Intestinal Parasitic Infection in the Suruí Indians, Brazilian Amazon.

Cassius S. Palhano-Silva, Adauto J. G. Araújo, Ana E. P. Lourenço, Otílio M. P. Bastos, Ricardo V. Santos and Carlos E. A. Coimbra, Jr.

Cassius S. Palhano-Silva. M.D., Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Brazil. M.Sc. in Public Health, Escola Nacional de Saúde Pública (ENSP), Brazil. Researcher, ENSP, Rio de Janeiro, Brazil.

Adauto J. G. Araújo. M.D., UNIRIO, Brazil. D.Sc. in Public Health, ENSP, Brazil. Professor, ENSP and Director of Medical and Health Sciences, Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro, Brazil.

Ana E. P. Lourenço. Nutritionist, Universidade Federal Fluminiense (UFF), Brazil. M.Sc. in Public Health and doctoral student, ENSP, Rio de Janeiro, Brazil.

Otílio M. P. Bastos. M.D., UFF, Brazil. D.Sc. in Parasitology, Fundação Instituto Oswaldo Cruz (FIOCRUZ), Brazil. Professor and Director, Centro de Ciências Médicas, UFF, Brazil.

Ricardo V. Santos. B.Sc. in Biology, Universidade de Brasília, Brazil. Ph.D. in Biological Anthropology, Indiana University USA. Professor, ENSP, FIOCRUZ and UNIRIO, Brazil.

Carlos E. A. Coimbra Jr. B.Sc. in Biology, Universidade de Brasília, Brazil. Ph.D. in Medical Anthropology, Indiana University, USA. Professor, ENSP, Brazil. Address: Escola Nacional de Saúde Pública, FIOCRUZ, Rua Leopoldo Bulhões 1480, Rio de Janeiro, RJ 21041-210, Brazil. e-mail: coimbra@ensp.fiocruz.br

SUMMARY

This study reports the results of a cross-sectional survey carried out in 2005 to investigate the epidemiology of intestinal parasitism among the Suruí Indians, Brazilian Amazon. A total of 519 stool samples were examined by zinc-sulphate-flotation and formol-ether-sedimentation. Entamoeba histolytica/E. dispar-positive samples were further tested by ELISA. Thirty-six percent of the subjects were positive for one more helminth species; 70.7% harbored at least one protozoan species. The most frequent helminth was Hymenolepis nana (29.5%). Nematodes were rare (hookworm= 3.3%; Strongyloides stercoralis= 0.2%). Capillaria sp. was identified in 5.2% of the samples and one case of parasitism by Dipylidium caninum was detected. Prevalence of Giardia duodenalis and E. histolytica/E. dispar was 16.2% and 12.3%, respectively. Based on ELISA, the prevalence of E. histolytica infection was 3.2%. The overall prevalence of intestinal nematode infections depicted in this study was surprisingly low compared to what is often reported for other indigenous populations in the Brazilian Amazon. It is argued that the prevalence of helminths in the Suruí are associated with anthelminthic mass treatment schemes undertaken by the Indian health service, in the absence of other measures. The authors propose that a special program aimed at controlling intestinal parasitism in indigenous communities should step beyond the top-down distribution of medication, but rather be designed in collaboration with the target population, encompassing education, better housing, alternative sewage disposal systems and safe water supply to all villagers.

Parasitosis intestinal en los Indios Suruí, Amazonia Brasilera.

RESUMEN

Se reportan los resultados de un estudio transversal llevado a cabo en 2005 sobre la epidemiología del parasitismo intestinal en indios Suruí de la amazonia brasilera. Un total de 519 muestras de heces fueron examinadas por flotación en sulfato de zinc y sedimentación en etil-éter. Muestras positivas para Entamoeba histolytica/E. dispar fueron testeadas por ELISA. Una o más especies de helmintos estuvieron presentes en 36% de los sujetos y 70,7% presentaron al menos una especie de protozoario. El helminto más frecuente fue Hymenolepis nana (29,5%). Los nematodos fueron escasos (anquilostomo= 3,3%; Strongyloides stercoralis= 0.2%). Se identificó Capillaria sp. en 5,2% de las muestras y se detectó un caso de parasitismo por Dipylidium caninum. Las prevalencias de Giardia duodenalis y E. histolytica/E. dispar fueron 16,2% y 12,3%, respectivamente. Según ELISA la prevalencia de infección por E. histolytica fue 3,2%. La prevalencia de infección por nematodos fue sorpresivamente baja en comparación con reportes frecuentes en otras poblaciones indígenas de la amazonia brasilera. Se argumenta que los cambios en la prevalencia de helmintiasis en los Suruí se asocian a tratamientos masivos con antihelmínticos llevados a cabo por el servicio de salud de indígenas, en ausencia de otras medidas. Se propone que un programa especial orientado a controlar el parasitismo intestinal en poblaciones indígenas debe desligarse de la distribución de medicación, sino ser diseñado en colaboración con los habitantes locales, abarcando educación, mejores viviendas y sistemas de drenaje y disposición de residuos, y suministro de agua segura a todos los pobladores.

Infecção por parasitoses intestinais entre os Indios Suruí, Amazônia Brasileira.

RESUMO

Este trabalho apresenta os resultados de um estudo seccional conduzido em 2005 que visou investigar o perfil epidemiológico das parasitoses intestinais entre os índios Suruí, localizados em Rondôna, Amazônia brasileira. Um total de 519 amostras fecais foi examinado pelas técnicas de flutuação com sulfato de zinco e sedimentação com formol-éter. Amostras positivas para Entamoeba histolytica/E. díspar foram posteriormente testadas pelo método ELISA. Trinta e seis por cento dos indivíduos encontravam-se positivos para pelo menos uma espécie de helminto; 70,7% abrigavam pelo menos uma espécie de protozoário. O helminto mais freqüente foi Hymenolepis nana (29,5%). Nematódeos foram raros (ancilostomídeos= 3,3%; Strongyloides stercoralis= 0,2%). Capillaria sp. foi identificado em 5,2% das amostras e um caso de parasitismo por Dipylidium caninum foi observado. As prevalências de Giardia duodenalis e E. histolytica/E. dispar foram de 16,2% e 12,3%, respectivamente. Baseada no teste ELISA, a prevalência de infecção por E. histolytica foi de 3,2%. A prevalência total de infecção intestinal por nematódeos demonstrada neste estudo foi surpreendentemente baixa se comparada ao que tem sido geralmente reportado para outras populações indígenas da Amazônia brasileira. Argumenta-se que a baixa prevalência de helmintos entre os Suruí está em larga medida associada a esquemas de tratamento em massa com anti-helmínticos dispensados pelo serviço de saúde indígena. Os autores propõem que um programa especial destinado ao controle de parasitoses intestinais em comunidades indígenas deve ir além da distribuição de medicamentos. Preferencialmente, deve ser planejado em colaboração com a população alvo, considerando aspectos educacionais e visando a melhoria nas moradias e no sistema de esgoto e de fornecimento de água.

KEYWORDS / Amazonia / Epidemiology / Helminth Control / Intestinal Helminths / Intestinal Protozoa / South American Indians /

Received 07/26/2008. Modified: 03/16/2009. Accepted: 03/17/2009.

Introduction

Intestinal parasites are important causes of morbidity among indigenous peoples of Amazonia. Most studies carried out among different ethnic groups stress a high prevalence of intestinal nematode infections (ascariasis, trichuriasis, hookworms, and strongyloidiasis), often affecting over half the village population, and moderate prevalence of cestode infections (mainly hymenolepiasis). Cases of taeniasis have been rarely reported (Coimbra and Mello, 1981). As for intestinal protozoans, prevalence rates of Entamoeba histolytica/E. dispar and of Giardia duodenalis infections are variable and may affect nearly one fourth of the population (Lawrence et al., 1980; Coimbra and Santos, 1991a, b; Ferrari et al., 1992; Kroeger et al., 1992; Santos et al., 1995; Gómez et al., 2004; Rivero et al., 2007).

Recent changes experienced by indigenous peoples from Amazonia might greatly influence the epidemiology of intestinal parasites in these communities. The curtailment of population mobility and the adoption of new housing architecture have been pointed out as major drawbacks of such changes, directly implicated in the intensification of transmission of intestinal parasites (Schwaner and Dixon, 1974; Kroeger et al., 1992). Against a background of inadequate sanitation and insufficient safe water supply associated with sedentarization, environmental contamination of indigenous villages with infective protozoan cysts as well as eggs and/or larvae of helminths rapidly builds up and sustains year-round transmission of intestinal parasites at high levels of endemicity in these populations (Lawrence et al., 1980; Coimbra and Mello, 1981; Chernela and Thatcher, 1989; Coimbra and Santos, 1991b; Fitton, 2000; Gómez et al., 2004). If these factors might intensify parasite transmission, the implementation of basic sanitation associated with the widespread use of antihelminthic drugs, often cheap and readily available in the health services, might help to reduce prevalence.

The present study was carried out in the context of a rapidly changing Indian society of southwestern Brazilian Amazonia that is highly exposed to Western medical services, the Suruí. The study was designed to examine the prevalence of intestinal parasitism taking into consideration two important pieces of information: a) according to previous assessments of intestinal parasitism carried out in the Suruí, the prevalence of major parasitic helminths and protozoa was very high (Coimbra and Mello, 1981; Coimbra and Santos, 1991a); and b) in recent years the population has been receiving systematic health care by the Brazilian government, which include the implementation of basic sanitation in the villages and primary health care. As far as we are aware, the present study is the first of its kind carried out in an indigenous Amazonian society, as it provides a diachronic perspective in the interpretation of parasitological results by comparing the present-day situation among the Suruí with a previous survey. The study also aims at contributing to the understanding of the epidemiology of intestinal parasitism in indigenous populations in Amazonia in order to assist in the design of more effective and culturally-sensitive control measures.

Population and Methods

Fieldwork and setting

Fieldwork was carried out between February and March 2005 among the Suruí people of the Sete de Setembro Indian reserve, on the border between the states of Rondônia and Mato Grosso, southwestern Brazilian Amazon (~60-61ºW and 10-12ºS). The landscape is dominated by inter-fluvial tropical rain forest and is crisscrossed by small to medium-size rivers. Annual rainfall in the state of Rondônia presents a north-south gradient that varies from 2500 to 1750mm. Mean annual temperature is 24-26ºC; lower temperatures are recorded during the short dry season (June-August) when average temperature ranges between 20-22ºC (Nimer, 1979).

At the time of fieldwork the Suruí totaled 993 individuals (nearly 51% of the population was <15 years old) distributed over 11 villages. Nine villages, including the two largest ones, were surveyed by the research team, accounting for nearly 80% of the total population.

Physical examinations were carried out by one of the authors (Palhano-Silva) at a field clinic that was established in every village. No specific sampling technique was used. An attempt was made to examine all willing individuals of both sexes, independent of age. At the time of examination, a plastic container marked with an identification number and the name of the person was handed out along with instructions about how to collect a stool sample. Samples returned next morning were split into two subsamples: one was preserved with 5% formalin for examination by light microscopy and the other frozen at -20°C for ELISA testing. A household survey aimed at characterizing Suruí housing conditions and sanitation was also carried out. Data collected included house structure (type of walls, roof, and floor), availability of sanitary facilities and sources of drinking water.

Laboratory analyses

Stool specimens were examined by zinc sulphate flotation and formol-ether sedimentation techniques. One slide was prepared from each stool sample processed by each technique. Slides were independently examined by two of the authors (Palhano-Silva and Bastos). The presence of parasites was confirmed when eggs, cysts and/or larvae were observed with any of the two techniques.

In order to estimate E. histolytica infection, samples kept in the freezer were defrosted at room temperature and used in a monoclonal ELISA essay for E. histolytica adhesin (Entamoeba histolytica II -TechLab Inc., Blacksburg, VA, USA). ELISA was performed only on those samples that tested positive for E. histolytica/E. dispar under the microscope.

Management of patients and ethics

Subjects diagnosed with intestinal parasites were referred to the Indian health service in Cacoal for treatment. A single dose of 400mg of Albendazole was prescribed against nematode infections, a single dose of 5-10mg/Kg Praziquantel against cestodes, and Metronidazole 500-750mg three times a day against protozoan infections by G. duodenalis and/or E. histolytica/E. dispar infections, following standard dosages.

This study is part of a broader project about the health of Suruí Indians, whose major focus is the epidemiology of tuberculosis, but which also includes the general health and nutritional assessment of the population (Basta et al., 2006; Orellana et al., 2006). Guidelines for research in humans determined by the Brazilian National Committee on Research Ethics (CONEP) of the Ministry of Health were followed. A research permit was also obtained from the National Indian Foundation (FUNAI). A consent form was signed by the leaders of the surveyed villages. All field procedures were undertaken in the company of a local Suruí health agent indicated by the community, who helped explain the objectives of the research plan and acted as an interpreter when necessary.

Statistical analyses

Prevalence ratios were used to assess differences in proportions between age groups and sexes for the most prevalent helminths and protozoans. P values <0.05 were considered statistically significant and 95% confidence intervals were constructed around estimates. All statistics were performed using SPSS version 11 (SPSS Inc., Chicago, IL, USA).

Results

A total of 786 Suruí individuals of all ages and both sexes (79.2% of the total population in the visited villages) were examined. There was no refusal for physical examination (individuals who were not assessed were absent from the village during our visit). Abdominal complaints (such as pain, diarrhea, nausea and/or epigastralgia) were the most common symptoms, referred by 90% of the subjects. Respiratory symptoms (mostly dry cough) and arthralgia were also common complaints. No associations between symptoms and intestinal parasitism were observed.

Approximately 98% of Suruí houses have walls made of wood boards or bricks (mixed constructions were observed). Cemented floors are present in 95.4% of the houses. Roofs are often made with simple zinc corrugated sheets (77.0%); roofing tiles were observed in 20.8% of the houses. All households referred the village well as their major source of water for domestic use. These wells were excavated by the Indian health service and usually have an electric pump in order to distribute water to one or more public faucet taps scattered throughout the village. As for sewage disposal, collective pit latrines installed by the Indian health service are the rule and can be seen in the back of almost every house (93.8%) in all villages. These are shallow holes covered with a wooden platform that has an opening in the middle, encircled by a rudimentary wall made of wood boards painted white. Very few houses (6.0%) have private indoor privies with a flushing system.

A total of 519 stool samples were processed, representing 66.0% of the subjects who underwent physical examinations. Losses were determined by insufficient stools turned in or by the person’s inability to collect any specimen within the time-span given.

Table I summarizes the findings for protozoa and helminths by sex and age groups. The overall prevalence of intestinal protozoans was 70.7%. While the most affected age group by E. histolytica/E. dispar was that of adults >40 years old (19.7%), for G. duodenalis children 5-9 years were the most affected (28.8%). Helminths were detected in 36.0% of the samples examined. Overall prevalence of hymenolepiasis (i.e., H. nana and/or H. diminuta) was 30.1%, with the highest prevalence observed in children 5-9 years old (51.0%). The only nematodes detected were hookworms (3.3%) and S. stercoralis (0.2%). It is worth mentioning the absence of Ascaris lumbricoides and Trichuris trichiura, often reported in previous surveys of the kind. On the other hand, the finding of two helminth species not typically reported in surveys carried out in Amazonia should be highlighted. Twenty-eight subjects of various ages and both sexes presented Capillaria sp. eggs in the stools and the sample from one adult woman was positive to Dipylidium caninum. Considering the rarity of this finding, a new stool sample was collected from this person two months later and again proved positive to D. caninum. No association between prevalence of protozoan and/or helminth infection was discernible. Parasitism by more than one species of helminth and/or protozoa was detected in 46.2% of the samples.

For the three most frequent parasite species found (Hymenolepis spp., G. duodenalis and E. histolytica/E. dispar), ratios of prevalence of infection between adults and children were constructed (the ratio’s numerator indicates the proportion of a given infection in adults, while the denominator indicates its relative weight in children). Prevalence ratios for hymenolepiasis and giardiasis were, respectively, 0.48 (95% confidence interval: 0.34-0.68) and 0.31 (95% confidence interval: 0.18-0.54), indicating that children <10 years old constitute the most affected age group for these parasitic diseases. The infection prevalence ratio for amoebiasis was 1.83 (95% confidence interval: 1.06-3.17), which shows that this infection is almost twice more frequent among adults than children.

A total of 64 E. histolytica/E. dispar positive samples under microscopy underwent ELISA, 17 of which tested positive for E. histolytica. Therefore, based on ELISA results, the prevalence of E. histolytica infection in the population assessed was 3.2%. These include individuals of both sexes (53% males) and all age groups.

Table II compares the prevalence of major intestinal parasites observed in 2005 with previous data collected in 1987 for Suruí children <10 years old (Coimbra and Santos, 1991a) that was analyzed by the same technique and whose sample comprised 95% of the population in this age group. There have been sharp decreases in prevalence for most nematode species; frequencies dropping from >60% to <5% for A. lumbricoides and hookworms. Substantial decreases were also observed in the prevalence of S. stercoralis and T. trichiura. Notwithstanding, while infection frequencies dropped for all nematode species, cestode (Hymenolepis spp.) prevalence increased from 19.4 to 39.4%.

Discussion and Conclusions

The overall prevalence of intestinal nematode infections depicted in this study was surprisingly low compared to the 40-60% often reported for other indigenous populations in the Brazilian Amazon (Chernela and Thatcher, 1989; Confalonieri et al., 1989; Salzano, 1990; Coimbra and Santos, 1991b; Santos et al., 1995). Previous surveys carried out in the Suruí (Coimbra and Mello, 1981; Coimbra and Santos, 1991a) revealed a completely different picture, more similar to what most authors have found in other indigenous communities in Amazonia, i.e., high prevalence of infection by A. lumbricoides, T. trichiura and hookworms, with over 50% of the population harboring at least one helminth species. These early surveys carried out among the Suruí also showed high infection rates by S. stercoralis (30%), the highest so far reported for an indigenous group in Amazonia. Interestingly, when comparing data for children below age 10 in 1987 and 2005, the present study revealed a much higher prevalence of hymenolepiasis.

It is well established that environmental contamination with infective parasite forms (e.g., eggs, larvae, cysts) is critical to the epidemiology of intestinal parasitism. For this reason, housing and sanitation play a key role in control strategies. Educational interventions to promote better hygiene (e.g., food preparation, clean water storage, housekeeping) and periodic de-worming aimed at target populations (e.g., children) are considered important supplementary measures (Okun, 1988; Albonico et al., 1999; Scolari et al., 2000; Asaolu and Ofoezie, 2003; Urbani and Albonico, 2003; Sur et al., 2005).

Health services provided to indigenous peoples in Brazil have gone through major changes in the last decade. A new system, integrated with the national unified health system (known as SUS) was initiated in 1999 (Garnelo et al., 2003). Primary care is to be dispensed at the village level by Indian health agents. Multi-professional health teams provide continuous supervision, and patients in need of further assistance are referred to Indian health clinics (Casa de Saúde do Índio) or general hospitals in the nearest town. Another aspect that has been emphasized is village sanitation, focusing on the construction of pit-latrines and collective wells.

Despite its many limitations (e.g., lack of personnel and uncertain budget), the current system has facilitated the access of Indian patients to health services. A greatly increased investment of resources from higher levels of the system to the local levels has produced at least one immediate result: village health posts are stocked with an unprecedented diversity of drugs. Among these are the antihelminthics. During fieldwork it was found that the Suruí had been under a mass treatment regime for at least the previous 18 months. According to the head nurse of the local Indian health clinic in the city of Cacoal, to where Suruí patients are referred, the following bi-annual regime was being applied at the time: Albendazole 400mg single dose for adults and children ³10 years old, and Mebendazole 100mg twice daily during three days for children <10 years old. The regime was repeated after one week. The last de-worming campaign among the Suruí had been carried out at all villages in the semester previous to this survey.

Unfortunately, it appears that the ready availability of unexpensive anti-parasitic drugs in Brazil, coupled with the prevailing view among health professionals that these are relatively safe and can be administered with minimal technical supervision, has led to the adoption of unsystematic de-worming campaigns by the Indian health service. Usually, baseline surveys are not conducted, which precludes the proper evaluation of the intervention, and no clear-cut intervals between mass treatments are established. The long-term challenge, however, remains, since as it has been exhaustively demonstrated, re-infection is likely to take place rapidly. Drug mass therapy may reduce morbidity in the short run but it does not ensure sustained control of intestinal parasitism (Machado et al., 1996; Idris et al., 2001; WHO, 2001; Beltramino et al., 2003; Zani et al., 2004). This can only be achieved by significantly reducing both fecal contamination of the environment and human exposure to potentially contaminated sources. Moreover, independently of its practicality and minimal risks for human subjects, the indiscriminate distribution of antihelmintics to Indian villagers can produce at least one unwanted effect in the long run: the emergence of resistant helminth strains (Geerts and Gryssels, 2001; Albonico, 2003).

The efficacy of such unsystematic distribution of antihelmintics can also be challenged on the basis of its lack of specificity. Although this survey identified hymenolepiasis as the major helminth problem in the population, the drug regime prescribed by the Indian health service was clearly not adequate to eliminate cestodes (Amato-Neto et al., 1990; MeCraeken et al., 1992; Horton, 2000; Juan et al., 2000). Over 30% of the general population is infected with H. nana/H. diminuta and nearly 50% of the children <10 years old harbor the parasite. As noted by Mirdha and Samantray (2002), the clinical and epidemiological importance of hymenolepiasis should not be overlooked, especially in children, due to its implication in immunosuppression and flattered growth.

Various authors have highlighted that it does not necessarily follow that simply increasing the number of latrines in a community achieves a significant reduction in the rate of parasite transmission (Asaolu and Ofoezie, 2003; Corrales et al., 2006). As shown in this study, most Suruí families have access to pit-latrines. These are usually installed outdoors, at the back of the houses, and are intended for collective use. Through observation and informal conversations with Suruí villagers, however, one finds that these are not always used (as is revealed by the dense grasses that often encircle the little latrines), with the excuse of insufficient privacy, bad smell and the constant nuisance of flies.

This study also revealed some further unusual parasitological findings that deserve comment. The presence of Capillaria sp. eggs in stools has been reported in other studies carried out among indigenous peoples in the Amazon (Coimbra and Mello, 1981; Santos et al., 1985, 1995; Carme et al., 2002). This has been interpreted as resulting from transit eggs probably due to the recent ingestion of lightly cooked game liver. Among the Suruí game liver is considered a delicacy. True parasitism by C. hepatica does not pass eggs in stools, and human intestinal parasitism by any other species of Capillaria is unknown in South America (Bhattacharya et al., 1999). The finding of D. caninum is rather unusual in surveys carried out throughout Brazil and probably indicates close human-dog contact (Marinho and Neves, 1979). Suruí villages have countless free-roaming dogs, increasing the likelihood of human exposure to zoonotic helminths.

As already indicated, the changing pattern in intestinal parasitic infections (especially nematodes) among the Suruí is probably related to recent interventions undertaken by the Indian health service with a focus on mass chemotherapy. Notwithstanding, the high prevalence of intestinal protozoa infections in general clearly indicates that fecal-oral routes of transmission have not been effectively eliminated in the Suruí. Protozoa species well known for their role in determining serious gastrointestinal ailments were detected during the study, and the presence of E. histolytica in the population was confirmed by ELISA. Although more severe forms of amoebiasis and giardiasis are rare, both E. histolytica and G. duodenalis can cause acute and persistent diarrhea and may be implicated in nutrient malabsorption, leading to growth and development retardation (Lima and Guerrant, 1992; Farthing, 2002; Gendrel et al., 2003). This constitutes an issue of concern since protein-energy malnutrition affect one-fourth of Suruí children <10 years old and the prevalence of anemia in this age group is 80% (Orellana et al., 2006). Although the precise diagnosis of protozoal parasites by conventional microscopy presents difficulties, enzyme immunoassays and molecular techniques are not readily available in laboratory routine by the Brazilian public health service.

A sustainable program for the control of intestinal parasites in the Suruí should consider alternative ways for environmental sanitation that take into account Suruí perceptions about gastrointestinal disease, housing, personal hygiene and environmental health. Top-down approaches like those observed are unlikely to produce long-lasting results. A special consideration should be given to children, since they tend to be more susceptible to gastrointestinal infection in general. For this reason, a sanitation program should be designed in collaboration with the target population, encompassing educational measures, better housing, an alternative sewage disposable system, and safe water supply to all villagers. These measures will yield results far beyond the control of specific diseases or parasites, raising health standards more effectively.

Acknowledgements

The authors thank the Suruí for their hospitality and support in all phases of the study. Researchers from the Centro de Estudos em Saúde Indígena de Rondônia of the Universidade Federal de Rondônia, as well as the local staff of the National Health Foundation (FUNASA) and the National Indian Foundation (FUNAI) provided logistical support and advice. This study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 470850/2004-3 and 506392/2004-0) and The Ford Foundation.

References

1. Albonico M (2003) Methods to sustain drug efficacy in helminth control programmes. Acta Trop. 86: 233-242.        [ Links ]

2. Albonico M, Crompton DWT, Savioli L (1999) Control strategies for human intestinal nematode infections. Adv. Parasitol. 42: 277-341.        [ Links ]

3. Amato-Neto V, Moreira AAB, Ferreira GMP, Nascimento SAB, Matsubara L, Campos R, Pinto PLS (1990) Avaliação da atividade terapêutica do Albendazol sobre infecções experimental e humana pela Hymenolepis nana. Rev. Inst. Med. Trop. São Paulo 32: 185-188.        [ Links ]

4. Asaolu SO, Ofoezie IE (2003) The role of health education and sanitation in the control of helminth infections. Acta Trop. 86: 283-294.        [ Links ]

5. Basta PC, Coimbra CEA, Escobar AL, Santos RV, Alves LCC, Fonseca LS (2006) Survey for tuberculosis in an indigenous population of Amazonia: the Suruí of Rondônia, Brazil. Trans. R. Soc. Trop. Med. Hyg. 100: 579-585.        [ Links ]

6. Beltramino D, Lurá MC, Carrera E (2003) El tratamiento antihelmíntico selectivo frente al tratamiento masivo: Experiencia en dos comunidades hiperendémicas. Rev. Panam. Salud Publ. 13: 10-18.        [ Links ]

7. Bhattacharya D, Patel AK, Das SC, Sikdar A (1999) Capillaria hepatica, a parasite of zoonotic importance - a brief overview. J. Commun. Dis. 31: 267-269.        [ Links ]

8. Carme B, Motarda A, Bau P, Day C, Aznar C, Moreau B (2002) Intestinal parasitosis among Wayampi Indians from French Guiana. Parasite 9: 167-174.        [ Links ]

9. Chernela JM, Thatcher VE (1989) Comparison of parasite burdens in two native Amazonian populations. Med. Anthropol. 10: 279-285.        [ Links ]

10. Coimbra CEA, Mello DA (1981) Enteroparasitoses e Capillaria sp. entre o grupo Suruí do Parque Indígena Aripuanã, Rondônia. Mem. Inst. Osw. Cruz 76: 299-302.        [ Links ]

11. Coimbra CEA, Santos RV (1991a) Avaliação do estado nutricional num contexto de mudança sócio-econômica: o grupo indígena Suruí do estado de Rondônia, Brasil. Cad. Saúde Publ. 7: 538-562.        [ Links ]

12. Coimbra CEA, Santos RV (1991b) Parasitismo intestinal entre o grupo indígena Zoró, Estado de Mato Grosso (Brasil). Cad. Saúde Publ. 7: 100-103.        [ Links ]

13. Confalonieri U, Araújo A, Ferreira LF (1989) Enteroparasitos em índios Yanomami. Mem. Inst. Osw. Cruz 84 (Supl. 4): 111-113.        [ Links ]

14. Corrales LF, Izurieta R, Moe CL (2006) Association between intestinal parasitic infections and type of sanitation system in rural El Salvador. Trop. Med. Int. Health 11: 1821-1831.        [ Links ]

15. Farthing MJ (2002) Tropical malabsorption. Sem. Gastrointest. Dis. 13: 221-231.        [ Links ]

16. Ferrari JO, Ferreira MU, Camargo LMA, Ferreira CS (1992) Intestinal parasites among Karitiana indians from Rondônia State, Brazil. Rev. Inst. Med. Trop. São Paulo 34: 223-225.        [ Links ]

17. Fitton LJ (2000) Helminthiasis and culture change among the Cofán of Ecuador. Am. J. Hum. Biol. 12: 465-477.        [ Links ]

18. Garnelo L, Macedo G, Brandão LC (2003) Os Povos Indígenas e a Construção das Políticas de Saúde no Brasil. Pan-American Health Organization. Brasília, Brazil. 120 pp.        [ Links ]

19. Geerts S, Gryssels B (2001) Antihelmintic resistance in human helminthes: a review. Trop. Med. Int. Health 6: 915-921.        [ Links ]

20. Gendrel D, Treluyer JM, Richard-Lenoble D (2003) Parasitic diarrhea in normal and malnourished children. Fund. Clin. Pharmacol. 17: 189-197.        [ Links ]

21. Gómez J, Botto C, Zent S, Marín A, Sánchez J, Noguera C, Rangel T (2004) Influencia del tipo de vivienda y del tamaño de asentamiento de comunidades indígenas Piaroa en la transmisión de helmintos intestinales. Interciencia 29: 389-395.        [ Links ]

22. Horton J (2000) Albendazole: a review of antihelmintic efficacy and safety in humans. Parasitology 121: S113-S132.        [ Links ]

23. Idris MA, Shaban MAA, Fatahallah M (2001) Effective control of hookworm infection in school children from Dhofar, Sultanate of Oman: a four-year experience with albendazole mass chemotherapy. Acta Trop. 80: 139-143.        [ Links ]

24. Juan JO, López CN, Gargala G, Favennec L (2000) Comparative clinical studies of nitazoxanide, albendazole and praziquantel in the treatment of ascariasis, trichuriasis and hymenolepiasis in children from Peru. Trans. R. Soc. Trop. Med. Hyg. 96: 193-196.        [ Links ]

25. Kroeger A, Schulz S, Witte B, Skewes-Ramm R, Etzler A (1992) Helminthiasis and cultural change in the Peruvian rainforest. J. Trop. Med. Hyg. 95: 104-113.        [ Links ]

26. Lawrence DN, Neel JV, Abadie SH, Moore LL, Adams LJ, Healy GR, Kagan IG (1980) Epidemiological studies among Amerindian populations of Amazonia. III. Intestinal parasitosis in newly contacted and acculturating villages. Am. J. Trop. Med. Hyg. 29: 530-537.        [ Links ]

27. Lima AA, Guerrant RL (1992) Persistent diarrhea in children: epidemiology, risk factors, pathophysiology, nutritional impact, and management. Epidemiol. Rev. 14: 222-242.        [ Links ]

28. Machado MT, Machado TMS, Yoshikae RM, Schmidt ALA, Faría RCA, Paschoalotti MA, Barata RCB, Chieffi PP (1996) Ascariasis in the subdistrict of cavaços, municipality of Alterosa (MG), Brazil: effect of mass treatment with albendazole on the intensity of infection. Rev. Inst. Med. Trop. São Paulo 38: 265-271.        [ Links ]

29. Marinho RP, Neves DP (1979) Dipylidium caninum (Dilepididae-Cestoda). Report of two human cases. Rev. Inst. Med. Trop. São Paulo 21: 266-268.        [ Links ]

30. MeCraeken RO, Lipkowitz KB, Dronen NO (1992) Efficacy of albendazole and mebendazole against Hymenolepis microstoma and Hymenolepis diminuta. Parasitol. Res. 78: 108-111.        [ Links ]

31. Mirdha BR, Samantray JC (2002) Hymenolepis nana: a common cause of paediatric diarrhoea in urban slum dwellers in India. J. Trop. Pediatr. 48: 331-334.        [ Links ]

32. Nimer E (1979) Climatologia do Brasil. Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro, Brazil. 421 pp.        [ Links ]

33. Okun DA (1988) The value of water supply and sanitation in development: an assessment. Am. J. Publ. Health 78: 1463-1467.        [ Links ]

34. Orellana JDY, Coimbra CEA, Lourenço AEP, Santos RV (2006) Nutritional status and anemia in Suruí Indian children, Brazilian Amazon. J. Pediatr. (Rio J.) 85: 383-388.        [ Links ]

35. Rivero Z, Maldonado A, Bracho A, Gotera J, Atencio R, Leal M, Sánchez R, Silva C (2007) Enteroparasitosis en indígenas de la comunidad Japrería, Estado Zulia, Venezuela. Interciencia 29: 389-395.        [ Links ]

36. Salzano FM (1990) Parasitic load in South American tribal populations. In Swedlund AC, Armelagos GJ (Eds.) Disease in Populations in Transition: Anthropological and Epidemiological Perspectives. Bergin and Garvey. New York, USA. pp. 201-221.        [ Links ]

37. Santos RV, Coimbra CEA, Ott AMT (1985) Estudos epidemiológicos entre grupos indígenas de Rondônia III: Parasitoses intestinãis nas populações dos vales dos rios Guaporé e Mamoré. Cad. Saúde Publ. 1: 467-477.        [ Links ]

38. Santos RV, Coimbra CEA, Flowers NM, Silva JP (1995) Intestinal parasitism in the Xavánte Indians, Central Brazil. Rev. Inst. Med. Trop. São Paulo 37: 145-148.        [ Links ]

39. Schwaner TD, Dixon CF (1974) Helminthiasis as a measure of cultural change in the Amazon Basin. Biotrópica 6: 32-37.        [ Links ]

40. Scolari C, Torti C, Beltrame A, Castelli F, Gulleta M, Ribas M, Morana S, Urbani C (2000) Prevalence and distribution of soil-transmitted helminth infections in urban and indigenous schoolchildren in Ortigueira, state of Paraná, Brazil: implications for control. Trop. Med. Int. Health 5: 302-307.        [ Links ]

41. Sur D, Saha DR, Manna B, Rajendran K, Bhattacharya SK (2005) Periodic deworming with albendazole and its impact on growth status and diarrhoeal incidence among children in an urban slum of India. Trans. R. Soc. Trop. Med. Hyg. 99: 261-267.        [ Links ]

42. Urbani C, Albonico M (2003) Antihelminthic drug safety and drug administration in the control of soil-transmitted helminthiasis in community campaigns. Acta Trop. 86: 215-221.        [ Links ]

43. WHO (2001) Schistosomiasis and Soil-transmitted Helminth Infections. Resolution WHA54.19. World Health Organization, Geneva, Switzerland. www.who.int/wormcontrol/about_us/en/ea54r19.pdf; (Cons. 01/15/2009).        [ Links ]

44. Zani LC, Favre TC, Pieri OS, Barbosa CS (2004) Impact of antihelminthic treatment on infection by Ascaris lumbricoides, Trichuris trichiura and hookworms in covas, a rural community of Pernanbuco, Brazil. Rev. Inst. Med. Trop. São Paulo 46: 63-71.        [ Links ]