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Landless Farmworkers in Sergipe – Brazil: Assessment on S. mansoni in Epidemiological Queries Author Information * Correspondence: MsC Genilde Gomes de Oliveira. Federal University of Sergipe Brazil. Email address [email protected]. Address: Claúdio Batista Street, no number; Sanatório Neighborhood. Aracaju City, United of Sergipe- Brazil Drª Angela Maria da Silva. Federal University of Sergipe - Brazil. Email address: [email protected] DRª Karina Conceição Gomes Machado de Araujo. Federal University of Sergipe Brazil. Email address: [email protected] Dr. Roque Pacheco de Almeida. Federal University of Sergipe - Brazil. Email address: [email protected] MsC Marcio Bezerra Santos. Federal University of Sergipe - Brazil. Email address: [email protected] MsC Luciana Barros de Santana. Federal University of Sergipe - Brazil. Email address: [email protected] 1Landless Farmworkers in Sergipe – Brazil: Assessment on S. mansoni in Epidemiological Queries Abstract Background: Schistosomiasis mansoni is a disease caused by the digenetic trematode Schistosoma mansoni. It is an endemic disease in 78 tropical and subtropical countries. In Brazil, it affects the States of Alagoas, Pernambuco, Sergipe, Bahia, Paraíba, and Minas Gerais. The Movimento de Sem Terras [Landless Workers' Movement] – MST is a Brazilian movement, which has as objective the implementation of the land reform. Methods: This is a cross-sectional study conducted in 2010 and 2015, when 13 Landless settlements were investigated. These farmworkers are susceptible to the disease due to migration to areas considered by them as nonproductive areas and they use the river water for consumption, domestic chores and leisure. In 2010, 601 individuals were enrolled in the research, as they delivered the stool pathophysiology test in 2015, 1139. In the two queries, TF (Test® Three Fecal Test) was used for stool analysis and in the second query the positive results were submitted to an abdominal ultrasound. Results: In 2010, a 4.3% proportion of positive parasitological tests for S. mansoni was obtained in the intestinal chronic phase. In 2015, 2.6% were infected, eight of them in the hepato-intestinal phase. In the second query, a disordered population increase was observed; the settlements maintained the social-demographic conditions of the first, such as lack of basic sanitation, sewerage systems, treated water for consumption and education level. In the two queries, the positive human cases were treated and the most severe ones were referred to the outpatient department of University Hospital of Universidade Federal de Sergipe for follow-up. Out of the 13 settlements assessed in 2010, 08 (61.5%) had a positive result for S. mansoni. In 2015, 11 (84.6%) showed a positive result. In the year of 2010 and 2015, the occurrence of nine species of helminths and four species of protozoa was shown. Conclusion: The second query shows a worrying scenario, there was an increase in the number of settlements with focus of the disease and there was a worsening in the clinical setting, considering that in 2010 the intestinal chronic setting was evidenced, and in the second query the hepatic impairment was observed. The pressing need for intervention by the government regarding disease prevention and control is notorious. Key-words: Schistosomiasis, epidemiology, parasitoses. 1 The manuscript does not have trial registration number for the case of two independent cross-sectional studies. The second survey is an extension of the first authorized by the Research Ethics Committee of the Universidade Federal de Sergipe -UFS, CAAE – 0081.0.107.000-08. BACKGROUND Schistosomiasis mansoni is a disease caused by the digenetic trematode (Schistosoma mansoni), the important manifestation of which is related to liver fibrosis caused by the parasite1. It is characterized as asymptomatic in the beginning, and it can evolve to extremely severe forms and lead to the patient's death2. Its distribution is associated with several factors, including complex social and cultural processes related to human behavior and disordered occupation of urban areas3. It is endemic in 78 countries, tropical and subtropical, 42 of them located in Africa4. According to the World Health Organization – WHO (2012), approximately 240 million people are infected with this disease, specially in Africa, Asia and the Americas5, of those, 120 million experience symptoms and 20 million experience severe diseases all over the world4. In Brazil, it is endemic in the littoral zone, however, its higher prevalence is observed in the States of Alagoas, Pernambuco, Sergipe, Bahia, Paraíba, and Minas Gerais6. The State of Sergipe has one of the highest prevalences in the country, according to the data from the Ministry of Health, the mean prevalence of schistosomiasis in Sergipe during the period of 1980 through 1989 was 17.3%, the second highest in Brazil, only lower than the one of the State of Alagoas. Considering the period between 1990 and 2002, the State mean was 17.7%, way above the national mean of 9.2%7. The precarious socioeconomic conditions, the difficulties of having access to health services, the migratory movements and the bad conditions of water treatment and sewer constitute the main factors for transmission of Schistosomiasis in endemic areas8. The Movimento de Sem Terra [Landless Workers' Movement] - MST is a Brazilian social movement initiated in the '80s, the main objective of which was to implement the land reform9. This population becomes susceptible to Schistosomiasis due to migration to lands considered by them as nonproductive areas, and they settle in farms under poor hygiene conditions, with no proper place for human waste and with no drinkable water, and they use the river water for consumption, domestic chores and leisure, favoring cycle of the disease progression10. Settlement is a set of independent farming units, settled by INCRA (Instituto Nacional de Colonização e Reforma Agrária [National Institute for Colonization and Agrarian Reform] where originally, there was a land real estate owned by a single owner. Each of these units is given by INCRA to a family with no economic conditions to purchase and maintain a land real estate by any other means. The land workers receiving the lot undertake to live in the parcel and to explore it for their own support, operated exclusively by the family11. In light of the severity and the harmful effects caused by the intestinal parasitoses and the scarce study on the current situation of enteroparasitoses in the State of Sergipe, this study assessed the occurrence of intestinal parasites based on the Schistosomiasis mansoni population living in Landless settlements in the South of the State of Sergipe and its clinical correlation. METHODOLOGY These are two cross-sectional studies conducted in 2010 and 2015. Thirteen Landless settlements were investigated, located in cities in the South region of the State of Sergipe, as shown in the map below (figure 1). It was attempted to maintain the same population from the first query, that is, from 2010, thus, the settlements investigated in the second query were the same as those in the first query. In 2010, 822 residents of settlements were interviewed, out of those, 601 were enrolled in the research, as they delivered the stool pathophysiology test. In 2015, 1772 were interviewed and 1139 delivered the stools for the analysis, being enrolled in the research. The test was conducted in the first stool bulk, in three samples, collected every other day. The stool was collected in an individual collector from the Kit TF Test® (Three Fecal Test). Based on the study conducted by Carvalho et al, in 2012, the TF Test® provides a reliable estimate of the infection prevalence by the protozoa in endemic areas. The socioeconomic and practical aspects showed that the TF-Test® technique is appropriate for individual diagnosis, population queries, as well as for the evaluation of chemotherapy administered in programs of intestinal parasitoses control12. The stool samples were submitted to the clinical analysis laboratory of the and analyzed by a single previously trained professional. The entire studied population signed an informed consent form (ICF), consenting to participate in the research. At the end of the study, treatment for all the individuals infected with S. mansoni was conducted, and the most severe cases were referred to the outpatient department of HU/UFS. Statistical Analysis The epidemiological data were described by simple and percent frequencies. The prevalence ratios and its respective confidence intervals were calculated to identify the potential factors associated with the year of assessment and the prevalence of Schistosoma mansoni. The analysis of categorical data was conducted along with the qui-square test and Fisher's exact test for small samplings. Then, the prevalence ratio measure of association was calculated with the respective 95% confidence intervals. The prevalence ratio was estimated through the prevalence calculation of the number of people with positive tests for Schistosoma mansoni compared with those with negative test. Ethical Considerations This Research Project was approved by the Research Ethics Committee of the Universidade Federal de Sergipe -UFS, CAAE – 0081.0.107.000-08. RESULTS Figure 2 shows the result of the stool pathophysiology test - EPF in 2010 and 2015. In table 1 the characterization of prevalence by gender and risk behavior of the Landless from the two queries can be observed. In table 2, the main clinical manifestations of the Landless with positive results for S. mansoni are presented. In the years 2010 and 2015, the occurrence of nine species of helminths (Ascaris lumbricoides, Enterobius vermicularis, Taenia solium, Taenia saginata, Trichuris trichiura, Ancylostoma duodenale, Hymenolepis nana, Strongyloides stercoralis, and Schistosoma mansoni) and four species of protozoa (Entamoeba sp., Endolimax nana, Giardia lamblia and Iodamoeba bütschlii.) were observed. The highest prevalence in the two periods studied was of the protozoa E. nana, 327 (55%) in 2010 and 523 (32%) in 2015. As shown in table 3. DISCUSSION The studied population increased since the last epidemiological query. In 2015, the double of parasitological tests was assessed and it was observed that the increase occurred in a disordered manner, with houses being built in the backyards, aggregating relatives; this disordered increase makes the population more vulnerable to the infection. Dabo et al, 2015 emphasizes that due to the migration and rapid and disordered urbanization, urban areas in Africa and South America are now the focus of transmission13. The field study conducted with the same population in 2010 and 2015 showed some important particularities for the epidemiological query. In 2010 the entire population diagnosed with S. mansoni was treated with praziquantel; nevertheless, in the new query it was observed the presence of helminthiasis in the population, also, one of the families that had been treated in the first query experienced the infection again in the second query, possibly as a consequence of reinfection. These data show the need for continuous control in risk populations and indicates the need to associate it with chemotherapy, control of molluscs in the water, supply of treated water, sanitation facilities and health education14. Among the patients with positive results in 2015, 29 (2.6%) were positive for Schistosomiasis, out of those, 23 (79.3%) made use of the rivers nearby the settlement to bathe, none of them had access to basic sanitation and treated water, so they used the water from the river or artesian wells. An identical scenario to that seen in 2010, with a prevalence of 26 (4.3%) and a usage frequency of the river of 61.5% was observed. Regarding the transmission conditions, Schistosomiasis is classically described as a land disease, which occurs in areas with no drinkable water and proper sanitation13. For some Landless, the contact with the river may be pointed out as accidental, involuntary and inevitable, considering that they need to cross it on a daily basis in order to conduct their social and labor activities, the study shows recreation by the river with a statistical significance of p 0.025. The study by Abou-Zeid et al, 2013, showed the higher risk for infection with Schistosomiasis in the rural area, with a five-fold increase compared with the urban area. Other factors identified were the risk associated with swimming and bathing in rivers and contact with rivers more frequently than once a week15. Despite the reduction in the prevalence, the situation of the Landless is still worrying in the South region of Sergipe. In 2010, 08 settlements had positive cases, in the new query, another three settlements were infected, that is, 11 showed positivity. In the study by Oliveira et al, 2013, it can be noticed that the Schistosomiasis control has been challenging for the public health services, because the importance of the disease is not restricted to its prevalence and geographical distribution, but it also incorporates issues as molluscicide-resistant molluscs, poor housing conditions and basic sanitation and economical activities related to the use of water. The presence of infection with S. mansoni in the settlements is worrying, because these migratory populations can transmit the disease to other regions, so development of public policies towards the disease control by the managers is required16. Symptoms such as headache and abdominal pain were the most prevalent in patients infected with S.mansoni, both in 2010 and 2015, showing an elevated rate of occurrences of symptoms, a setting similar to the one described in the literature on clinical manifestations in individuals with the parasite, in addition to these symptoms, cercarial dermatitis and Katayama fever may manifest in the acute phase of the disease17. In 2010, the intestinal clinical form was observed in all settlements; however, in 2015 the hepato-intestinal clinical form was observed in 08 out of 29 positive human cases. The intestinal form of Schistosomiasis mansoni is characterized by abdominal pain, diarrhea, bloody stools, nausea, fatigue, and somnolence18. The hepato-intestinal phase is characterized by the presence of diarrhea and epigastralgia. During physical examination, the patient experiences palpable liver, with nodules which in the most advanced phases correspond to areas with fibrosis due to periportal granulomatosis of Symmers' Fibrosis10. The occurrence of helminths and protozoa evidenced in 2010 was repeated in 2015, according to table 3. Oliveira et al 2012 conducted a study in land settlements in Sergipe, identifying high rates of parasite infections, predominantly with Endolimax nana, Entamoeba histolytica, Giardia lamblia, Ascaris lumbricoides, and Ancilostomideos. It was observed that the land settlements counted with minimal sanitation conditions and practices of personal and domestic hygiene, thus promoting conditions for the dissemination of parasite infections19. Infections with helminths are a noticeable subgroup among other neglected tropical diseases (NTD), propagated mainly due to lack of access to drinkable water and sanitation. CONCLUSION The second query shows a worrying scenario, the number of settlements with focus of the disease has increased, and there was worsening in the clinical setting, considering that in 2010 the intestinal chronic setting was observed and in the second query, liver impairment was observed. Also, the presence of nine species of helminthiases was observed in the two periods, supporting the evidence that governmental interventions are required regarding population education, basic sanitation and water treatment for consumption, seeking prevention and control of the disease. DECLARATIONS Presentation Letter We declare for the intent of publication that the entitled paper: Landless Farmworkers in Sergipe – Brazil: Assessment on S. mansoni in Epidemiological Queries, it’s being submitted for exclusivity publication at Infectious Diseases of Poverty. We also emphasize that the paper is extremely relevant since it’s related to a neglected disease, considered a big public health issue. All the related authors approve the paper for publication. Authors’ Contributions GGO – Been involved in drafting the manuscript and acquisition of data; AMS – Been involved in drafting the manuscript and revising critically for important intellectual content; KCA – Analysis and interpretation of data; RPA – Analysis and interpretation of data; MBS – Acquisition of data and LBS – Acquisition of data. All the authors read and approved the final manuscript. Availability of Data and Materials The Manuscript’s data were not shared because it is a research with possibilities new developments. The data will be available after the effective research’s conclusion. Competing Interest The authors declare that there have no competing interest. Approval of the Ethics Committee This research project was approved by the Research Ethics Committee of the Universidade Federal de Sergipe -UFS, CAAE – 0081.0.107.000-08. Consent to Publish I, _____________________________________________________________, undersigned, allow the researcher: Genilde Gomes de Oliveira , under the guidance of the Dr. Ângela Maria da Silva, to develop the research described below: Landless Farmworkers in Sergipe – Brazil: Assessment on S. mansoni in Epidemiological Queries. The study will be made in the settlements of the landless rural workers, located in the southern region of the State of Sergipe Expected benefits: Contribute with the upkeep of Community Health. Informations: The participants are guaranteed will be answered about any question and will be clarified about any doubt associated to the research subjects. And the aforementioned researcher is committed to provide updated informations got during the study. Withdrawal of Consent: The voluntary is free to withdraw you consent of any moment and leave the study, without harm to voluntary. Legal Aspect: Prepared in accordance with the guidelines and standards of research involving humans comply with Resolution nº. 466/2012. Reliability: The voluntarys will have the right to privacy. The identity (full names) of the participant will not be released. Yet the voluntarys signed the term of consent to the results can presented at conferences and publications. About the indemnity: Don’t have predictables harms in the research results, nevertheless will have indemnity if necessary. Aracaju, _____de _____de 200____ _____________________________________ Signature of Research/ Legal Representative. ________________________________________ Signature of Witness _________________________________________ Signature of Representative about the Study. Acknowledgements None Funding Financed by authors List of abbreviations MST – Movimento de Sem Terras [Landless Workers' Movement] TF TEST - Three Fecal Test WHO- World Health Organization INCRA (Instituto Nacional de Colonização e Reforma Agrária [National Institute for Colonization and Agrarian Reform] HU - University Hospital UFS- Universidade Federal de Sergipe EPF – Exame Parasitológico de Fezes [Stool pathophysiology test] S. mansoni - Schistosoma mansoni ICF - Informed Consent Form NTD - Neglected Tropical Diseases REFERÊNCIAS 1 - Amorim RF et al. Schistosomiasis in The Northern State of Espírito Santo, Brazil. Rev Patol Trop. 2014. Vol. 43 (3): 323-331. 2- Silva MBA et al. Perfil Epidemiológico de Pacientes Suspeitos de Esquistossomose e Patologias Associadas em um Hospital Pernambucano. Rev. Enf. 2015, 1(1):43 - 46. 3 - de Souza Gomes et al. Risk Analysis for Occurrences of Schistosomiasis in the Coastal Area of Porto de Galinhas, Pernambuco, Brazil. Infectious Diseases of Poverty. 2014, 14:101 . 4 - He et al. Nucleic Acid Detection in the Diagnosis and Prevention of Schistosomiasis. Infectious Diseases of Poverty. 2016, 5:25. 5 - World Health Organization (WHO). Schistosomiasis: Progress Report 2001-2011 and Strategic Plan 2012-2020. Geneva: WHO, 2012. 6 - Assaré et al. Sustaining Control of Schistosomiasis mansoni in Moderate Endemicity Areas in Western Côte d’Ivoire: A SCORE Study Protocol. Public Health. 2014, 14:1290. 7 - Rollemberg CVV et al. Aspectos Epidemiológicos e Distribuição Geográfica da Esquistossomose e Geo-Helmintos, no Estado de Sergipe, de Acordo com os Dados do Programa de Controle da Esquistossomose. Rev. Soc. Bras. Med. Trop. 2011, 44(1):9196. 8 - Silva PCV, Domingues ALC. Aspectos Epidemiológicos da Esquistossomose Hepatoesplênica no Estado de Pernambuco, Brasil. Epidemiol. Serv. Saúde. Brasília, 2011, 20(3):327-336. 9. Patriarcha TF; Pastor M. Gênero e Movimento dos Trabalhadores Rurais Sem Terra. 2011. 10. Santos GO dos. Aspectos Epidemiológicos da Esquistossomose em Trabalhadores Rurais Sem Terra no Estado de Sergipe. Dissertação (Mestrado em Ciências da Saúde) – Universidade Federal de Sergipe. Aracaju, 2010. 11. INCRA – Institututo Nacional de Colonização e Reforma Agrária. 2016. 12. Carvalho GLX de et al . A Comparative Study of the TF-Test®, Kato-Katz, Hoffman-Pons-Janer, Willis and Baermann-Moraes Coprologic Methods for the Detection of Human Parasitosis. Mem. Inst. Oswaldo Cruz. Rio de Janeiro, 2012. v. 107, n. 1, p. 80-84. 13. Dabo et al. Urban Schistosomiasis and Associated Determinant Factors Among School Children in Bamako, Mali, West Africa. Infectious Diseases of Poverty. 2015, 4:4. 14. Masaku et al. Current status of Schistosoma mansoni and the factors associated with infection two years following mass drug administration programme among primary school children in Mwea irrigation scheme: A cross-sectional study. Public Health. 2015, 15:739. 15. Abou-Zeid et al. Schistosomiasis Infection Among Primary School Students in a War Zone, Southern Kordo fan State, Sudan: a Cross-Sectional Study. Public Health. 2013, 13:643. 16 - Oliveira GG et al. Epidemiological Aspects of Schistosomiasis in Workers of the Movement of Landless Rural Workers. Rev. Soc. Bras. Med. Trop. 2013, 46( 4 ): 519521 17.Vitorino RR et al. Esquistossomose Mansônica: Diagnóstico, Tratamento, Epidemiologia, Profilaxia e Controle. Rev. Bras Clin Med. São Paulo. 2012,10(1):3945. 18. Mazigo et al. Epidemiology and Interactions of Human Immunodeficiency Virus – 1 and Schistosoma mansoni in Sub-Saharan Africa Infectious. Infectious Diseases of Poverty. 2014, 3:47. 19.Oliveira GG de et al. Prevalence of Intestinal Parasitoses in Families of Landless Workers' Mvement. Rev. enferm UFPE online. 2012, 6(10):2490-6. Figure legends Figure 01: Space Distribution of the MST Settlements by City LEGEND Brazil Sergipe Southern Region of Sergipe Settlements