Immunological Status Against Toxoplasma gondii in Non-Cat Owners from an Endemic Region of Mexico

Introduction

T oxoplasmosis is an infectious disease of public health impact produced by the protozoan Toxoplasma gondii. In humans, eye diseases and major alterations of the nervous system may occur associated with the disease. Currently, it has been estimated that two thirds of the population of the United States is infected (Jones et al. 2009). There is a varying seroprevalence in Mexico. For instance, immunoglobulin G (IgG) was detected in 8.2% and 23.8% of pregnant women and general population in rural Durango, Mexico (Alvarado-Esquivel et al. 2008a, 2009). Traditionally, the presence of the disease in humans has been associated with possession and close contact of a pet cat at home. For instance, Etheredge et al. (2004) describe that children playing with dogs and cats in endemic regions may get infected by direct contact because animals can act as mechanical vectors. In Brazil, Avelino et al. (2004) and Lopes et al. (2009) found a significant association of the presence of cats and T. gondii seroconversion in pregnant women and women of childbearing age, respectively. In another study, it was found that cats in the household are a significant risk factor (odds ratio [OR] for owning a cat = 1.25) for infection (Kolbekova et al. 2007). Other studies have shown that contact with cats is not necessarily associated with an increased risk of T. gondii infection (Kapperud et al. 1996, Cook et al. 2000), and other risk factors are probably playing a more important role in transmitting the disease to people. Considering the oral route as one of the main entrances of the parasite to man, factors such as the consumption of raw ground beef, sheep meat almost raw, dried, cured, or smoked meat, unpasteurized goat milk, and raw shellfish (Jones et al. 2009) and consumption of meat from wild animals (Kijlstra and Jongert 2008) may be highly associated with ingestion of the parasite.

Toxoplasmosis is recognized as an emerging food-borne parasitic disease (Dorny et al. 2009). In the state of Yucatan there are both clinical case reports (Castro et al. 2004) and epidemiological studies (Zavala-Velázquez et al. 1989, Góngora-Biachi et al. 1998) concerning human toxoplasmosis. Toxoplasmosis in cats is considered endemic in the region with prevalences of IgG and IgM of 91.8% and 75.5%, respectively (Jimenez-Coello et al. 2009b). However, there are no studies of the serological status of people in contact or not with cats and their eating habits.

The objective of this study was to determine the seroprevalence of T. gondii IgM and IgG antibody titers in adult people without contact with cats in the city of Merida, Yucatan, and to determine the role of their eating habits as a probable route of infection toward T. gondii.

Material and Methods

Results

Of the 80 people tested in the study, 29 (37%) and 20 (25%) of them were positive for IgM and IgG, respectively, by ELISA. Only 14 (18%) were positive to both IgM and IgG T. gondii antibodies. There was no difference by gender. From the total of T. gondii-seropositive persons (n = 35), 30 (85%) regularly consume pork and 16 (45%) consume pork more than three times a week. No significant association was found between the food habits of persons and the presence of IgG antibodies against T. gondii (Table 1). However, a significant proportion of IgM seropositivity was found in people consuming pork meat (p-value = 0.04) and wildlife meat (OR = 4.5; confidence intervals = 1.47–14.25; p-value = 0.009) (Table 2). None of the participants had previously received a blood transfusion or had practiced gardening. All participants had access to drinkable tap water and were of a medium to high socioeconomical status, and few of them had contact with dogs.

Discussion

Our results show a high circulation of T. gondii in the studied population (young adults between 18 and 21 years of age) without contact with cats. Seropositivity was found in 29 (37%) and 20 (25%) of 80 persons for IgM and IgG, respectively. Other studies reported IgG prevalence rates between 23.9% and 69% depending on the study population (Fiedler et al. 1999, Asthana et al. 2006, Elsheikha 2008, Fernandes et al. 2009, Fromont et al. 2009, Kamani et al. 2009, Salahi-Moghaddam and Hafizi 2009), indicating a wide distribution of the agent.

Human toxoplasmosis is transmitted by several mechanisms. Epidemiological studies indicate that ingestion of tissue cysts is the major source of infection with T. gondii in humans (Dubey and Beattie 1988, Chatterton 1992, Chintana et al. 1998, Alvarado-Esquivel et al. 2006, Asthana et al. 2006, Birgisdottir et al. 2006, Kijlstra and Jongert 2008). The consumption of properly cooked meat is an important factor to avoid the infection. Significant differences in seropositivity to toxoplasmosis have been reported among people who eat raw meat and consumers of properly cooked meat (19.5% and 9.6%, respectively; OR = 2.28) than those who do not (Jacquier et al. 1995). Viable cysts have been found in many different meals and processed meats, which indicates that the different processes of food preparation does not always completely eliminate the parasite. The presence of tissue cysts in meat varies between different animal species, highlighting the meat of sheep (9%–23%) and pigs (12%–15%) and a lesser proportion of beef cattle (0%–10%) and birds (0.3%–8%) (Beattie 1982). However, pork has been recognized as the main food for oral infection with T. gondii (Beattie 1982, Buffolano et al. 1996). Toxoplasmosis in finished pigs in the state of Yucatan is considered endemic, where significant antibody IgM and IgG titers (92% and 80%, respectively) are reported (Jimenez-Coello et al. 2009a). This indicates a very high circulation of T. gondii in the pig farms of the region, which is characterized by high consumption per capita (24 kg/person per year) of pig meat compared with the national average (14 kg/person per year). Our results suggest that habits of pork meat consumption of the studied people may probably be involved with the high proportion of IgM seropositive and may indicate reinfection with the agent. An important aspect to be considered in the oral transmission of T. gondii is the consumption of meat from the wildlife, particularly deer. In our study, around one third of seropositive individuals were consumers of such meat, similar to that found by Kijlstra and Jongert (2008). Wild animals have propensity to become naturally infected with T. gondii (Vikøren et al. 2004, Gauss et al. 2005, 2006), so consumption of its meat may increase the risk of infection as seen by the consumption of pigeons in rural Mexico (Dubey et al. In Press).

Consumption of water contaminated with oocysts from the feces of infected cats is also an important route of infection by T. gondii (Jones and Dubey 2010) as seen in urban and rural areas of Mexico (Alvarado-Esquivel et al. 2008b, Dubey et al. In press). However, the probability of infection by this route is considered of low risk in our study because water was consumed from purified sources.

Some studies have reported higher rates of seropositivity of toxoplasmosis among families owning pet cats in comparison to those who do not possess (Roghmann et al. 1999, Dubey et al. In Press), an increased presence of antibodies to T. gondii in people with cats at home compared with those without (Chintana et al. 1998), a positive correlation between humans and cats in terms of evidence of distribution of antibodies to T. gondii, and higher rates of seroconversion in cat breeders of purebreds (Ulmanen and Leinikki 1975). However, rather than the direct contamination with cats, the most probable mechanism of transmission of the infection in humans is the contact with contaminated soil (Weigel et al. 1995, 1999), especially in tropical climatic conditions where oocysts are highly resistant (Jacquier et al. 1995). In very few cases, the mechanical transmission may occur when playing with pets contaminated with oocyts (mechanical vector) (Etheredge et al. 2004) or when gardening or changing cats sandbox. Nevertheless, the presence of kittens at home may increase the risk of exposure to T. gondii. Kittens consuming preys such as rodents and birds become primo-infected with T. gondii and will have an excretion period of millions of resistant oocysts (Jones et al. 2009). However, high seroprevalence was observed in the sampled people of our study who neither had a history of previous contact with cats nor had practiced gardening. Similar to that described in other studies (Kapperud et al. 1996, Cook et al. 2000, Kamani et al. 2009), pet ownership (cats and dogs) is not a determining factor for infection with T. gondii, meaning that the infection in our environmental conditions is occurring via food consumption as in many other countries.

Conclusion

This study identified the presence of IgG and IgM antibodies in the studied population, indicating previous contact and/or recent infections with T. gondii despite avoiding direct contact with cats. Control measures and monitoring of meat consumption are vital, especially in susceptible populations of immunosuppressed people (such as pregnant women, patients infected with AIDS, or patients with transplant). Ingestion of pork and meat from wild animals appears to be playing a key role in transmitting the parasite. This study will contribute to establish a public health plan to control human toxoplasmosis and to implement educational strategies to prevent exposition to the agent.