PREVALENCE OF HUMAN TOXOPLASMOSIS IN SAN CARLOS ISLAND, VENEZUELA

Leonor Chacín-Bonilla, Yulaicy Sánchez-Chávez, Jesús Estévez, Yraima Larreal and Emelyn Molero 

Leonor Chacín-Bonilla. Doctor in Medical Sciences, La Universidad del Zulia (LUZ), Venezuela. Professor LUZ. Address: Instituto de Investigaciones Clínicas, Apartado 1151, Maracaibo 4001-A, Venezuela. email: ebonillaro@yahoo.com.

Yulaicy Sánchez-Chávez. Licenciate in Bioanalysis, LUZ.

Jesús Estévez. MD, LUZ. Professor, LUZ. email: rjestevez1@cantv.net.

Yraima Larreal. MD, LUZ. Professor, LUZ.

Emelyn Molero. MD, LUZ. Physician, San Carlos Health Center. San Carlos Island, Venezuela.

Summary

A survey of 335 individuals, 1-65 years of age (mean ±SD of 20.8 ±15.7), in 6 communities from the San Carlos Island, Western Venezuela, was conducted to study the prevalence of serum antibody to Toxoplasma gondii. The indirect hemagglutination test showed an overall infection rate of 49.8% (167 of 335) that ranged 23-64.8% according to the locality. No association between antibody status and age or risk factors was detected. Higher antibody rates were found in a windward coast community, and lower rates in a rural sector when compared to 3 other localities. Higher geometric mean titers were found in the communities with higher antibody rates. Toxoplasmosis is prevalent and widely spread in the area. Infection by oocysts from cat feces appears to be the predominant mode of transmission and contaminated drinking water seems to play a role in the transmission.

Resumen

Se realizó una encuesta serológica de 335 individuos de 1 a 65 años de edad (promedio ± DS de 20,8 ±15,7) en 6 comunidades de la isla de San Carlos en el occidente de Venezuela, para estudiar la prevalencia de anticuerpos anti-Toxoplasma gondii. La técnica de hemaglutinación indirecta mostró una tasa de infección de 49,8% (167 de 335) que fluctuó de 23 a 64,8% de acuerdo a la localidad. No se detectó asociación entre la prevalencia de anticuerpos y la edad o los factores de riesgo. Se observaron tasas de anticuerpos más altas en una comunidad de la costa de barlovento, y tasas menores en el sector rural en comparación a otras tres localidades. Las comunidades con las prevalencias de anticuerpos más altas mostraron los mayores títulos geométricos promedios. La toxoplasmosis es prevalente y ampliamente distribuida en la isla. La infección por ooquistes provenientes de heces de gatos parece ser el modo predominante de transmisión y el agua contaminada parece jugar un papel en la transmisión.

Resumo

Realizou-se uma pesquisa de serología em 335 indivíduos de 1 a 65 anos de idade (media ± DS de 20,8 ±15,7) em 6 comunidades da ilha de San Carlos no ocidente da Venezuela, para estudar a prevalência de anticorpos anti-Toxoplasma gondii. A técnica de hemo-aglutinação indireta mostrou uma taxa de infecção de 49,8% (167 de 335) que flutuou de 23 a 64,8% de acordo a localidade. Não se detectou associação entre a prevalência de anticorpos e a idade aos fatores de risco. Observaram-se taxas de anticorpos mais altas em uma comunidade da costa de barlovento, e taxas menores no setor rural em comparação a outras três localidades. As comunidades com as prevalências de anticorpos mais altas mostraram os maiores títulos geométricos médios. A toxoplasmoses é prevalente e amplamente distribuída na ilha. A infecção por ooquistes provenientes de fezes de gatos parece ser o modo predominante de transmissão e a água contaminada parece jogar um papel na transmissão.

KEYWORDS / Toxoplasma gondii / Prevalence / Venezuela /

Received: 02/07/2003. Modified: 07/11/2003. Accepted: 07/23/2003

Introduction

Human infection with Toxoplasma gondii occurs worldwide and is mainly transmitted through accidental ingestion of sporulated oocysts from cat feces deposited in the environment, or tissue cysts from undercooked meat (Jackson and Hutchison, 1989). In Latin America, human toxoplasmosis is widely distributed and primarily due to the former mode of transmission (Frenkel and Ruiz, 1980, 1981), with the exception of the southern area (Stagno and Thiermann, 1973). High seroprevalence rates have been found in Mexico (Velazco Contreras et al., 1992), South and Central America (Remigton et al., 1970; Frenkel and Ruiz, 1981; Frenkel et al., 1984; Sousa et al., 1988; Arias et al., 1996; Contreras et al., 1996; Petersen et al., 2001), and the Caribbean Islands (Barbier et al., 1983; Machín Sánchez et al., 1987; Prabhakar et al., 1991; Etheredge and Frenkel, 1995). Considerable variations in seroprevalence rates have been observed, dependent upon geographic area, age, sex, ethnic group, socioeconomic and sanitary conditions, cat or soil contact, patterns of work and behavior of populations, and location and configuration of communities (Wallace, 1976; Sousa et al., 1988; Jackson and Hutchison, 1989; Etheredge and Frenkel, 1995; Weigel et al., 1999; Petersen et al., 2001).

In Venezuela, studies on toxoplasmosis have been very limited, conducted in a few areas, and most date back more than 30 years. Seropositivity rates have been reported as 57.7% in children aged 0-15 years (Vargas de Caminos, 1982), 40.8-53.5% in 0-60 year-old individuals (Serrano, 1974; Bonfante Garrido et al., 1984), 41-61% in pregnant women (Fígallo and Maekelt, 1962; Maekelt and Gómez, 1962), and 49.7-88% in Amerindian populations (De La Rosa et al., 1999; Chacín-Bonilla et al., 2001). Based on these data, it is difficult to document the geographic distribution and prevalence of the infection in the country. The studies usually provide little information about the epidemiological methodology and demographic features, and most of them have been based on hospital or clinic samples that lack of statistical representation of the population. However, it is evident that toxoplasmosis is common, acquired early in life, and that antibody rates increase with age. On the other hand, there are few studies in humans worldwide (Etheredge and Frenkel, 1995), including one from Venezuela (Chacín-Bonilla et al., 2001), that look at transmission to humans related to environmental features. The aim of this study was to estimate T. gondii seroprevalence among the human population of the San Carlos Island, Venezuela.

Materials and Methods

Study area

The San Carlos Island (SC) is located in Zulia State, Northwestern Venezuela, at 11º00'N and 71º30' - 72º00'W. It is the largest (120km2) of 12 islands that constitute an archipelago between the Gulf of Venezuela and the Maracaibo Lake (Figure 1). The capital is San Carlos, also named El Pueblo. The area has a tropical dry climate with temperatures from 23 to 29°C and annual rainfall from 500 to 1000mm. The relief is predominantly flat and the vegetation is mainly xerophytic. The fauna is poor, limited to the common species of the tropical dry forest; rats, cats, and dogs are common. In the coastal area migratory birds and terrestrial mollusks are frequent.

The island is a vast but largely uninhabited region. The populated area is distributed in six localities: the urban center named El Pueblo (EP); four semi-urban settlements, El Caño (EC), Fuego Vivo (FV), Pueblo Nuevo (PN), and San Bernardo (SB); and the rural sector, El Monte (EM). These communities are located within an area of about 3km2, with the exception of the latter, which is 12km west. There are no paved roads between towns in the area and residents travel mainly by foot. The urban center (EP) is a compact-shaped community with houses distributed in blocks; streets are concrete paved with only small sand areas. EC is located in the leeward coast and the houses are arranged in blocks on both sides of a lineal road that is the only paved street outside the urban area. FV is located inland, between the other sectors, and has loosely grouped houses. SB and PN are located in the windward coast. The latter is behind an unstable sand bank and their houses are grouped 10-20m from the gulf shore. In SB, households are closed to each other, arranged along a circular coast. In the rural sector, houses are loosely grouped. A school and a health center exist in the island.

The communities feature low socio-economic status and poor environmental sanitation. The services of water supply, sanitation, garbage disposal, health care, and education are inadequate. Drinking water is supplied by lighter twice a week, stored in public tanks, and then distributed to the houses. Presence of many flies, roaches, cat and dog feces, and much garbage were present in several places.

Study population

The island population consisted of 1537 inhabitants (12.8 people per km2), 35.8% of them were under 15 years of age (Conzuplan, 1994). However, at the time of the survey, according to the local authorities, the population consisted of 1339 native islanders distributed in 280 households, due to emigration of families. A representative sample of 335 residents (25%) aged 1-65 years (mean ±SD of 20.8 ±15.7), belonging to 84 randomly chosen households from all communities was analyzed. Mean ages of population per sector showed small variations. Children <1 year were excluded to avoid passively transmitted antibodies. The sex distribution was approximately equal, 171 (51%) were male and 164 (48.9%) were female.

People live in single-family dwellings, which contain 2 to 13 related occupants. Most of the houses (62/84, 73.8%) are of concrete construction and the remainder (22, 26.2%) are huts with earthen floors and zinc, wooden, or rushed walls and roofs. Most of the dwellings have indoor plumbing. However, due to the shortage of fresh water, it is stored in tanks and pipes in 24 houses (28.6%), in pipes and other containers in 42 (50%), and 18 (21.4%), had wells. Garbage is collected by the public service, once a week, in 40 (47.6%) of the houses; in the remainder it is burned or thrown away on close-by open spaces and bushes. Pigs, chickens, and pigeons are raised for food in 14 (16.7%) of the houses. Cat or dog ownership was established in 23 (27.4%) and 37 (44%) of the householders, respectively. Wandering cats or dogs were reported inside, near, or around the dwellings in 71 (84.5%) and 69 (82.1%) house units, respectively. Rats, flies, and roaches were reported in 55 (65.5%), 61 (72.6%), and 53 (63%) of the households, respectively. In the rural sector, islanders have established small farms where goats are raised. Some horses, cows, and donkeys are present.

The islanders have close contact among them. However, contact with the outside is limited due to scarcity of boats. The majority of the residents practice subsistence fishing and those from PN use to search for snails buried in the shore, activities that result in direct manual contact with the soil. Children play mainly on the ground, in the backyards and gardens of the houses, and at the beaches. Geophagia was noted in some young children. The islanders’ diet consists mainly of fish. Other kinds of meat, like pork, beef, goat, chicken, and pigeon are less frequently eaten by 83 of 335 (24.8%) residents. Meat and eggs are well cooked, only 3.6% of people admitted to eat medium-cooked meat and none the consumption of raw meat. The rural residents drink unboiled goat milk.

Epidemiological procedures

At the beginning of the survey the authors, with the approval of the leaders of the island and the assistance of a nurse visited home by home, gave an explanation of the goal of the study and obtained informed consent of the head of each family before enrollment in the study. At each visit, an interview was conducted with each participant. Information was obtained on demographic characteristics and an inquiry was made concerning risk factors to which people were exposed, such as contact with cats or other domestic animals, exposure to soil or water, sanitary conditions that might favour the transfer of oocysts from cat feces to residents, economic status, places where children play, outdoor activities and feeding habits, especially consumption of undercooked meat, and symptoms that could be related to the infection.

Laboratory methods

Blood samples were drawn by venous puncture, transported to the field laboratory and centrifuged. Serum aliquots were frozen and transported by boat to the laboratory, where they were stored at -20°C. Sera were analyzed for immunoglobulin G antibodies in U-shaped microtiter plates by a commercial indirect hemagglutination test (TOXO-IHA test, USA). Sera were screened first for antibodies by doubling dilution from 1:2 to 1:64. If positive, they were titrated by dilution beginning at 1:64 to 1:4096. Titers ³64 were considered as positive.

Statistical analysis

Chi-square test and Fisher’s exact test were performed to examine antibody status. Linear regression was used to test the relationship between antibody prevalence rates and geometric mean titers (GMT) of the communities. A value of P< 0.05 was considered significant.

Results

The overall percentage of individuals positive to T. gondii in the combined communities of the island was 49.8% (167 of 335; range 23%-64.8%; Table I). The highest antibody prevalences were found in PN, EP and SB, with significant differences as compared with the rural settlement (P< 0.0001, 0.001, and 0.01, respectively). In addition, there were significant higher seropositivity rates in PN as compared with FV and EC, and in EP with respect to FV (P< 0.05). Higher GMT were found (Table I) in the sectors with higher prevalence rates (P<0.05).

Since the serological profile and GMT, according to age, had similar trends in all localities, the data were tabulated together in Figure 2. The rate of positive subjects was high in all age groups and rose sharply from 33.3 to 58% between the groups aged 1-5 and 11-15 years (P< 0.05). Otherwise, there was no association between age and antibody status; the rates remained about the same, below 60%, from age 10 onwards. Antibody titers were highest in the youngest group, falling with increasing age as shown by GMT. No relationship between sex and antibody status was found in any of the age groups.

The frequency distributions of antibody titers in residents of EP, EC, FV, and EM showed the same pattern, but were different from those of PN and SB (Table II). In the former sectors combined, the lowest positive titer (1:64) was most common (33 of 86, 38.4%) and then began a steady decline to less frequencies of higher titers as these increased; the highest titer (³1:4096) was found in 1 (1.2%) of the positive subjects. Most of the positive subjects (63, 73.3%) had low titers (£1:256) and 11 (12.8%) had high titers (³1:1024); the GMT was 176.7. In contrast, in PN and SB combined the most common titer was 1:1024 (21 of 81, 26%) followed by 1:512 (19.7 %), 1:256 (16%), 1:128 (14.8%), 1:64 (13.6%), 1:2048 (6.2%), and ³1:4096 (3.7%). A high proportion (35.8%) had high titers  ³ 1:1024, and the GMT was 396.1. Among all positive subjects (167) in the island, low titers predominated (59.3%) and high titers were present in 40 cases (23.9%).

Within and between the communities, the comparative analyses between antibody status and risk factors such as cat or soil contact, contact with domestic animals, socioeconomic and hygienic indicators, and dietary information yielded no significant associations.

No symptoms were elicited that could reasonably be associated to toxoplasmosis during the study period.

Discussion

The serologic evidence shows a focus of T. gondii of high endemicity in SC Island, as indicated by the presence of antibodies in half of its population. The overall positivity rate observed is similar to those found in populations of similar age structure from Western Venezuela (Serrano, 1974; Bonfante Garrido et al., 1984; Chacín-Bonilla et al., 2001), and lower than that reported from Amerindians in the Southern area (De La Rosa et al., 1999). The prevalence rate in this study is lower than those reported from other Latin American areas as La Guadeloupe (Barbier et al., 1983), Panamá (Sousa et al., 1988), Costa Rica (Arias et al., 1996), and Brazil (Petersen et al., 2001), and higher than those noted in Cuba (Machín Sánchez et al., 1987) and Chile (Contreras et al., 1996).

Most of the positive subjects (59.3%) had low antibody titers. However, an appreciable proportion (23.9%) was high, suggestive of active or recent infection or frequent reinfection. The frequency distribution of antibody titers in PN and SB was surprising, since the most common titer was 1:1024 (26%), an important proportion (35.8%) was high, and the GMT was 396.1. In contrast, in the remaining sectors combined, 1:64 was the most frequent titer (38.4%), 12.1% of the titers were high, and the GMT was 176.7. These findings suggest a higher frequency of recent infections or reinfections in PN and SB. In a report from Costa Rica, the most frequent titer was also 1:1024 (Frenkel and Ruiz, 1980).

The high rates of infection (33-58%) observed in children confirm that toxoplasmosis is an infection of early childhood in the tropics (Remigton et al., 1970; Frenkel and Ruiz, 1980; Barbier et al., 1983; Sousa et al., 1988). A higher proportion of infections in 11-15 year-old children with respect to the youngest group was noted (P< 0.05). However, after 10 years of age, no significant rise was observed and the prevalence levels were similar in all age groups. This distribution of antibody prevalence by age is different from the known association between age and rise in seropositivity (Frenkel and Ruiz; 1980; Barbier et al., 1983; Sousa et al., 1988) but is consistent with the results of Etheredge and Frenkel (1995). The reasons for this finding are unclear. However, intermittent contamination of drinking water with oocysts could be a factor since people, regardless of age, would be infected when they drink water at the time of contamination.

Human acquisition of toxoplasmosis in SC appears to be primarily due to contact with oocysts from cat feces by the feeding habits of the residents and the high early seroconversion rate that is compatible with fecal-oral transmission. The lack of association between cats and antibody status in this report may be related to the high number of cats that could result in a relatively equal exposure to infective oocysts of all residents. Other contributory factors might be the existence of many flies, roaches, and terrestrial mollusks that could disseminate oocysts as mechanical vectors (Jackson and Hutchison, 1989) and the many opportunities of the islanders to be in contact with contaminated soil. In fact, children play together in extensive dirt areas and fishing activity brings about people in contact with soil, and the winds are a means of transportation for soil particles, sand, and probably infective oocysts, conducive to contamination of the environment. Drinking water could be another vehicle of transmission in the area. Indeed, cats may drink water from pipes and wells and contaminate it, or defecate near wells and oocysts be washed from the soil into them by the rain and winds. Toxoplasmosis is not generally considered as a waterborne infection. However, contaminated water might be an important means of transmission. In fact, there is a report of a waterborne outbreak of toxoplasmosis in Panama (Benenson et al., 1982) and other studies have suggested this mechanism of transmission (Etheredge and Frenkel, 1995; Bowie et al., 1997; Chacín-Bonilla et al., 2001).

In this study, within and between the communities, there were no significant associations between antibody status and traditional risk factors, such as, social, economic, and sanitary conditions, patterns of work, and behavior of residents. These findings might be due to the homogeneity and similar lifestyle of the islanders and the fact that all the sectors shared risk factors favorable to Toxoplasma infection due to the abundance of cats, high exposure of the residents to contaminated soils with cat feces and the presence of numerous mechanical vectors of the oocysts. Community was the only factor predictive of the prevalence of antibody. Differences found between individual localities may be due to several factors, since community features such as urban or rural location, configuration, closeness of houses to each other, amount of open spaces, moisture of the soil, oocysts survivability and human contact with soil, may affect antibody prevalence for the community as a whole (Frenkel and Ruiz, 1981; Sousa et al., 1988; Etheredge and Frenkel, 1995). In this report, the rural sector had a significant lower prevalence rate as compared with three other communities, as expected, since low concentration of oocysts in the area may result from peripheral oocyst loss due to sufficient soil availability in the open spaces. On the other hand, the urban center had a higher positivity rate as compared with FV and the rural area, as can be expected, since the former is a compact-shaped sector with high density of houses distributed in blocks, paved streets, and the least amount of open space; thus it is possible that the scarcity of available soil for cat defecation results in a higher oocyst density conducive to higher antibody prevalence (Frenkel and Ruiz, 1981; Etheredge and Frenkel, 1995).

The house density of PN does not explain its higher antibody prevalence rate as compared with FV, EC and EM, because of the existence of abundant open space where cats may defecate. The following factors are plausible explanations. The location of PN in the windward coast, behind an unstable sand bank whose sand particles are shifted and spread by the winds over this community, and the habit of their residents to look for snails buried in the shore, are conditions resulting probably in a greater soil contact of these people. Higher antibody prevalences have been found in windward coast localities (Barbier et al., 1983). PN is near the coastline where soil moisture is a determining factor in the oocysts survivability due to its ability to be a good reservoir that ensures a sufficient level of contamination. Thus, the chances of its residents to be infected and reinfected are presumably higher as compared with those from FV, EC and EM, and would account, at least in part, for the higher seropositivity rates in PN and the higher titers noted in this sector and SB, which is also located close to the gulf shore. In conclusion, human toxoplasmosis is prevalent and widely spread in the SC Island.

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