Understanding biological and epidemiological characteristics of important zoonoses is necessary if we are to implement effective control strategies.
Diseases transmissible from animals to humans are termed "Zoonoses". Published surveys indicate that pet owners are scarcely aware of the myriad of zoonotic disease agents that pets can harbor. In fact, few could name a single disease other than rabies. In the following, I will overview important parasitic zoonoses of companion animals. Understanding biological and epidemiological characteristics of important zoonoses is necessary if we are to implement effective control strategies.
Toxocara spp. ("roundworms")
Roundworms of dogs and/or cats (Toxocara canis, T. cati) are large (up to 4.5 inches), stout worms that live as adults in the lumen of the small intestine. T. canis is the species commonly found in dogs, T. cati is restricted as adult worms to cats. Both T. canis and T. cati usually undergo hepatotrachael migration prior to establishment in the small intestine. In older dogs and cats, a greater number (but not all) of migrating larvae are diverted to extra-intestinal tissues. The period of time from exposure to the parasite until mature worms are present in the intestine varies based on the route of infection. Generally, this period is between 2 and 5 weeks.
T. canis and T. cati remain prevalent in pets, based on recent surveys. Once such survey indicated that T. canis eggs were present in the feces of almost 15% of 6,458 dogs sampled from shelters in the United States. Although prevalences were reduced somewhat in adult dogs, the survey results indicate that T. canis is not restricted to puppies.
T. canis is a common parasite of dogs, regardless of geographic location, because of the potential for infection by several routes. These include embryonated eggs, transplacental transmission, transcolostral transmission (less common for T. canis), and by ingestion of transport hosts such as rodents and rabbits. Transplacental transmission accounts largely for the prevalence of T. canis in neonatal and juvenile dogs. Although age-associated immunity aids in the expulsion of some T. canis adults as dogs age, it is not completely effective in elimination of the parasites.
T. canis is important not only because of its ability to produce primary disease in dogs, but also because of its ability to produce several extra-intestinal disease syndromes known as "larva migrans" in many hosts, including humans. When ingestion of embryonated eggs results in migration and damage to internal organs, the syndrome is referred to as visceral larva migrans (VLM). VLM is observed most often in children less than 3 years of age. Encysted larvae induce nodules in organs such as liver, lungs, kidney and brain. Such infections generally manifest as profound eosinophilia, pneumonitis and hepatomegaly. Serological surveys suggest that exposure rates to Toxocara larvae vary from 3% in one US study, to 23% in other studies, depending on the region, socioeconomic group that is tested, and whether the test population resides in urban or rural areas. In older children (generally 3-13 years) the larvae apparently have a more pronounced predilection for the posterior chamber of the eye. The resulting granulomatous retinitis is the hallmark of this second syndrome known as ocular larva migrans (OLM). OLM can result in severe ocular damage and subsequent retinal detachment, loss of vision, and even blindness. Interestingly, OLM can occur in the complete absence of eosinophilia and signs or evidence of VLM. One graphic example of the potential for Toxocara spp. to cause ocular disease was the report in which an Atlanta, GA ophthalmology practice indicated that 37% (41 cases) of retinal diseases in children seen in children during a 18 month period were caused by Toxocara spp. Although T. cati is thought to be associated less often with human infections, recent research indicates that it too can cause them.
Adult female roundworms are prolific egg producers. For example, females of T. canis are estimated to produce between 25,000 and 85,000 eggs per day. Females of T. cati are capable of producing between 19,000 and 24, 000 eggs per day. Given these rates of egg production, it is easy to see how environments can eventually harbor large numbers of eggs. Parasite reproductive rates, combined with the resistance of embryonated eggs to adverse environmental conditions, can increase the risk of exposure and infection to both pets and humans. Roundworms infections can be controlled either by strategic deworming with narrow or broad spectrum agents or by repeated monthly administration of available broad spectrum heartworm preventives.
Baylisascaris procyonis ("raccoon ascarid")
Baylisascaris procyonis, is a prevalent and important parasite of raccoons. It is also known to infect dogs. However, such reports are rare. Because, infected dogs can pass eggs in their feces, they should be treated (see below) and precautions should be taken to prevent human exposure to environments that infected dogs have been exposed to. Baylisascaris is similar in structure and behavior to Toxocara spp. dogs and cats. However, it is not its disease consequences in raccoons that are important, but its capability to cause larva migrans in many other hosts. The raccoon has adapted well to encroachments by humans into its habitats. Given the high prevalences of Baylisascaris infection in raccoons (68%-82% in surveys in the United States), the raccoon's broad geographic range, and prevalences in urban environments, it is easy to see why B. procyonis is the most common and widespread cause of larva migrans in animals. Although larvae of Baylisascaris can invade a variety of tissues in man and other animals, including the eye, it is particularly prone to invasion of the central nervous system. The resulting "neural larva migrans" is the most serious of the migrans syndromes in humans or animals. The seriousness of the condition is a factor of rate of growth and size achieved by larvae compared to other ascarids. Documented infections in humans have resulted in severe, sometimes fatal encephalitis.
Baylisascaris is particularly prevalent in young raccoons, resulting in very high fecal egg shedding rates. The high shedding rates, combined with the raccoon's habit of using communal defecation sites ("latrines"), can result in environments with astonishingly high egg numbers. When these contaminated areas occur in close proximity to urban developments, the risk of human infections increases immensely. Veterinarians should discourage clients from feeding raccoons or adopting them as pets. Clients should also be advised of the potential for environmental contamination with eggs, particularly sites such as fallen trees, tree stumps, and woodpiles that might serve as communal latrines. Baylisascaris procyonis infections can be treated with a number of parasiticides including, pyrantel pamoate, Drontal Plus (febantel, pyrantel pamoate and praziquantel), milbemycin oxime, and fenbendazole.
Ancylostoma spp. ("hookworms")
Canine and feline hookworms are small (up to about 0.75 inches) whitish or reddish-brown worms with a hooked anterior end (hence the name). As adults, they reside in the small intestine of dog, cats and rarely humans. Ancylostoma spp. include A. caninum (the universally distributed canine hookworm), and A. braziliense (found in both dogs and cats in the subtropical US). In the survey mentioned above, A. caninum eggs were recovered from almost 20% of 6,458 fecal samples from shelter dogs.
Developmental cycles of hookworms include a free living phase in which larvae hatch from eggs and develop through 3 distinct stages. The 3rd environmental larval stage (infective stage) enters the host either by oral ingestion or by skin penetration. Most (but not all) orally ingested larvae establish in the intestine without extraintestinal migration. Those that penetrate the skin follow a vascular/pulmonary migration prior to their establishment in the small intestine. In addition, both prenatal (transplacental) and transmammary modes of transmission can occur. The reservoir for such larvae is somatic as is the case with T. canis.
Hookworms may cause dermal disease, pulmonary disease and intestinal disease. The latter is the most common syndrome in the dog. Hemorrhagic enteritis caused by A. caninum can be a peracute, life-threatening disease in young dogs. In these animals, the transmammary route of infection can lead to the establishment of very high worm burdens in neonatal dogs in a short period of time. The remaining species are less significant pathogens, but not always innocuous. Ancylostoma caninum, similar to T. canis, is a prolific egg producer. It is estimated that mature females of A. caninum can produce up to 20,000 eggs per day. This magnitude of fecundity can result in substantial environmental reservoirs of infective larvae in rather short periods of time.
Free-living infective larvae of some Ancylostoma spp. may penetrate the skin of humans and migrate subsequently for short periods of time. These dermal wonderings result in reddish, pruritic, serpentine lesions. This condition is referred to as cutaneous larva migrans (CLM) or "creeping eruption". Although less significant than the larva migrans syndromes caused by the roundworms, the cutaneous syndrome caused by the hookworms remains a concern for veterinarians and pet owners. Larvae of Ancylostoma braziliense appear to be the most common cause, although cases of CLM caused by A. caninum have been documented. Recent evidence suggests that adults of A. caninum may also inhabit the intestines of humans. More than 200 such cases of "eosinophilic enteritis" have now been reported in the medical literature. Human infections with adult A. caninum can result in both acute and chronic signs. Clinical signs included recurrent abdominal pain, small bowel thickening, eosinophilia, increased levels of IgE and also inflammation of the distal ileum and colon.
As discussed for roundworms, hookworm infections can be controlled either by strategic deworming with narrow spectrum or broad spectrum agents, or by repeated monthly administration of available broad spectrum heartworm preventives.
Dipylidium caninum ("flea tapeworm", cucumber seed tapeworm")
Dipylidium caninum is a common tapeworm of dogs and cats. It is transmitted by consumption of fleas usually during the pet's self-grooming. Human infections with D. caninum occur when fleas are inadvertently ingested, usually by small children. Although not usually of pathogenetic significance, infections in children are a cause of considerable alarm and distress among parents and care-givers when proglottids are passed in feces or are found in soiled diapers. Human infections are best prevented by controlling D. caninum in dog and cat hosts. Flea control is a must is complete elimination of D. caninum is to be expected. Both narrow spectrum, combination products and combination products with heartworm preventive capabilities are available for elimination of both Dipylidium and Echinococcus (see below).
Echinococcus spp. ("hydatid tapeworms")
Many tapeworms of dogs or cats are of little primary disease importance and present little danger to either humans or domesticated animals (exceptions are Dipylidium and Echinococcus spp.). Echinococcus species (hydatid tapeworms) are important exceptions. Human and animal echinococcosis, acquired through contact with the feces of infected canids or felids, is a potentially serious disease, requiring constant surveillance by knowledgeable, trained personnel. Echinococcus granulosus uses canids as definitive hosts and many omnivores and herbivores as intermediate hosts. Echinococcus multilocularis uses canids and felids as definitive hosts and microtine rodents (voles, lemmings, muskrats, water rats) as principal intermediate hosts. Echinococcus granulosus and E. multilocularis undergo complex cycles of development involving the following morphologically distinct stages: (1) the adult tapeworm (2-11 mm) which inhabits the small intestine of the canine or feline definitive host; (2) the egg, which contains the larval tapeworm (oncosphere); and (3) the metacestode, which contains infective protoscolices in either unilocular or multilocular cysts within the intermediate host. The oncosphere is enclosed within a striated wall (embryophore), which renders the eggs similar in appearance to those of Taenia spp. The metacestode (hydatid) is the replicative stage in the life cycle during which the parasite increases its numbers. When fully developed, the hydatid of E. granulosus consists of a single (unilocular) fluid-filled cyst. The cyst wall is a multilaminar structure which gives rise to brood capsules, each containing numerous protoscolices. The hydatid of E. multilocularis is alveolar-like and grows by outward budding of the germinative layer. Invasive growth into surrounding tissues forms many adjacent chambers (hence alveolar or multilocular) containing protoscolices. Both E. granulosus and E. multilocularis are transmitted through predator-prey cycles. In each instance, the carnivore definitive host becomes infected by ingesting the larval metacestode (hydatid containing protoscolices) within the intermediate host. Eggs and disintegrating gravid proglottids, excreted in the definitive host's feces, are dispersed widely in the environment. Intermediate hosts (including humans) ingest eggs and become infected. Oncospheres are liberated in the intermediate host's intestinal tract and are distributed to many extraintestinal sites via the venous and lymphatic systems. Development leads to the formation of a fluid-filled unilocular hydatid (E. granulosus) or a multilocular hydatid (E. multilocularis) in many organs. The life cycle is completed when the definitive host ingests the hydatid stage within the viscera of the intermediate host. Disease in intermediate hosts is caused by either the unilocular or multilocular hydatid cyst. In intermediate hosts, cysts of E. granulosus are usually found within the liver and lungs. Other less common sites include kidneys, spleen, heart, bones, and CNS. Disease caused by E. multilocularis is more serious than that caused by E. granulosus. The infection is progressive and malignant. Most multilocular hydatid cysts locate in the liver, rarely in other organs.
Fecal flotation is not a reliable means of demonstrating Echinococcus infections in definitive hosts. The eggs are similar to those of taeniid tapeworms, and they are excreted erratically in feces. Diagnosis of hydatidosis in intermediate hosts such as livestock or wildlife is best accomplished at necropsy of suspect animals. An array of advanced techniques including radiography, computerized tomography, ultrasonography and scintigraphy has been applied to antemortem diagnosis of human infections. Such procedures, augmented by immunologic assays have proved useful in the detection of human infections. Cestocides are available for treatment of both juvenile and adult Echinococcus tapeworms in definitive and intermediate hosts. Treatment of infected dogs or cats with effective cestocides is the best means of control in urban environments. As mentioned above for Dipylidium, narrow spectrum products , combination products and combination products with heartworm preventive capabilities are available for elimination of Echinococcus infections in dogs if they are encountered.
Giardia spp. are dimorphic enteric flagellates that infect the intestine a wide range of vertebrate hosts. The genus Giardia consists of several valid species that parasitize mammals, birds, and amphibians. Giardia duodenalis, the principal species, can be further divided into at least 7 different genotypes. Human infections are usually caused by assemblage A (rarely B). Most Giardia infections are specific to hosts that they infect. For example G. duodenalis genospecies C & D are common in dogs and are not thought to infect humans. Giardia duodenalis genospecies F is thought only to infect cats. At this point humans infections in the United States have not been attributed to either of genospecies C, D, or F.
Giardia stages consist of a flagellated, binucleate trophozoite, and a quadrinucleate cyst . The trophozoite attaches to the surface of epithelial cells in the small intestine; formation of cysts occurs in the ileum, cecum or colon. Like Cryptosporidium, cysts of Giardia are immediately infective when passed in feces. Infections result from ingestion of cysts in contaminated environments, food, and water.
Although the mechanism(s) of Giardia-induced disease remains unknown, evidence suggests that the disease is likely multifactorial involving inhibition of brush border enzymes or other factors such as altered immune responses, nutritional status of the hosts, presence of intercurrent disease agents, and the strain or genotype of Giardia involved in the infection. Most infected animals remain asymptomatic, The most common presenting sign in clinically affected animals and humans is small bowel diarrhea. Feces are usually semi-formed, but may be liquid. Blood usually is not present in animal infections. Feces have been described as pale (often gray or light brown), fetid and containing large amounts of fat. Dogs or cats with giardiasis may present with poor body condition, weight loss, and occasional vomiting. It is not unusual to find Giardia coincidentally with other gastrointestinal diseases such as inflammatory bowel disease.
Giardiasis is best diagnosed by fecal flotation using zinc sulfate (specific gravity = 1.18-1.20). Centrifugation of the preparation increases the likelihood of recovering cysts. Also, the addition of a small amount of Lugol's iodine to the slide prior to placement of the coverslip will aid in visualizing the small (10-12 •m) cysts. Use of barium sulfate, antidiarrheals or enemas prior to sampling feces may interfere with detection of cysts and should be avoided if possible. Other diagnostic techniques that can be used to recover trophozoites, cysts, or proteins produced by the parasite include direct examination of feces (wet-mount), immunofluorescent procedures, and ELISA. These techniques are either too insensitive (direct examination) or impractical for the practicing veterinarian because of cost, necessary equipment or because of the effort required to conduct the test.
Given that cysts of the different genotypes are not differentiable based on their structure, it is best to be conservative about the potential for human infections with animal genotypes of Giardia. Consequently, it is my view that all animals that are positive by fecal examination should be treated. Several options are available for treatment of Giardia infections in dogs or cats. Options include fenbendazole (50 mg/kg X 3-5 days), metronidazole (25 mg/kg BID X 5 days [dog]; 10 mg/kg BID X 5 [cat]), Drontal Plus - (Bayer – approved dose for 3 days), tinidazole (50 mg/kg SID), nitaxoxanide (100 mg BID X 3 [up to 45 lbs]); 200 mg/kg BID X 3 [45-90 lbs]) It is good practice to treat all animals in a household or kennel that have had contact with infected animals. Bathing animals to remove adherent fecal debris can aid in the control of giardiasis. Provide all animals with clean water since contaminated water is a common source of infection for both humans and animals. A commercial vaccine is available to aid in the prevention and control of giardiasis in dogs and cats. Though normally not considered a first line vaccine, vaccination for Giardia should be considered for pets in multiple-pet households, kennels or catteries, or in situations in which giardiasis has been a problem. It has also been suggested that the vaccine might augment treatment of giardiasis in certain problem cases.
Cryptosporidium spp. are small, intracellular coccidia-like protozoans that can infect a variety of tissues and organs in vertebrate hosts. Most Cryptosporidium spp. that infect mammals undergo development at the luminal end of enterocytes of the small intestine. However, when either medications or diseases such as AIDS alter the hosts immune system, Cryptosporidium spp. may spread to less common sites such as the stomach, lung, or ducts associated with the liver or pancreas.
At present, there are 15 recognized species of Cryptosporidium. The most important of the valid species are C. parvum, a causative agent of cryptosporidiosis in many species of mammals and C. canis/C. felis in dogs and cats. Cryptosporidium parvum can be further divided into at least 6 different genotypes or cryptic species, based on molecular characterizations and host specificity. It is important to note that at least two genotypes of C. parvum and perhaps 6 additional species of Cryptosporidium are capable of infecting humans. The developmental cycle of Cryptosporidium includes asexual and sexual stages similar to stages in the life cycles of canine and feline coccidia. Similarly, the life cycle of Cryptosporidium culminates in the production of resistant oocysts that are shed immediately infective with feces into the infected host's environment. This differs from most other coccidia, which require a period of time to develop to the infective sporulated oocyst. Oocysts of Cryptosporidium spp. can remain viable for many months, if protected from extremes of temperature and from dessication. Available data suggest that human cryptosporidiosis results from ingestion of oocysts shed into the environment from other humans, farm animals, companion animals, or by consuming contaminated food, drinking water, or recreational water.
Clinical signs of cryptosporidiosis in animals and humans include diarrhea, abdominal pain, dehydration, and weight loss. Both human and animal cryptosporidiosis are usually self-limiting diseases lasting little more that 2 weeks. However, in hosts with abnormal immune responses (including immunocompromised humans), cryptosporidiosis can be a chronic, life-threatening disease.
Diagnosis of cryptosporidiosis in animal or humans can be confirmed by detection of oocysts or Cryptosporidium-specific antigens in feces. Oocysts are small (4-6 •m) and difficult to visualize using standard fecal flotation procedures. Commercially-available fluorescent antibody kits can aid in visualization of oocysts, but require an epifluorescence microscope. ELISA kits are available for detection of fecal antigens, but they are expensive and require strict adherence to step by step procedures. At present, the only approved drug for treatment of cryptosporidiosis is nitazoxanide (Alinia®, Romark Laboratories - 100 mg BID X 3 [up to 45 lbs]); 200 mg/kg BID X 3 [45-90 lbs])). Other agents such as paromomycin (125-165 mg/kg twice daily for 5 days (dog and cat), azithromycin (5-10 mg/kg twice daily for 5-7 days [dog]; 7-15 mg/kg twice daily for 5-7 days [cat] and tylosin (10-15 mg/kg three times daily for 14-21 days) also have been reported to have activity against Cryptosporidium.
Toxoplasma gondii is a ubiquitous protozoon parasite that infects virtually all warm-blooded vertebrates. It is estimated that up to 33% of humans worldwide possess circulating antibodies to T. gondii, implying either active infection with the parasite or prior exposure. Three distinct structural stages comprise the life cycle of T. gondii: Sporozoites within infective oocysts, tachyzoites in pseudocysts or groups, and bradyzoites in tissue cysts. Domestic cats and other felids serve as definitive hosts for T. gondii. All remaining hosts, including humans, serve as intermediate hosts. Within intermediate hosts, the parasite replicates as asexual tachyzoites. These stages divide quickly (hence the name), destroying cells and organs in which they develop. Tachyzoites can infect many different cells and organs, which accounts for the multi-systemic nature of the disease. Eventually, tachyzoites transform into slowly dividing bradyzoites and are enclosed by a cyst wall. Bradyzoites remain inactive until they are ingested by definitive hosts. Within the intestinal tract of felids, T. gondii undergoes a typical coccidia-like life cycle which culminates in the production of oocysts that are passaged in feces. The greatest number of oocysts are shed by kittens during their first infection. During these shedding events, millions of oocysts can be passaged during a short patent period of about 2 weeks. It was once believed that after an initial infection and subsequent oocyst shedding, cats remained immune to the parasite and would passage oocyst again. However, recent research indicates that after lapses of several years, it is possible for cats to passage oocysts if tissue cysts are ingested.
Once in the environment, oocysts develop to the infective stage in 1 to 5 days. Sporulated oocysts can remain viable for many months in protected environments such as damp soil. Intermediate hosts (including humans) are infected by ingestion of sporulated oocysts from the environment, or by consumption of raw or undercooked tissues that contains cysts. The tachyzoite is the stage that crosses the maternal fetal interface and infects the developing fetus in utero. Infection by this route is referred to as congenital toxoplasmosis. If infection occurs after birth, usually after ingestion of sporulated oocyst or tissue cysts in raw or undercooked meat, the disease is referred to as acquired toxoplasmosis.
In immunocompetent humans, toxoplasmosis is either an inapparent, asymptomatic infection, or a brief flu-like illness. Persons experiencing the latter usually present with fever, malaise and enlarged, inflamed lymph nodes. Toxoplasmosis can be a severe, life threatening disease in immunocompromised persons, especially those with AIDS. In such cases, resting bradyzoites within tissue cysts in the brain revert to the tachyzoite stage and divide repeatedly. Rapid reproduction of the parasite, unimpeded because of a compromised immune response, results in severe brain disease or toxoplasmic encephalitis.
In about 10% of cases, congenital toxoplasmosis results in abortion or neonatal death. Newborns can also suffer from the classic triad of retinochoroiditis, intracranial calcification, and hydrocephalus. Others develop a complex of symptoms including fever, anemia, convulsions, splenomegaly, hepatomegaly and lymphadenopathy. Those infants that survive infection during the post-natal period can suffer from progressive neurological deficiency. Many of these children require specialized care for the remainder of their lives.
Feline toxoplasmosis, when it occurs, usually results in systemic disease. Symptomatic cats often present with dyspnea, polypnea, icterus, and abdominal discomfort. Ocular disease, characterized by uveitis and retinochoroiditis is also common in cats with systemic toxoplasmosis.
Toxoplasmosis can be prevented by avoiding contact with sporulated oocysts in the environment and avoiding consumption of raw or undercooked meat. This can be achieved by washing hands after exposure to soil, sand, raw meat or unwashed vegetables, cooking or freezing meat thoroughly, avoiding untreated drinking water, and for pregnant women, allowing someone else to change the cat litter tray.
Both fecal examination and serological techniques can be used to detect either intestinal infection (oocyst shedding) in cats or systemic infection in cats and other hosts. It is important to remember that cats generally shed detectable oocysts for short periods of time. Negative fecal results only confirm that the cat is not currently shedding oocysts. Shedding could have occurred prior to fecal examination or could occur at some time in the future. Also, cats may be seronegative at the time that they are shedding oocysts. Therefore results of fecal examination and serologic tests must be interpreted with some caution. Positive serologic tests can be helpful in either diagnosing or ruling out systemic toxoplasmosis.
A number of drugs including sulfonamides, clindamycin, and pyrimethamine can be used to treat systemic toxoplasmosis or reduce oocyst shedding in cats.
1. Purchase or adopt animals from reputable breeders and shelters that maintain only healthy animals. Animals less that 1 year of age are more likely to be infected with potentially zoonotic agents. However, this is not always the case.
2. Establish and maintain regular veterinary visitation schedules (i.e. at least annually) for vaccines, fecal examinations, and wellness examinations. Remember that certain important parasites are not eliminated by broad spectrum parasite control products.
3. Use broad spectrum internal parasite control products, particularly those used primarily for heartworm prevention or ectoparasite control that also possess activity against other internal parasites (i.e. Toxocara spp., Ancylostoma. spp.)
4. Consult with your veterinarian regarding all cases of diarrhea in dogs and cats. Consider seeking medical advice if prolonged diarrhea occurs coincidentally in pets and pet owners. This is particularly important for persons who are immunocompromised.
5. Support leash and fecal removal laws and policies in pet exercise areas and public places.
6. Feed pets only commercially prepared, complete rations. Do not feed animals raw or undercooked meat, or allow them to hunt and consume prey.
7. Avoid feeding wildlife such as raccoons. This behavior encourages their immigration into developed human environments and exposure to potential zoonotic agents.
Pet owners should discuss concerns about potential zoonoses with veterinarians, physicians, trained parasitologists, or infectious disease and public health experts. They should not presume that all information from sources such as lay publications, the Internet, and email groups is either accurate or up to date.
References available on request