Risk factors and prevalence of enteroparasitic diseases in Shellfish Pickers from a lake area in the Northeast of Brazil

Introduction: Intestinal parasitosis are a public health problem worldwide. There are several risk factors and a high association with some specific labor activities. Objective: The present study assessed the risk factors and prevalence of enteroparasitic diseases in shellfish pickers from one district of Maceió, Alagoas state, Brazil. Methods: Crosssectional study of 41 female shellfish pickers including parasitological tests in fecal samples and a questionnaire with objective and subjective questions. Sand samples from their working environment were also analyzed. Results: At least one species of parasite was found in 19.51% of the fecal samples. Pathogenic species of Giardia lamblia, Trichuris trichiura, Schistosoma mansoni, Ascaris lumbricoides, Enterobius vermicularis, from the Ancylostomatidae family, and non-pathogenic species of Entamoeba coli were found. Polyparasitism was diagnosed in 37.5% of the positive samples. A total of 57.14% of sand samples contained hookworm larvae. Regarding the risk factor, low educational level was statistically associated to the presence of parasites (p<0.05). Conclusion: Greater investment in basic education is needed to increase the knowledge about preventive measures against parasitic diseases and the promotion food-handling courses in order to change existing inadequate habits in the community. Basic sanitation is also essential in preventing environmental contamination.


INTRODUCTION
Intestinal parasitosis are a public health problem worldwide and present high morbidity indices in developing countries, where population growth is not accompanied by better living conditions [1][2][3][4] . The parasitosis can affect nutritional balance, interfering in nutrient absorption, inducing intestinal bleeding, reducing food ingestion and, in cases of overpopulation, may lead to death 5,6 . The warm environments of tropical countries, associated with malnutrition, lack of health care, poor sanitary conditions, inadequate personal hygiene, housing and peridomestic environments are associated with higher exposure of the population to infection 7,8 . Brazil has 12% of the world's fresh water, including 8.2 billion meters of water distributed into rivers, lakes, dams and reservoirs, in addition to environmental and climatic conditions favorable to making it one of the leading fishing producers in the world 9 .
The shellfish picking is a manual fishing technique in Brazil, exerted mainly by women called "marisqueiras", who harvest shrimp, "sururu", oyster, soft crab, and crab 10 . Shellfish pickers work both for subsistence and commercial purposes, being responsible for their own equipment and all the production stages 11 , from preparing the materials for shellfish harvesting to selling of the final product. These stages are conducted at home, and in peridomestic and extradomestic environments 12

Sand collection and analysis
Seven sand samples were collected from two areas of shellfish harvesting and manipulation. The samples were collected 5cm deep from the land surface and 1m distant from each other.
The sand samples were inserted in flasks with lids, without preservative, and evaluated in the same day. The methods adopted were: Hoffman, Pons & Janer 15 and Baermann-Moraes 17 . Two slides from each sample/technique were evaluated under bright-field microscopy (100 and 400⨉ magnification).

Statistics
Risk factors were identified via interviews consisting of multiple-choice questions, considering the economic situation, education, eating and hygiene habits and basic sanitation. The chisquared test (X 2 ) was used to determine the relation between the variables (risk factors) and prevalence of parasitic infections in the study population. p<0.05 was considered significant.
All the shellfish pickers received the laboratory results. Positive cases were oriented about parasitic prevention and referred to the appropriate health units for treatment.

DISCUSSION
The manual fishing, especially in urban areas, is commonly a casualty of environmental problems originated from irregular urban growing 18 . In recent years, environmental problems, such as contaminated water, air, soil, domestic and work environments, have had a significant impact on human health 19 .  Moreover, considering the three cities shored by the Mundaú Lake, the percentage of houses with basic sanitation is low. The biggest city shored by Mundaú Lake has only 19% of the houses with basic sanitation and, consequently, waste can be disposed in the Mundaú Lake and urban rivers 14 . The present study stresses this problem, as 7.4% of the shellfish pickers waste directly in the Mundaú Lake and the remaining population interviewed have septic tanks, which means that there is no basic sanitation in the community. The E. vermicularis eggs that were found, without the need of the parasitic specific Graham test, might indicate that the real prevalence is higher than our present results. Furthermore, it is noted that an adult was positive for this specific parasite, considering that children are more frequently affected. Previous parasitic studies with adults food handlers and fishermen also reported cases of E. vermicularis 26,27 . Adequate hygienic sanitary habits are more important than basic sanitation to prevent the aforementioned parasite transmission, considering that it is commonly diagnosed in people with close proximity and transmitted by direct contact or through contaminated objects.
Three of the four positive sand areas were adjacent and located in a region where shellfish are handled and sold, contributing to food contamination and affecting more individuals. The larvae found in the sand were from the Ancylostomatidae family, and eggs of this parasite were found in the parasitological examination of feces, which increase the hypothesis that the shellfish pickers may have become infected at their work environment 28 .
The extreme precariousness of artisanal fishing increases the likelihood of fishers suffering accidents and contracting diseases due to the significant physical effort required, climatic variations and contact with pathological agents in an environment with not enough basic sanitation [29][30][31] . Thus, the age is a restrain factor for shellfish pickers, reducing their working period, which could explain the negative results in all "marisqueiras" aging above 60 years old.
The low education level, including analphabetism, was statistically significant as a risk factor among the shellfish pickers. Higher prevalence of intestinal parasites is found in lower socioeconomic classes with less education 32 . Education level is an important factor in understanding diseases, forms of transmission and prevention 33,34 . Other studies also found a relationship between low education levels and transmission of schistosomiasis 35,36 and other enteroparasites 37 .
Despite importance of artisanal fishing communities in the Brazilian fish production, these people are generally among the poorest groups in the population, and this may be due to their dependence on exploiting a limited natural resource and the inherent unpredictability of fishing 18,38 . In our study, the monthly family income of 33 shellfish pickers (80.48%) was below one minimum wage. Similar percentages were found in a parasitological study in the suburb of Manaus, where 90% of the people earned less than one minimum wage 32 . Such a low income precludes investing in personal protective equipment (PPE), important to minimize risks and infection during work-related activities 39 .
Considering that low education was the risk factor related to parasitic infection, a higher investment of the government in adult education is necessary, in order to facilitate the population knowledge about preventive measures for parasitic diseases.
Some of the diagnosed parasitic infections could be controlled if the shellfish pickers had access to courses focused in personal hygiene, food handling and environment contamination, with the main goal of changing the established habits and further protecting the shellfish pickers and costumers health. Furthermore, actions related to better basic sanitation and adequate wasting are fundamental.

ACKNOWLEDGMENTS
We offer our deepest thanks to Vieira de Lima Fishing Colony that provided support for the development of this study.