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

Origin, domestication, and early history

All members of the felid family, from kittens to lions and tigers, share a common feline ancestor which lived in Southeast Asia approximately 11 million years ago.  The clouded leopard, an endangered felid found in Southeast Asia, is genetically the closest felid to the original one. About 9 million years ago, “the felid family underwent an explosive diversification, giving rise to thirty-seven species that today cover the Earth’s geographical and ecological spectrum”¹. One of these species was Felis sylvestris sylvestris, indigenous to the Middle East, East Asia, North Africa and Europe, and the predecessor of all domestic cats. There are four other subspecies of Felis sylvestris sylvestris but this is the only one that was domesticated.

Cats were initially domesticated in Turkey, part of the Fertile Crescent, approximately 10,000 years ago, at the time farming was beginning². They were later domesticated in Egypt, probably independently. It is likely that wild cats were attracted by the mice that accompanied the collections of grain. There is also some evidence that cats were independently domesticated in China about 5,000 years ago, but the wildcat of origin was the leopard cat, which is different from the wildcat previously domesticated in Turkey³. 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”⁴.

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. DNA sequencing from an Egyptian mummy found T. gondii DNA sequences in 2013⁵. 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. Edward II, a 14th century king of England, required “all English vessels to have a cat on board for pest control”⁶ 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”⁷.

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”⁸. In 1233 Pope Gregory IX issued a papal bull “that describes orgies of witches fraternizing with Lucifer in the guise of a black cat”⁹. 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.”¹⁰ Cats became especially associated with heretical religious sects, such as the Waldensians and Manicheans, 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 merriment¹¹.

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 1777¹².

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, also called the Norway 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”¹³. 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”¹⁴. 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”¹⁵. 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 of cats

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”¹⁶. 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 Africa¹⁷.

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”^18-19.

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.

Cat ownership increased sharply following World War II with the invention of kitty litter and widespread availability of canned cat food. In the United States, there was a 50% increase in owned cats reported between 1989 and 2006²⁰. In many American families, cats have close contact with their owners; one American study reported that 62% of cats slept with their adult owners and another 13% slept with children²¹.

There has also been a marked increase in recent years in the keeping of cats as pets in developing countries as people become more affluent. For example, a study of T. gondii  oocysts in public parks was also recently carried out in Wuhan, China²²; under the regime of Mao Zedong, the keeping of pets was considered bourgeois and discouraged. Pet keeping only started to become prevalent after the death of Mao in 1976 and did not become common until recent years^23-24. Yet, when 252 soil samples were taken from six public parks in Wuhan in 2009 and 2010, 58 samples (23%) contained T. gondii  oocysts. The soil samples were taken from areas frequented by cats. The wider prevalence of T. gondii  in modern China is also reflected in surveys of T. gondii  seropositivity in pregnant women. In seven studies between 1996 and 2004, the average seropositivity rate was found to be 4.5%, but in six studies completed since 2004 the average rate was 10.2%²⁵.

Counting cats is notoriously difficult. In the United States, it has been estimated that there are approximately 90 million owned cats, which are found in one-third of all households, and an additional 70 million or more (estimates range from 60 to 100 million) feral cats, thus totaling at least 160 million²⁶.  Estimates of the number of owned cats which are kept exclusively indoors range from 30-60 percent²⁷. Britain is said to have about 10.3 million owned cats, France 8.1 million and Australia to have 20 million, one for every person²⁸.  Of these 20 million cats, 18 million are said to be feral²⁷.  Globally there is estimated to be 600 million owned cats²⁶. It is well known that, left unchecked, cats reproduce rapidly²⁹. According to one analysis, “a pair of cats could produce 354, 294 descendants in five years”⁹.

Cat feces and T.gondii oocyst distribution

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 when they first start hunting. 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 have a reactivation of their T. gondii infection if they are later infected with other viruses, such as the feline immunodeficiency virus, or with a different strain of T. gondii,⁵⁰ or are stressed, and they may excrete oocysts and again become infectious at that time³⁰. At any given time, it has been estimated that approximately 1 percent of cats are excreting T. gondii oocysts. There is also evidence that some cat brands (e..g Persian) are more likely to carry T. gondii than other breeds (see reference #43 in next section). One study claimed that “cats can shed as many as 500 million oocysts” during their initial infection³¹ 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 feces³². Insofar as these communities are representative of the United States population, the 81.7 million owned cats would produce 856,930 tons of outdoor cat feces each year. Assuming there are only 25 million feral cats, these would produce another 360 459 tons of cat feces, resulting in a total accumulation of 1,217,389 tons deposited annually in the environment of the United States³³. A review of this estimate in the Los Angeles Times claimed that this weight of cat feces was the equivalent of 12 aircraft carriers³⁴.

The oocysts are remarkably stable, especially if they are deposited in shady, moist, and temperate conditions. In Texas, under outdoor shaded conditions with a mean air temperature of 19.5⁰C, oocysts remained viable during a 13 month experiment³⁵. In Kansas, oocysts were buried in loose soil and remained viable for 18 months³⁶. Oocysts maintained experimentally at 4⁰C in seawater or freshwater remained viable for 24 and 54 months, respectively^37-38. Oocysts also survived for over a year in vials of 2% sulfuric acid at 4⁰C³⁹. Since almost all of these studies were terminated while at least some of the oocysts were still viable, we do not yet know the outer limit of viability for T. gondii  oocysts deposited in various environmental conditions.

Given this large number of T. gondii  oocysts, what is the effect of this oocyst burden on a specific community? In the three California communities cited above, the T. gondii  annual oocyst burden was calculated by dividing the cat feces by the land area of residential housing. The communities differed by size and number of cats⁴⁰. Depending on estimations of oocyst production by the cats, the number of T. gondii  oocysts ranged from 9 to 434 per square foot⁴¹. A similar study was carried out in three communities in rural France, using comparable assumptions, and reported that the annual environmental oocyst burden varied from 3 to 335 oocysts per square foot⁴².  In a village in Panama, it was estimated that the oocyst burden in soil near houses where cats are fed varied from 18 to 72 per square foot⁴³.

The environmental contamination of residential living areas by T. gondii oocysts has also been assessed in several studies by testing soil samples for T. gondii.  The results differ depending on the number of cats living in the area; the type of soil tested; the depth of the sample (oocysts may be in the soil up to 4 inches below the surface); temperature; moisture; and the method used to identify the oocysts (PCR of DNA; indirect fluorescent antibody; histopathology; mouse bioassay, etc.)

In addition to the study in Wuhan China, cited above, at least 5 other such studies have been carried out.  In Harbin, China, said to be home to over 100,000 cats, 9,420 soil samples from various parts of the city were tested by PCR.  T. gondii was found in 2,853 (30%) of the samples, mainly in samples from “residential areas and school campuses”⁴⁴.  In a village in France which had 184 cats, 243 soil samples were collected from random locations in and near the village.  Using PCR, T. gondii was detected in 71 of the 243 samples (29%), most heavily in the village but “unexpectedly…substantial contamination of areas more than 300m [meters] away from households and farms.”⁴⁵ In another French study, T. gondii  oocysts were identified in 8 of 62 soil samples collected from cat defecation sites on the grounds of an urban hospital⁴⁶. In Brazil, T. gondii  oocysts were isolated from 10 soil samples taken from the playgrounds of 31 elementary schools; the authors suggested that these results indicated a wide distribution of T. gondii oocysts around elementary schools in the region⁴⁷. In a village in Panama, it was estimated that the oocyst burden in soil near houses where cats are fed varied from 18 to 72 per square foot⁴⁸. In Poland, T. gondii  oocysts were isolated from 18 of 101 soil samples taken from places thought to be favored by cats for defecation: sandboxes, playgrounds, parks, gardens, and areas around rubbish pits⁴⁹.

References

1. Budiansky S. The Character of Cats. New York: Viking; 2002:6
2. Driscoll CA, Menotti-Raymond M, Roca AL, et al. The Near Eastern origin of cat domestication. 2007;317:519–523
3. Cats domesticated twice? Science2015; 351: 429
4. Bretnor R. Bring cats! A feline history of the West. The American West. 1978;15:32-35,50
5. Khairat R, Ball M, Chang CC, et al. First insights into the metagenome of Egyptian mummies using next-generation sequencing. J Appl Genet. 2013
6. Marra P.P. and Santella C. Cat Wars, Princeton University Press, 2016: 15
7. Lynnlee JL. Purrrfection: The Cat. West Chester, Pa: Schiffer; 1990:21
8. Ibid
9. Tucker. The Lion in the Living Room. Simon and Schuster, 2016: 20
10. Lynlee, p. 21.
11. Serpell JA. The Domestication and History of the Cat. In: Turner DC and Bateson P, eds. The Domestic Cat. Cambridge: Cambridge University Press; 1988:156
12. Kete K. The Beast in the Boudoir. Berkeley: University of California Press; 1994:119
13. Méry F. The Life, History and Magic of the Cat. London: Paul Hamlyn; 1967:56, 59
14. Lynlee, p. 28.
15. Repplier AQ. Agrippina. Atlantic Monthly. 1892;69:760.
16. The cat. Household Words. 1857;15:370.
17. Cats. Chamber’s Journal. 1872;49:178.
18. Peterson DR, Cooney MK, Beasley RP. Prevalence of antibody to Toxoplasmaamong Alaskan natives: relation to exposure to the felidae. J Infect Dis. 1974;130:557–563.
19. Huldt G, Lagercrantz R, Sheehe PR. On the epidemiology of human toxoplasmosis in Scandinavia especially in children. Acta Paediatr Scand. 1979;68:745–749.
20. US Census Bureau. Surveys by the American Veterinary Medical Association, 1987 and 2006. In Statistical Abstract of the United States. U.S. Government Printing Office; 2010.
21. Chomel BB, Sun B. Zoonosis in the bedroom. Emerg Infect Dis. 2011;17:167-172.
22. Du F, Feng HL, Nie H, et al. Survey on the contamination of Toxoplasma gondiioocysts in the soil of public parks of Wuhan, China. Vet Parasitol. 2012;184:141-146.
23. Eckholm E. Dog’s life in China: Hiding from police dragnets. New York Times, 2001.
24. Zhu S. Psychosis may be associated with Toxoplasmosis. Med Hypotheses. 2009;73:799-801.
25. Zhou P, Chen Z, Li HL, et al. Toxoplasma gondiiinfection in humans in China. Parasit Vectors. 2011;4:165.
26. Dabritz HA, Conrad, PA. Cats and Toxoplasma: Implications for public health. Zoonoses Public Health. 2010;57:34-52.
27. Tucker 128; B Peterson, The case against cats, Atlantic,December 2016.
28. Will G. Millions and millions of cats. Washington Post. July 13, 1997.
29. Kelson L. The race to outpace feral cat overpopulation. Animal Guardian. 1998;4:8.
30. 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; 2004:58–124.
31. Dubey JP, Jones JL. Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol. 2008;38:1257–1278.
32. 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.
33. Torrey EF, Yolken RH. Toxoplasma oocysts as a public health problem. Trends Parasitol. 2013;29:380-4
34. Morin M. Is your kitty’s poop a public health threat? Los Angeles Times, July 9, 2013.
35. Yilmaz SM, Hopkins SH. Effects of different conditions on duration of infectivity of Toxoplasma gondii J Parasitol. 1972;58:938-9.
36. Frenkel JK, Ruiz A, Chinchilla M. Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am J Trop Med Hyg. 1975;24:439-43.
37. Dubey JP. Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol. 1998;84:862-5.
38. Lindsay DS, Dubey JP. Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. J Parasitol. 2009;95:1019-20.
39. Frenkel JK, Dubey JP. Toxoplasmosis and its prevention in cats and man. J Infect Dis. 1972;126:664-73.
40. Dabritz HA, Atwill ER, Gardner IA, Miller MA, Conrad PA. 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.
41. Dabritz HA, Miller MA, Atwill ER, et al. Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J Am Vet Med Assoc. 2007;231:1676-84.
42. 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;138:1105-13.
43. Sousa OE, Saenz RE, Frenkel JK. Toxoplasmosis in Panama: a 10-year study. Am J Trop Med Hyg. 1988;38:315-322.
44. Gao X, Wang H, Wang H, et al. Land use and soil contamination with Toxoplasma gondii oocysts in urban areas. Science of the Total Environment. 2016; doi:10.1016/j.scitotenv.2016.06.165
45. Gotteland C, Gilot-Fromont E, Aubert D, et al. Spatial distribution of Toxoplasma gondii oocysts in soil in a rural area: Influence of cats and land use. Veterinary Parasitology. 2014; 205:629-37.
46. Afonso E, Lemoine M, Poulle ML, et al. Spatial distribution of soil contamination by Toxoplasma gondii in relation to cat defecation behavior in an urban area. Int J Parasitol. 2008;38:1017-23.
47. dos Santos TR, Nunes CM, Luvizotto MC, et al. Detection of Toxoplasma gondii oocysts in environmental samples from public schools. Vet Parasitol. 2010;171:53-7.
48. Sousa OE, Saenz RE, Frenkel JK. Toxoplasmosis in Panama: a 10-year study. Am J Trop Med Hyg. 1988;38:315-322.
49. Lass A, Pietkiewicz H, Modzelewska E, Dumètre A, Szostakowska B, Myjak P. Detection of Toxoplasma gondii oocysts in environmental soil samples using molecular methods. Eur J Clin Microbiol Infect Dis. 2009;28:599-605.
50. Zulpo DL, Sammi AS, dos Santos JR, et al. Toxoplasma gondii: A study of oocyst re-shedding in domestic cats. Vetinary Parasitology. 2018; 249: 17-20.