I.      All about Cats

Since felines are the definitive host of T. gondii, it is useful to know about them.

•   Origin, domestication, and early history

Cats were initially domesticated in Turkey, part of the Fertile Crescent, approximately 10,000 years ago, at the time farming was beginning (Driscoll CA, Menotti-Raymond M, Roca AL et al., The Near Eastern origin of cat domestication, Science 2007;317:519–523). It is likely that wild cats were attracted by the mice that accompanied the collections of grain. Given cat behavior as we know it, it also seems likely that cats domesticated themselves rather than being domesticated by humans.

From the beginning, cats were very useful to people in protecting grain and other food supplies, and they continued to be so in this role until recent years. For example, in 1850 a gold miner in California wrote: “This evening old Coe came up with our wagons and brought us a cat. Never were cats in such demand. . . . The whole town is overrun with mice, and they destroy a deal of property for us. . . . We were at once offered an ounce of gold dust for every pound the cat weighed” (Bretnor R, Bring cats! A feline history of the West, The American West, 1978;15:32-­35, 50).

For most of the time from when cats were initially domesticated 10,000 years ago until the end of the 18th century CE, cats were regarded almost exclusively as utilitarian creatures, specifically to kill mice and rats and thus protect food supplies. There are suggestions they occasionally were regarded as pets, but except for ancient Egypt, such examples are rare. For example, in a burial in Cyprus dated to 9,500 years ago, a human and cat were buried together.

The major example of cats being regarded as pets was in ancient Egypt when, approximately 3,500 years ago (1,500 BCE), a local cult worshipping a cat goddess (Bastet) became widespread. Cats were highly valued and often mummified when they died. Herodotus noted the Egyptian fondness for cats when he visited in 450 BCE. The Egyptians attempted to restrict the distribution of cats to other countries and prohibited their export.

The Greeks and Romans kept some cats as mousers, but there is no evidence that pet-keeping was widespread. Some historians claim that ferrets were used more commonly than cats to protect the grain. The Romans are thought to have introduced cats to central and western Europe, including Britain. Cats are thought to have reached India approximately 2,200 years ago (200 BCE) and to have reached China and Japan even later. As trade by shipping became common, cats became essential items on ships to keep the mice, and later rats, under control, and in this manner cats became geographically disseminated. References to cats as companions or pets are rare, and “up until the tenth century the cat is viewed, if not with respect, then with tolerance and as a necessity and asset to the household” (Lynnlee JL, Purrrfection: The Cat, West Chester, Pa., Schiffer, 1990, p. 21).

 •  Modern History

Beginning in the 11th century, tolerance for cats began to decrease in Europe for religious reasons, and “by the 13th century the church viewed witches as real and cats as instruments of the devil” (Lynnlee, p. 20). Dante (1265–1321), for example, mentioned cats only once in his work and compared them to demons. From the 14th century well into the 18th century, cats were regularly killed on specific religious holidays. “By the late 15th century the persecution of cats and witches was a mainstay of European society. . . . The 15th and 16th centuries are almost devoid of any cat literature and art. . . . During this period the cat still was used to control rodents, but it was rarely seen as a pet, for if so its existence and that of its owner were in jeopardy” (Lynnlee, p. 21). Cats became especially associated with heretical religious sects, such as the Waldensians and Manichaeans, and members of these sects were accused of worshiping the Devil in the form of a black cat.

On feast days all over Europe, as a symbolic means of driving out the Devil, they were captured and tortured, tossed onto bonfires, set alight and chased through the streets, impaled on spits and roasted alive, burned at the stake, plunged into boiling water, whipped to death, and hurled from the tops of tall buildings, all in an atmosphere of extreme festive merriment. (Serpell JA, The domestication and history of the cat, in Turner DC and Bateson P, eds, The Domestic Cat, Cambridge, Cambridge University Press, 1988, p. 156).

At Metz, for example, on “cat Wednesday” during Lent, 13 cats were placed in an iron cage and publicly burned; this ritual took place each year from 1344 to 1777 (Kete K, The Beast in the Boudoir, Berkeley: University of California Press, 1994, p. 119).

The rehabilitation of cats began in the 18th century, driven by three things. First was a decline in the belief in witches. Second was the invasion of Europe by the brown (or gray) rat, which replaced the black rat and was more prolific and difficult to control. The brown rat reached Germany in 1753, Sweden in 1762, and Switzerland in 1808. Its multiplication was facilitated by increasing urbanization, and its distribution by increasing sea travel. Cats were increasingly valued in urban areas and on shipboard. “Many administrative authorities began to set aside a special budget for the breeding and maintenance of ratting cats in museums, libraries, prisons, barracks, warehouses and stores” (Méry F, The Life, History and Magic of the Cat, London, Paul Hamlyn, 1967, pp. 56, 59). Finally, as Pasteur’s work on microbes became well known, disease became associated with being dirty, and the cat, by virtue of its cleanliness, was increasingly associated with health.

The earliest modern examples of keeping cats as pets occurred in the mid-18th century, first in Paris and later in London, among artists and writers. Cats became associated with intellectuals. By the early 19th century, descriptions can be found of children playing with cats. Cats began to be used in advertising in the 1850s, and “some cats were seen on paper fans, matchbooks, bookmarkers, and the like” (Lynnlee, p. 28). By the 1870s, interest in cats as pets had become so widespread that writers referred to it as a “cat fever,” “cat cult,” “cat fancy,” or “cat craze.” “Of late years there has been a rapid and promising growth of what disaffected and alliterative critics call the ‘cat cult,’ and poets and painters vie with one another in celebrating the charms of this long-neglected pet” (Repplier AQ, Agrippina, Atlantic Monthly, 1892;69:760). The first cat show in London took place in the Crystal Palace in 1871; the first show in New York was in Madison Square Garden in 1894.

•   Distribution and numbers

As the British colonized the world in the 19th century, they took their cats with them and thereby introduced cats to Canada, Australia, and New Zealand. In 1857 in a popular journal, it was noted that “cats have increased the excitement caused by the arrival of our modern missionaries amongst an isolated and untaught people” (Anonymous, The cat, Household Words, 1857;15:370). In India cats became popular only among members of the upper castes who wished to emulate the British. In many other countries, cats were relatively uncommon and, if they appeared, were regarded as a source of protein rather than as pets. For example, in 1872 “the enormous amount of rats and scarcity of cats” was noted in West Africa (Anonymous, Cats, Chamber’s Journal, 1872;49:178).

Following World War II, cats became very widely distributed around the world, even in the Arctic. Among five Eskimo villages in Alaska north of the Arctic Circle, 8 percent of families owned a pet cat in 1974. Among Skolt Lapps in northern Finland, it was said in 1979 that “practically each family had at least one cat” (Peterson DR, Cooney MK, Beasley RP, Prevalence of antibody to Toxoplasma among Alaskan natives: relation to exposure to the felidae, J Infect Dis 1974;130:557–563; Huldt G, Lagercrantz R, Sheehe PR, On the epidemiology of human toxoplasmosis in Scandinavia especially in children, Acta Paediatr Scand 1979;68:745–749).

In recent years, several cities have been said to be heavily infested with cats. Stockholm has been called the “cat capital of the world,” and Paris is also said to have large numbers. In the Middle East, Istanbul, Damascus, and especially Cairo are also said to have many cats, the latter even having a “cat garden,” originally created by a 13th-century sultan.

Counting cats is notoriously difficult. In the United States, it has been estimated that there are approximately 78 million pet cats, which are found in one-third of all households, and an additional 73 million feral cats, thus totaling 151 million. Britain is said to have about 8 million cats, and Australia to have 20 million, one for every person (Will G, Millions and millions of cats, Washington Post, July 13, 1997). It is well known that, left unchecked, cats reproduce rapidly (Kelson L, The race to outpace feral cat overpopulation, Animal Guardian 1998;4:8).

 •  Cat feces

Cats excrete the oocysts of T. gondii in their feces for two to three weeks when they first become infected, usually as kittens or young cats. This brief two-to-three-week period is generally thought to be the only time during the life of that cat when it is infectious. There is some evidence, however, that some cats may later have a reactivation of their T. gondii infection if they are later infected with other viruses, such as the feline immunodeficiency virus, or are stressed, and they may excrete oocysts and again become infectious at that time (Hall S, Ryan M, Buxton D, The epidemiology of toxoplasma infection, in Joynson DHM, Wreghitt TG, eds, Toxoplasmosis: A Comprehensive Clinical Guide, Cambridge, Cambridge University Press, 2004, pp. 58–124). At any given time, it has been estimated that approximately 1 percent of cats are excreting T. gondii oocysts. One study claimed that “cats can shed as many as 500 million oocysts” during their initial infection (Dubey JP, Jones JL, Toxoplasma gondii infection in humans and animals in the United States, Int J Parasitol 2008;38:1257–1278). Another recent study of three communities in California with 12,244 total households reported 7,284 owned and 2,046 feral cats. The annual fecal deposition of these 9,330 cats in the three communities was estimated to be 106 tons of feces (Dabritz HA, Atwill ER, Gardner IA et al., Outdoor fecal deposition by free-roaming cats and attitudes of cat owners and nonowners toward stray pets, wildlife, and water pollution, J Am Vet Med Assoc 2006;229:74–81).

These same researchers calculated the fecal burden by square foot of soil in another California study. It is known that infected cats can excrete up to 20 million T. gondii oocysts each day during the period they are infected and that each oocyst can remain viable for a year or longer under proper climate conditions. Assuming that cats defecated in a completely random manner, the researchers calculated that each square foot of ground in these communities would be burdened with between 9 and 434 infected T. gondii oocysts each year (Dabritz et al.). A similar study was carried out in rural France and arrived at a similar conclusion regarding the degree of soil contamination by T. gondii oocysts (Afonso E, Thulliez P, Gilot-Fromont E, Local meteorological conditions, dynamics of seroconversion to Toxoplasma gondii in cats [Felis catus] and oocyst burden in a rural environment, Epidemiol Infect 2010;138:1105–1113). Cats, of course, do not defecate randomly but favor specific outdoor spots, meaning that such spots are inevitably burdened with a very large number of oocysts (Afonso E, Lemoine M, Poulle M-L et al., Spatial distribution of soil contamination by Toxoplasma gondii in relation to cat defecation behaviour in an urban area, Int J Parasitol 2008;38:1017–1023).

 •  Transmission of T. gondii to humans

T. gondii can be transmitted to humans in one of two ways. This can occur at any time in life, including while in utero if the pregnant woman becomes infected.

A.   As tissue cysts in the muscle of infected animals

The infection of mammals with T. gondii is widespread. Such infections occur when farm animals ingest feed containing cat feces; when grazing animals inhale or ingest dried cat feces deposited on the ground; and when an animal eats a smaller animal, such as a mouse or rat that is infected. T. gondii then invades many parts of the body, especially muscles, where it becomes tissue cysts and remains for life. When the muscle is eaten as meat, especially if it has not been thoroughly cooked, the person becomes infected.

Lamb and pork are thought to be the most common source of T. gondii tissue cysts for humans, although cysts also occur in beef, chicken, and wild animal meat (e.g., deer, moose, bear). There have even been epidemics of adult toxoplasmosis among individuals who ate undercooked meat, such as hamburger, from a common source (Kean BH, Kimball AC, Christenson WN. An epidemic of acute toxoplasmosis. JAMA 1969;208;1002–1004).

 B.  As oocysts directly from the feces of infected cats

As previously noted, approximately 1.5 million cats (1 percent of 150 million) in the United States are excreting oocysts on any given day; they may excrete up to 20 million oocysts per day, and the oocysts may live for a year or longer. Thus, wherever cats defecate is likely to be a source of contamination. Children’s play areas and sandboxes are common places for cats to defecate because they can use the area’s loose soil or sand to bury their feces. A study in Brazil reported that school playgrounds in elementary schools were heavily contaminated by T. gondii oocysts (dos Santos TR, Nunes CM, Luvizotto MCR et al., Detection of Toxoplasma gondii oocysts in environmental samples from public schools, Vet Parasitol 2010;171:53–57). Children may become infected by putting dirty hands, including oocysts, in their mouths. A family epidemic was described as having occurred this way (Stagno S, Dykes AC, Amos CS et al. An outbreak of toxoplasmosis linked to cats. Pediatrics 1980;65:758–762, copyright 1980, the American Academy of Pediatrics; linked to PDF file with permission).

As the cat feces dry, the oocysts may become aerosolized. They can thus be inhaled by a person changing cat litter or just walking in an area where cats have defecated. An outbreak of toxoplasmosis among patrons of a riding stable was thought to have occurred in this manner (Teutsch SM, Juranek DD, Sulzer A et al. Epidemic toxoplasmosis associated with infected cats. N Engl J Med 1979;300:695–699).

Sandboxes (also called sandpits) are of special interest. Studies of sandboxes in public parks have been carried out in Japan. In one study, 12 of the 13 sandboxes were contaminated with animal feces; the “mean number of feces found in 1 square meter of the sandpits was 35” (Uga S, Prevalence of Toxocara eggs and number of faecal deposits from dogs and cats in sandpits of public parks in Japan, J Helminthol 1993;67:78–82). In another study of three public sandboxes observed over 140 days, an average of 2.3 cat defecations occurred each day in each sandbox (Uga S, Minami T, Nagata K. Defecation habits of cats and dogs and contamination by Toxocara eggs in public park sandpits. Am J Trop Med Hyg 1996;54:122–126).

Assuming that 1 percent of the cats were infected, that each infected cat excreted 10 million oocysts each time it defecated, and that the oocysts remained viable for one year, each sandbox would contain approximately 85 million viable oocysts at any given time. For children playing in such a sandbox, the chances of inhaling or ingesting (e.g., by putting fingers in mouth) T. gondii oocysts would appear to be high.

Gardens are also commonly used by cats for defecation and are also thought to be a common source of infection by inhalation for gardeners. Unwashed vegetables from gardens can also carry oocysts. Studies have also shown that cockroaches and flies can carry oocysts from cat feces to fruits and vegetables (Wallace GD, Experimental transmission of Toxoplasma gondii by cockroaches, J Infect Dis 1972;126:545–547; Wallace GD, Experimental transmission of Toxoplasma gondii by filth-flies, Am J Trop Med Hyg 1971;20:411–413). Another possible mode of transmission is by dogs that roll in cat feces. One study reported that 23 percent of dogs did this, suggesting “the contamination of fur, after rolling in cat feces containing oocysts, might make these accessible to children who pet dogs” (Frenkel JK, Parker BB, An apparent role of dogs in the transmission of Toxoplasma gondii: the probable importance of xenosmophilia, Ann NY Acad Sci 1996;791:402–407).

Finally, water infected with T. gondii oocysts is increasingly suspected of being a major source of transmission (Dubey JP, Toxoplasmosis—a waterborne zoonosis, Vet Parisit 2004;126:57–72). The water is thought to become contaminated by runoff from areas where cats defecate. Several epidemics of toxoplasmosis have been reported due to contaminated water, most notably a 1995 epidemic in Victoria, British Columbia, due to the contamination of the city water supply by cat feces (Bowie WR, King AS, Werker DH et al. Outbreak of toxoplasmosis associated with municipal drinking water. Lancet 1997;350:173–177, copyright 1997; linked to PDF file with permission from Elsevier).

The relative importance of different modes of T. gondii transmission has been widely debated but minimally studied. In countries like France, which has a high rate of T. gondii-infected individuals, the most important source of transmission is thought to be undercooked meat. Studies of pregnant women in Europe have identified the eating of raw or undercooked meat as the most likely source of transmission (Kapperud G, Jenum PA, Stray-Pedersen B et al., Risk factors for Toxoplasma gondii infection in pregnancy: results of a prospective case-control study in Norway, Am J Epidemiology 1996;144:405–412; Baril L, Ancelle T, Goulet V et al., Risk factors for Toxoplasma infection in pregnancy: a case-control study in France, Scand J Infect Dis 1999;31:305–309; Cook AJC, Gilbert RE, Buffolano W et al., Sources of toxoplasma infection in pregnant women: European multicentre case-control study, Br Med J 2000;321:142–147). In countries like the United States, in which meat is generally well cooked, direct transmission from cats is thought to be more important.

One other mode of oocyst transmission must be considered. It was recently reported that T. gondii oocysts can be transmitted from dog to dog in semen (Arantes TP, Lopes WD, Ferreira RM et al., Toxoplasma gondii: evidence for the transmission by semen in dogs, Exp Parasitol 2009;123:190–194). There is also an unpublished report of T. gondii oocysts being found in the epididymis of rats, from which it could get into the rats’ semen. This raises the theoretical possibility of sexual transmission of T. gondii in humans, although this has never been studied

The question has been raised whether the clinical outcome is different if a human becomes infected by a tissue cyst or an oocyst. In mice, infection by oocysts appears to be more pathogenic. In humans, “circumstantial evidence suggests that oocyst-induced infections . . . are clinically more severe than tissue cyst-acquired infections” (Dubey JP, Toxoplasmosis—a waterborne zoonosis, Vet Parisit 2004;126:57–72). There are also suggestions that reinfection can occur with different strains of T. gondii (Elbez-Rubinstein A, Ajzenberg D, Dardé M-L et al., Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review, J Infect Dis 2009;199:280–285).