Transmission and epidemiology of zoonotic protozoal diseases of companion animals

Abstract

Over 77 million dogs and 93 million cats share our households in the United States. Multiple studies have demonstrated the importance of pets in their owners' physical and mental health. Given the large number of companion animals in the United States and the proximity and bond of these animals with their owners, understanding and preventing the diseases that these companions bring with them are of paramount importance. Zoonotic protozoal parasites, including toxoplasmosis, Chagas' disease, babesiosis, giardiasis, and leishmaniasis, can cause insidious infections, with asymptomatic animals being capable of transmitting disease. Giardia and Toxoplasma gondii, endemic to the United States, have high prevalences in companion animals. Leishmania and Trypanosoma cruzi are found regionally within the United States. These diseases have lower prevalences but are significant sources of human disease globally and are expanding their companion animal distribution. Thankfully, healthy individuals in the United States are protected by intact immune systems and bolstered by good nutrition, sanitation, and hygiene. Immunocompromised individuals, including the growing number of obese and/or diabetic people, are at a much higher risk of developing zoonoses. Awareness of these often neglected diseases in all health communities is important for protecting pets and owners. To provide this awareness, this review is focused on zoonotic protozoal mechanisms of virulence, epidemiology, and the transmission of pathogens of consequence to pet owners in the United States.

Fig 1

Global burden of zoonotic protozoal disease in humans. (Panels D and E are adapted from references and , respectively, with permission of Elsevier.)

Fig 2

Toxoplasma gondii life cycle. Domesticated and wild cats are the definitive hosts of Toxoplasma gondii and become infected after the consumption of animals containing infective tissue cysts. Fecal oocysts are shed in large numbers by acutely infected cats for approximately 2 weeks. After shedding, parasite sporulation into infective oocysts takes place in 1 to 5 days. The ingestion of oocysts by other species leads to the formation of tissue. T. gondii rapidly excysts within the intestine, developing into the highly invasive tachyzoite form. Cellular infection results in bradyzoite-containing tissue cysts.

Fig 3

Canine toxoplasmosis. This section of canine skeletal muscle contains numerous lymphocytes and macrophages with myofibrillar necrosis and fibrosis and a myriad of Toxoplasma gondii tachyzoites (arrowheads) confirmed by immunohistochemistry (magnification, ×40). (Reproduced from a slide by Alexandria University, Department of Veterinary Pathology, Egyptian Society for Comparative and Clinical Pathology, Alexandria, Egypt, from the Armed Forces Institute of Pathology Wednesday Slide Conference 2007-2008, Conference 8, Case 2.)

Fig 4

Giardia sp. life cycle. Giardia cysts shed in the feces are infectious. Infection occurs after the ingestion of cysts either through the fecal-oral route or through the ingestion of contaminated water or food. Cysts are environmentally resistant and can persist for months in soil or water (50). Excystation occurs within the small intestine. Trophozoites remain either free in the intestinal lumen or attached to villous enterocytes, causing clinical signs. Trophozoites encyst upon movement toward the colon, becoming infectious oocysts, and are shed in the feces.

Fig 5

Giardia cyst observed in a fecal flotation from a patient dog at the Iowa State University College of Veterinary Medicine.

Fig 6

Babesia sp. life cycle. Sporozoite-carrying ticks infect a mammalian host while taking a blood meal. Sporozoites enter erythrocytes (RBCs) and reproduce through asynchronous binary fission, resulting in two, or sometimes four, merozoites. Once present in a reservoir host (for B. microti, the reservoir is the white-footed mouse), parasites will develop into male and female gametes. When an ixodid tick feeds upon a competent reservoir, blood-stage gametes are introduced into the gut, where these gametes are fertilized to become zygotes. Zygotes enter the tick salivary gland and undergo a sporogonic cycle, forming infectious sporozoites. Humans are generally an intermediate host of Babesia species, although blood transfusion transmission does occur. Dogs are intermediate hosts, much like humans, although they may have a domestic reservoir role in the human transmission of the newly emerging species Babesia conradae.

Fig 7

B. conradae piroplasms. Parasites are indicated by an arrow. Babesia conradae was present in erythrocytes from a canine patient of the veterinary medical teaching hospital at the University of California, Davis. (Courtesy of Jane Sykes.)

Fig 8

Life cycle of Trypanosoma cruzi. An infected triatome vector or “kissing bug” takes a blood meal from a mammalian host, releasing infective trypomastigotes in feces near the bite wound or mucosae. Infective trypomastigotes enter the mammalian host, penetrating intact mucous membranes, including conjunctiva, or orally through the intestinal tract after food-borne exposure. Trypomastigotes invade cells and replicate near the site of infection, differentiating into intracellular amastigotes. Amastigotes replicate via binary fission within parasitophorous vacuoles, escape into the cytoplasm, and differentiate into trypomastigotes. Trypomastigotes are released from the cell, reaching the bloodstream. Triatome insects become infected through the ingestion of circulating trypomastigotes in mammalian blood meals, transform into epimastigotes within the triatome midgut, and undergo final differentiation into infective trypomastigotes within the insect hindgut.

Fig 9

Neonatal rat cardiomyocytes and a Trypanosoma cruzi trypomastigote with fluorescent immunolabeling. Actin myofilaments are labeled in green, the T. cruzi trypomastigote is labeled in red, and nucleic acids are labeled in blue (DAPI).

Fig 10

The life cycle of Leishmania species. Sandflies inject infective promastigotes into a susceptible mammal during feeding. Promastigotes are phagocytosed by resident phagocytes, transform into tissue-stage amastigotes, and multiply within these cells through simple division. The parasite continues to infect phagocytic cells either at the site of cutaneous infection or in secondary lymphoid organs, with eventual parasitemia. Sandflies become infected through feeding on a host either with an active skin lesion in CL or with parasitemia in VL. Parasites convert to promastigotes within the sandfly midgut. Promastigotes migrate from the midgut and transform into highly infectious metacyclic promastigotes.

Fig 11

Leishmania parasites in culture and in a tissue section. (A) Leishmania amazonensis promastigote from culture with a visible kinetoplast. (Photo by Pedro Martinez.) (B) Zoonotic visceral leishmaniasis in canine spleen. The spleen was enlarged and infiltrated by large numbers of foamy macrophages containing numerous intracellular Leishmania infantum amastigotes (arrows), confirmed by immunohistochemistry (magnification, ×100).