Introduction and Purpose
Toxoplasmosis, a zoonotic disease prevalent worldwide, is caused by the protozoan parasite
Toxoplasma gondii (
T. gondii). The lifecycle of this parasite has three stages: the oocyst, bradyzoite (cyst), and tachyzoite. Tachyzoites actively and rapidly invade hosts cells, aided by one of the most prevalent proteins: Granule-1 (GRA-1). This protein is responsible for binding with the calcium released into the lumen of the vacuole and interacting with tissue (Weis and Kami 1995; Lee et al.
2014). Toxoplasmosis can lead to congenital malformation in the intermediate host, abortion, and hydrocephalus (Fusco et al.
2007; Tavassoli et al.
2013).
Worldwide, over 6 billion people have been infected with toxoplasmosis (Klaren and Kijlsstra 2002). The seroprevalence of toxoplasmosis in humans varies in different countries, with previous studies reporting country-specific prevalence rates of 6.7% in Korea; 12.3% in China; 23.9% in Nigeria; 46.0% in Tanzania, and high prevalence of up to 98.0% in some regions (Glasner et al.
1992; Fromont et al.
2009; Kamani et al.
2009; Shin et al.
2009; Swai and Schoonman
2009; and Xiao et al.
2010). Serological studies in livestock revealed that worldwide the average
T. gondii prevalence is 14.0% in cattle; 27.0% in goats; 25.0% in pigs; 66.0% in sheep; and 44.0% in horses (Tenter et al.
2000). In Indonesia, the prevalence of toxoplasmosis in livestock has been estimated as 8.8% in cattle, 51.0% in goats, and 45.0% in sheep (Artama et al.
2007). The prevalence of human toxoplasmosis in Indonesia for humans has been reported from 43 to 88% in some regions (Subekti et al. 2006).
Transmission of toxoplasmosis can occur through two mechanisms: vertically from mother to fetus and horizontally through the consumption of undercooked meat, contaminated milk, and raw vegetables, and also in the case of transplants and accidents in laboratory (Fusco et al.
2007; Gangneux and Marie,
2012; Uttah et al.
2013; and Wing
2016). Members of the family
Felidae (domestic cats) are the definitive hosts; however, many mammals (live stocks and humans), birds, and fishes are intermediate hosts (Gilot-Fromont et al.
2012; Webster et al.
2013). A single cat can shed more than 100 million oocysts in prepatent period about 18 days. In order for these oocysts to become infectious, they must undergo sporulation, which can take more than 4 days and occurs in environments with high humidity and a low temperature. Oocysts can survive outdoors for many months, remain viable for long periods of time in water, and resist freezing and moderately high water temperatures. Tissue cysts in meat are usually destroyed by heating to 67°C. The survival of tissue cysts at lower temperatures depends on the duration of cooking (Tenter et al.
2000).
Country-specific environmental conditions, eating habits, hygiene, and host susceptibility all contribute to global differences in the prevalence of toxoplasmosis (Furtado et al. 2011). Indonesia has a tropical climate, providing suitable conditions for gardening and farming, increasing human contact with soil and livestock, as well as the possibility of increasing contact with raw meat. Additionally, it is common to consume goat, sheep, beef, chicken, and rabbit satay, potentially with undercooked meat and raw vegetables. In a multicenter study in Europe, meat consumption was estimated to be responsible for between 30.0 and 63.0% of toxoplasmosis cases, while soil contact was identified as the cause of between 6.0 and 17.0% of cases (Gangneux and Marie
2012).
Health and disease are increasingly understood as the product of interrelated ecological, cultural, social, and economic situations (Blazkuez et al. 2014). Socio-demographic status, lifestyle, and environment are risk factors for toxoplasmosis; therefore, interdisciplinary collaborative research is essential to reduce the risk of transmission. EcoHealth is one of several integrative approaches that considers interactions between health and the environment, making it an ideal approach for researching a zoonosis such as toxoplasmosis.
Previous research on toxoplasmosis has identified high-risk geographical areas; however, further investigation using spatial techniques will achieve more accurate identification of high-risk locations, which can be used to improve strategies to prevent the spread of this disease. Geographic Information Systems (GIS) have been applied in several situations, including surveillance and monitoring of diseases (Jores et al.
2008), disease cluster detection (Miller et al.
2004), identification of environmental predictors of disease in wildlife populations (Miller et al.
2002), risk assessments (Hung et al.
2004, 2007), and modeling the spread and impact of disease (Norman 2008). In the present study, the use of GIS, combined with a seroprevalence study and risk factor questionnaire, demonstrates a true EcoHealth approach, which is essential when researching diseases, such as toxoplasmosis, where animal hosts, human lifestyle, and environmental factors are all involved in transmission. The use of GIS will aid in the identification of high-risk locations, enabling public health interventions to be targeted at specific populations in Middle Java. This system was constructed utilizing the administrative boundaries (at provincial and municipal levels) of the Campania region with toxoplasmosis cases (Fusco et al.
2007).
Using an EcoHealth approach, this study aims to determine the seroprevalence and spatial distribution of toxoplasmosis in Middle Java, and identify factors associated with the occurrence of toxoplasmosis.
Discussion
In this study, the prevalence of toxoplasmosis was greater in the lowlands as compared with the highland districts of Middle Java, Indonesia. One possible explanation could be the contamination of water sources from drifting soil, in the event of flooding or heavy rain, transporting oocysts from high to low ground, thus increasing the prevalence of oocysts in low-lying areas (Iskandar
1999).
Wonosobo and Banjarnegara had no cases of toxoplasmosis in this study. These are highland districts, with mountainous terrain, which may also affect the distribution of cats. As the cat is the definitive host of
T. gondii, (Tavassoli et al.
2013), fewer cats in the environment will reduce the risk of transmission to the environment and livestock, thereby reducing the prevalence of toxoplasmosis in the local population.
Daily contact with raw meat was also identified as a risk factor for toxoplasmosis. Toxoplasmosis can occur during the transmission of
T. gondii via the blood through a wound (CCOHS
2011). Daily contact with raw meat from infected animals increases the possibility of contact with tissue cysts, particularly if no protective equipment, such as gloves, is worn. Additionally, tissue cysts may be ingested during hand-to-mouth contact after handling undercooked meat, or from using knives, utensils, or cutting boards contaminated by raw meat (CDC
2004). This will also increase the risk of transmission in people who have regular contact with raw meat.
Consumption of unfiltered water was also identified as a risk factor for toxoplasmosis. Respondents who used non-filtered water were at increased risk of toxoplasmosis compared with those using a filtered water source. Consumption of unfiltered water was associated with water sources such as rivers, wells, and reservoirs. Oocysts can be transported via rivers and water during periods of heavy rain. Water is not just used for human consumption, but also for washing vegetables and as drinking water for livestock. The majority of respondents in Cilacap used filtered water. Cilacap is near the coast and because of the potential seawater contamination of water sources in this district, the use of filtered water is more widespread compared with other districts in Middle Java. This may be one factor leading to minimal cases of toxoplasmosis in several locations in Cilacap. Water is filtered using chlorine to reduce bacteria and parasites. Oocysts cannot survive for long in cold water conditions or in warm water with high levels of chlorination, UV, and ozone treatment (Wainwraight et al. 2007; Gangneux and Marie
2012).
This study identified a relationship between the population of cats and toxoplasmosis cases; people living in districts with high density of cats, Purworejo and Kebumen, were at increased risk of toxoplasmosis compared with those living in districts with low density of cats. Middle Java in general has a relatively small cat population, which varies in each district. A small number of cats do not necessarily indicate there is no risk of infection in that location. Cat feces take a long time to decay (Gangneux and Marie
2012), and during that time thousands of oocysts can develop (Ishaku et al.
2009).
In the surveyed population, men were at increased risk of infection compared with women. This could be associated with the differing roles of men and women in Middle Java; male-dominated professions, such as farming and meat production, will increase the risk of contact with contaminated meat, as well as increasing the risk of environmental exposure through spending long periods of time outdoors or in high-risk areas.
Conclusion
This study highlighted the high prevalence of toxoplasmosis in Middle Java, and identified some important environmental, ecological, and demographic risk factors. Low elevation, contact with raw meat, unfiltered water sources, and the high density of cats are supposed to be risk factors of toxoplasmosis in Middle Java. Modifiable risk factors, such as unfiltered water sources and direct contact with raw meat, are relatively straightforward to address by encouraging people to use filtered water and wear protective clothing, such as gloves, when handling raw meat. The oocyst from infected cats will be transmitted to the environment through water shed and flooding and distributed from high land to low-lying areas.