Cat owners with potentially immunosuppressive diseases are commonly counseled by human health care providers to adopt or euthanatize their pet cats due to risk of acquiring toxoplasmosis. However, it is very difficult to acquire toxoplasmosis from an individual cat; most people are infected by ingesting sporulated oocysts from the environment or by ingesting tissue cysts in undercooked meat.

Once passed into the environment, sporulated oocysts survive for months to years and so it is likely that many people acquire toxoplasmosis when working with soil or drinking contami�nated water. Clinical toxoplasmosis developed in a group of people following a common exposure in a riding stable and in a group of soldiers drinking contaminated water in Panama. All water collected from the environment should be boiled or filtered prior to drinking. Care should be taken to wash hands carefully after working with soil; alternately gloves should be worn. Produce from the garden should be washed carefully prior to ingestion. The children�s sandbox should be covered when not in use. If cats are owned, a litterbox liner should be used and the litterbox should be cleaned daily; oocysts require 1�5 days to sporulate. Immunosuppressed or pregnant cat owners should not clean the litterbox. Sporulated oocysts are extremely resistant to most disinfectants; it requires exposure to 10% ammonia for 10 minutes to inactivate this stage of the parasite. Thus, cleaning with scalding water or steam is most practical.

Veterinarians are commonly consulted concerning the risk of individual cats for the zoonotic transfer of T. gondii. While it cannot be stated definitively that a person will not acquire toxoplasmosis from their personal cat, it is probably unlikely. It is true that cats are the only definitive host for toxoplasmosis but oocysts are only shed for days to several weeks following primary inoculation. Thus, an individual cat will be passing oocysts into the human environment for only a small fraction of its entire life span. Following primary inoculation of cats, it is difficult to induce repeat oocyst shedding. Prednisolone administered at 10�80 mg/kg PO or methylprednisolone administered at 10-80 mg/kg IM will induce repeat oocyst shedding in some cats with toxoplasmosis. However, these doses are not routinely used in clinical practice. Administration of methyprednisolone acetate administered at 5 mg/kg, weekly for four to six weeks to cats infected with T. gondii for 14 weeks or 14 months failed to induce oocyst shedding.

Cats infected with T. gondii were given FIV followed by FeLV and shown to develop immunodeficiency associated syndromes (unpublished data), however, repeat T. gondii oocysts shedding could not be demonstrated. Cats with FIV or FeLV infections have been inoculated with T. gondii; oocyst shedding periods and number of oocysts shed were similar to those for cats without FIV or FeLV infections. It has been shown that gut immunity to T. gondii in cats is not permanent; four of nine cats inoculated six years after primary inoculation shed oocysts even though each had high serum antibody titers. However, T. gondii infected cats with and without FIV infection failed to repeat oocyst shedding when reinfected with T. gondii 16 months after primary inoculation. Thus, cats that are exposed to T. gondii frequently probably do not shed large numbers of oocysts after the first infection.

Toxoplasma gondii oocysts are not infectious when passed by cats; sporulation requires one to five days in the environment. Most cats are fastidious and do not leave feces on their fur for this period. Bioassay failed to detect oocysts on the fur of cats seven days after they were shedding millions of oocysts in feces. These findings suggest that touching individual cats is an unlikely way to acquire toxoplasmosis; this hypothesis is supported by epidemiologic studies as well. In general, veterinary health care providers are no more likely than the general population to be seropositive for T. gondii infection. Since oocysts are passed unsporulated and non-infectious, working with fresh feline feces (< 1 day old) is not a risk for veterinary health care personnel. People with HIV infection that owned cats were not more likely to acquire toxoplasmosis during their illness than people with HIV infection that did not have cat contact.

Oocysts measuring 10 X 12 � in a cat fecal sample could be T. gondii. Hammondia hammondi and Besnoitia darlingi are morphologically similar coccidians passed by cats but are not human pathogens. The feces should be collected daily until the oocyst-shedding period is complete; administration of clindamycin (25-50 mg/kg q24h PO), sulfonamides (100 mg/kg q24h PO), or pyrimethamine (2.0 mg/kg q24h PO) can reduce levels of oocyst shedding.

There is no serologic assay that accurately predicts when a cat shed T. gondii oocysts in the past and most cats that are shedding oocysts are seronegative. Most seropositive cats have completed the oocyst-shedding period and are unlikely to repeat shedding; most seronegative cats would shed the organism if infected. But since humans are not probably not commonly infected with T. gondii from contact with individual cats and since serologic test results cannot accurately predict the oocyst shedding status of seropositive cats, testing healthy cats for toxoplasmosis is of little clinical use. Fecal examination is an adequate procedure to determine when cats are actively shedding oocysts but cannot predict when a cat has shed oocysts in the past. If an owner is concerned that they may have toxoplasmosis, they should see their doctor for testing.

Ingestion of T. gondii in tissues can result in human toxoplasmosis. Meats (particularly pork in the United States) should be cooked to medium-well to inactivate tissue cysts. Gloves should be worn when handling raw meats (including field dressing) for cooking, or hands should be cleansed thoroughly afterwards. Freezing meat at -12� C for several days will kill most tissue cysts. Ingestion of raw goat�s milk can also result in human toxoplasmosis.

Salmonella spp., Campylobacter jejuni, E. coli, and Yersinia enterocolitica each infect dogs and cats and can cause disease in humans. Gastroenteritis can occur in both species following infection by these agents; Yersinia enterocolitica is probably a commensal agent in animals but induces fever, abdominal pain, and bacteremia following infection of humans. Dogs are occasionally subclinically infected by Shigella. Helicobacter pylori causes ulcers in people and has been isolated from a colony of cats; the zoonotic risks are currently undetermined. Infected pets and people in the same family have been found to be infected with Helicobacter spp. However, it is possible the human led to the infection of the animal. Salmonella infection in cats and dogs is often subclinical. Approximately 50% of clinically affected cats have gastroenteritis; many are presented with abortion, stillbirth, neonatal death, or signs of bacteremia. If neutrophils are noted on rectal cytology, culture for Salmonella and Campylobacter is indicated. Infection occurs after fecal-oral or fomite exposure and prevention is based on sanitation and control of exposure to feces. Antibiotic therapy can control clinical signs of disease but should not be administered to subclinical Salmonella carriers due to risk of antibiotic resistance. In bacteremic animals, parenterally administered quinolones are usually effective at controlling clinical signs of disease. Salmonella spp. and Campylobacter spp. infections were uncommon in client-owned dogs and cats with and without diarrhea in north-central Colorado; less than 2% of the animals in any group were infected.

References are available on request