Epidemiology of Schistosoma mansoni infection in a low-endemic area in Brazil: clinical and nutritional characteristics

Proietti, Fernando A.; Paulino, Urquisa H. M.; Chiari, Clea A.; Proietti, Anna B. F. C.; Antunes, Carlos M. F.

doi:10.1590/S0036-46651992000500007

Abstracts

A cross-sectional case-control study designed to evaluate the role of malnutrition in the association between the intensity of Schistosoma mansoni infection and clinical schistosomiasis, was conducted in an area with both low frequency of infection and low morbidity of schistosomiasis in Brazil. Cases (256) were patients with a positive stool examination for S. mansoni; their geometrical mean number of eggs/gram of feces was 90. Controls (256) were a random sample of the negative participants paired to the cases by age, sex and length of residence in the area. The clinical signs and symptoms found to be associated with S. mansoni infection, comparing cases and controls, were blood in stools and presence of a palpable liver. A linear trend in the relative odds of these signs and symptoms with increasing levels of infection was detected. Adjusting by the level of egg excretion, the existence of an interaction between palpable liver and ethnic group (white) was suggested. No differences in the nutritional status of infected and non-infected participants were found.

Schistosomiasis mansoni; Infection intensity; Clinical signs and symptoms; Malnutrition; Epidemiological case-control studies

Um estudo epidemiológico seccional, tipo caso-controle, planejado para avaliar o papel desempenhado pelo estado nutricional do paciente na associação entre a intensidade da infecção pelo Schistosoma mansoni e as manifestações clínicas da esquistossomose, foi conduzido em uma área do Estado de Minas Gerais que apresentava uma baixa freqüência desta parasitose e uma baixa morbidade devido a esta infecção. Casos (256) foram definidos como participantes que apresentavam exame de fezes positivo para S. mansoni, com uma média geométrica de 90 ovos/grama de fezes. Controles (256) foram definidos como uma amostra aleatória dos pacientes com exames de fezes negativo, pareados aos casos por idade, sexo e tempo de residência na área. Os sinais e sintomas clínicos assinalados como associados à infecção pelo S. mansoni, comparando-se casos e controles, foram a presença de sangue nas fezes e de fígado palpável. Foi detectada uma tendência linear nas odds relativas destes sinais e sintomas e níveis crescentes de infecção. Ajustando pelo numera de ovos de S. mansoni excretados, a existência de uma interação entre grupo étnico (brancos) e fígado palpável foi sugerida. Não foram encontradas diferenças significativas no estado nutricional dos casos e dos controles.

EPIDEMIOLOGY

Epidemiology of Schistosoma mansoni infection in a low-endemic area in Brazil: clinical and nutritional characteristics

Epidemiologia da infecção pelo Schistosoma mansoni em área de baixa endemicidade no Brasil: características clínicas e nutricionais

Fernando A. Proietti^I,III; Urquisa H. M. Paulino^I; Clea A. Chiari^II; Anna B. F. C. Proietti^IV; Carlos M. F. Antunes^II,III

^IDepartment of Clinical Medicine, School of Medicine

^IIDepartment of Parasitology, Institute for Biological Sciences

^IIIInterdepartmental Group for Epidemiological Research

^IVFederal University of Minas Gerais State and Hemominas, Minas Gerais Hospitals Foundation, Brazil

^{Address for correspondence} Address for correspondence: Dr. Carlos M. F. Antunes Departamento de Parasitologia ICB/UFMG Av. Antonio Carlos 6627 Cx. Postal 2486. 31270 - Belo Horizonte MG., Brasil

SUMMARY

A cross-sectional case-control study designed to evaluate the role of malnutrition in the association between the intensity of Schistosoma mansoni infection and clinical schistosomiasis, was conducted in an area with both low frequency of infection and low morbidity of schistosomiasis in Brazil. Cases (256) were patients with a positive stool examination for S. mansoni; their geometrical mean number of eggs/gram of feces was 90. Controls (256) were a random sample of the negative participants paired to the cases by age, sex and length of residence in the area. The clinical signs and symptoms found to be associated with S. mansoni infection, comparing cases and controls, were blood in stools and presence of a palpable liver. A linear trend in the relative odds of these signs and symptoms with increasing levels of infection was detected. Adjusting by the level of egg excretion, the existence of an interaction between palpable liver and ethnic group (white) was suggested. No differences in the nutritional status of infected and non-infected participants were found.

Key words: Schistosomiasis mansoni; Infection intensity; Clinical signs and symptoms; Malnutrition; Epidemiological case-control studies.

RESUMO

Um estudo epidemiológico seccional, tipo caso-controle, planejado para avaliar o papel desempenhado pelo estado nutricional do paciente na associação entre a intensidade da infecção pelo Schistosoma mansoni e as manifestações clínicas da esquistossomose, foi conduzido em uma área do Estado de Minas Gerais que apresentava uma baixa freqüência desta parasitose e uma baixa morbidade devido a esta infecção. Casos (256) foram definidos como participantes que apresentavam exame de fezes positivo para S. mansoni, com uma média geométrica de 90 ovos/grama de fezes. Controles (256) foram definidos como uma amostra aleatória dos pacientes com exames de fezes negativo, pareados aos casos por idade, sexo e tempo de residência na área. Os sinais e sintomas clínicos assinalados como associados à infecção pelo S. mansoni, comparando-se casos e controles, foram a presença de sangue nas fezes e de fígado palpável. Foi detectada uma tendência linear nas odds relativas destes sinais e sintomas e níveis crescentes de infecção. Ajustando pelo numera de ovos de S. mansoni excretados, a existência de uma interação entre grupo étnico (brancos) e fígado palpável foi sugerida. Não foram encontradas diferenças significativas no estado nutricional dos casos e dos controles.

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

ACKNOWLEDGEMENTS

The authors are indebted to Dr. Naftale Katz, to the staff of Ribeirão das Neves Health Center, to SUCAM-MG (Superintendência de Campanhas do Ministério da Saúde - Coordenadoria Regional de Minas Gerais) and to the staff of the Clinical Laboratory, School of Medicine, Federal University of Minas Gerais State, for their invaluable participation in this study.

Recebido para publicação em 22/1/1992

Aceito para publicação em 14/4/1992

This investigation received support from "Financiadora de Estudos e Projetos (FINEP)", from "Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)" and from the Research Strengthening Component of the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases.

1. BINA, J.C.; TAVARES-NETO, J.; PRATA, A. & AZEVEDO, E.S. - Greater resistance to development of severe schistosomiasis in Brazilian negroes. Hum. Biol., 50: 41-49, 1978.
2. BRASIL. - Consumo alimentar, antropometria. In: Estudo Nacional da Despeza Familiar. Rio de Janeiro, Fundaçăo Instituto de Geografia e Estatística, 1977.
3. BRENER, Z. & MOURĂO, O.G. - Inquéritos clínicos-epidemilógicos em focos endęmicos da esquistossomose mansoni em Minas Gerais. Rev. bras. Malar., 8: 519-526, 1956.
4. CAMPOS-FILHO, N. & FRANCO, E.L. - A microcomputer program for multiple logistic regression by unconditional and conditional maximum likelihood methods. Amer. J. Epidem., 129: 439-444, 1989.
5. CHEEVER, A.W.A. - Quantitative post-mortem study of schistosomiasis mansoni in man. Amer. J. trop. Med. Hyg., 17: 38-75, 1968.
6. CLINE, B.L.; RYMZO, W.T.; HIATT, W.B.; KNIGHT, W.B. & BERRIOS-DURAN, L.A. - Morbidity from Schistosoma mansoni in a Puerto Rican community: a population based study. Amer. J. trop. Med. Hyg., 26: 109-117, 1977.
7. COOK, J.A.; BAKER, S.T.; WARREN, K.S. & JORDAN, P.A. - A controlled study of morbidity of schistosomiasis mansoni in Santa Lucia children, based on quantitative egg excretion. Amer. J. trop. Med. Hyg., 23: 625-633, 1974.
8. COUTINHO, E.; BARBOSA, F.S.; BARBOSA, J.M.; PESSOA, D.; PINTO, R.F.; OLIVEIRA, P.A. & RODRIGUES, B.A. - Inquérito clínico-nutricional e antropométrico preliminar, em áreas endęmicas de esquistossomose mansoni, no nordeste do Brasil. Rev. Soc. bras. Med. trop., 6: 211-236, 1972.
9. DEAN, J.A.; DEAN A.G.; BURTON A. & DICKER, R. - EpiInfo Version 5. A Word Processing, Database, and Statistics System for Epidemiology on Microcomputer. Georgia, USD Inc, Stone Mountain, 1990.
10. FLEISS, J.L. - Statistical Methods for Rates and Proportions. 2. ed. New York, John Wiley and Sons, 1981. (Wiley Series in Probability and Mathematical Statistics).
11. GUIMARĂES, M.D.C.; BARROS, H.L. & KATZ, N. - A clinical epidemiological study in a schistosomiasis mansoni endemic area (Tuparece, Minas Gerais). Rev. Inst. Med. trop. S. Paulo, 27: 123-131, 1985.
12. GURNEY, J.M. & JELLIFFE, D.B. - Arm anthropometry in nutritional assessment: normogram for rapid calculation of muscle circumference and cross sectional muscle and fat areas. Amer. J. clin. Nutr., 26: 912-915, 1973.
13. HIATT, R.A. - Morbidity from Schistosoma mansoni infections: an epidemiological study based on quantitative analysis of egg excretion in two highlands Ethiopian villages. Amer. J. trop. Med. Hyg., 25: 808-817, 1976.
14. HIATT, R.A. & GEBRE-MEDHIN, M. - Morbidity from Schistosoma mansoni infections: an epidemiological study based on quantitative analysis of egg excretion in Ethiopian children. Amer. J. trop. Med. Hyg., 26: 473-481, 1977.
15. JELLIFFE, D.B. - The assessment of nutritional status of the community. Geneva, World Health Organization, 1963. (World Health Organization Monograph Series nş 53)
16. JORDAN, P. - Epidemiology and control of schistosomiasis. Brit. med. Bull., 28: 55-59, 1972.
17. KAMEL, I.A.; ELWI, A.M.; CHEEVER, A.W.; MOSIMANN, J.E. & DANNER, R. - Schistosoma mansoni and Schistosoma hematobium infections in Eqypt. IV. Hepatic lesions. Amer. J. trop. Med. Hyg., 27: 931-938, 1978.
18. KATZ, N.; MOTTA, E.; OLIVEIRA, V.B. & CARVALHO, E.F. - Prevalęncia da esquistossomose em escolares no Estado de Minas Gerais. In: CONGRESSO DA SOCIEDADE BRASILEIRA DE MEDICINA TROPICAL, 14. Joăo Pessoa, PB, 1978. Resumos. p. 102.
19. KATZ, N. & ZICKER, F. - Correlation between symptomatology and intensity of Schistosoma mansoni infection in inhabitants from endemic areas in Minas Gerais State Brazil. Bras. méd., 11: 55-59, 1975.
20. KEYS, A. - Recommendations concerning body measurement for the characterization of nutritional status. Hum. Biol., 28: 111-123, 1956.
21. KLOETZEL, K. - Splenomegaly in schistosomiasis mansoni. Amer. J. trop. Med. Hyg., 11: 472-476, 1962.
22. KRIEGER, H.; MORTON, N.E.; MI, M.P.; AZEVEDO, E.S.; FREIRE MAIA, A. & YASUDA, N. - Racial admixture in Northeastern Brazil. Ann. hum. Genet., 29: 113-125, 1965.
23. LEHMAN, J.S.; MOTT, K.E.; MORROW, R.H.; MUNIZ, T.M. & BOYER, M.H. - The intensity and effects of infection with Schistosoma mansoni in a rural community Northeast Brazil. Amer. J. trop. Med. Hyg., 25: 285-294, 1976.
24. LIMA E COSTA, M.F.F. de; LEITE, M.L.C.; ROCHA, R.S.; MAGALHĂES, M.H.A. & KATZ, N. - Anthropometric measures in relation to schistosomiasis mansoni and socioeconomic variables. Int. J. Epidem., 17: 880-886, 1988.
25. LIMA E COSTA, M.F.F. de; MAGALHĂES, M.H.A.; ROCHA, R.S.; ANTUNES, C.M.F. & KATZ, N. - Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull. Wld. Hlth. Org., 65: 57-66, 1987.
26. LIMA E COSTA, M.F.F. de; ROCHA, R.S. & KATZ, N. - Morbidade da esquistossomose e sua relaçăo com a contagem de ovos de Schistosoma mansoni em uma zona hiperendemica do Estado de Minas Gerais. Rev. Inst. Med. trop. S. Paulo, 27: 66-75, 1985.
27. LIMA E COSTA, M.F.F. de; ROCHA, R.S.; MAGALHĂES, M.H.A. & KATZ, N. - A clinico-epidemiological survey of schistosomiasis mansoni in a hyperendemic area in Minas Gerais State (Comercinho, Brazil). I. Differences in manifestations of schistosomiasis in the town center and in the environs. Trans. roy. Soc. trop. Med. Hyg., 79: 539-545, 1985.
28. McMAHON, J.E. - A study of some clinico-pathological manifestations in Schistosoma mansoni infection in Tanzania. Ann. trop. Med. Parasit., 61: 302-309, 1967.
29. MENEZES, A.P. & COURA, J.R. - Estudo seccional sobre esquistossomose mansonica no município de Riachuelo, Estado de Sergipe. Rev. Soc. bras. Med. trop., 13: 1-15. 1979/80.
30. NAKAMURA, R.M. - Immunopathology Clinical Laboratory Concepts and Methods. Boston, Little Brown and Company, 1974.
31. NIE, N.H.; HULL, C.H.; JENKINS, J.G.; STEINBRENNER, K. & BENT, D.H. - SPSS Statistical Package for the Social Sciences. 2. ed. New York, Mc Graw-Hill, 1975.
32. OMER, A.H.S.; HAMILTON, P.J.S.; MARSHALL, T.F.C. & DRAPER, C.C. - Infection with Schistosoma mansoni in the Gezira area of the Sudan. J. trop. Med. Hyg., 79: 151-157, 1976.
33. ONGON, V.L. & BRADLEY, D.J. - The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. I. Field studies of a community at Panayagoro. Trans. roy. Soc. trop. Med. Hyg., 66: 835-851, 1972.
34. PESSOA, S.B. & AMORIM, J.P. - Contribuiçăo para historia natural da esquistossomose mansonica no nordeste brasileiro e sugestőes para sua profilaxia. Rev. bras. Malar., 9: 5-18, 1957.
35. PESSOA, S.B. & COUTINHO, J.O. - Nota sobre incidencia de parasitoses intestinais em Aracaju-Sergipe, com especial referencia a esquistosomose. Rev. clín. S. Paulo, 28: 11-22, 1952.
36. PESSOA, S.B. & MARTINS, A.V. - Parasitologia Médica. 11Ş ed. Rio de Janeiro, Guanabara Koogan, 1982.
37. POPE, R.T.; KLINE, B.L. & EL ALAMY, M.A. - Evaluations of schistosomal morbidity in subjects with high intensities infections in Qalyub, Egypt. Amer. J. trop. Med. Hyg., 29: 416-425, 1980.
38. PRATA, A. - Esquistossomose mansoni. In: VERONESI, R. Doenças Infecciosas e Parasitarias. 7Ş ed. Rio de Janeiro, Guanabara Koogan S.A., 1982. Cap. 94, p.884.
39. PRATA, A. & SCHROEDER, S.A. - Comparison of whites and negroes infected with Schistosoma mansoni in a hyperendemic area. Gaz. méd. Bahia, 67: 93-98, 1967.
40. PRATA, A. & TAVARES NETO, J. - Forma hepatosplęnica da esquistossomose mansônica, em relaçăo ŕ composiçăo racial e ao nível sócio-econômico, em Catolândia, Bahia. Rev. Soc. bras. Med. trop., 23: 37-42, 1990.
41. PROIETTI, F.A. & ANTUNES, C.M.F. - Sensitivity, specificity and positive predictive value of selected clinical signs and symptoms associated with schistosomiasis mansoni. Int. J. Epidem., 18: 680-683, 1989.
42. ROTHMAN, K.J. & BOICE Jr., J.D. - Epidemiologic Analysis with a Programmable Calculator. Washington, US Department of Health, Education and Welfare, 1979. (National Institute of Health. NIH Publication nş 79-1649).
43. RUIZ, L.; COLLEY, J.R.T. & HAMILTON, P.J.S. - Measurement of triceps skinfold thickness. An investigation of sources of variation. Brit. J. prev. soc. Med., 25: 165-167, 1971.
44. SCHLESSELMAN, J.J. - Case Control Studies. Design, Conduct, Analysis. New York, Oxford University Press, 1982.
45. SIONGOK, T.K.A.; MAHAMOUD, A.A.F.; OUMA, J.H.; WARREN, K.S.; MULLER, A.S.; HANDA, A.K. & HOUSER, H.B. - Morbidity in schistosomiasis mansoni in relation to intensity of infection: study of a community in Machakos, Kenya. Amer. J. trop. Med. Hyg., 25: 273-284, 1976.
46. SMITH, D.H.; WARREN, K.S. & MAHAMOUD, A.A.F. - Morbidity in schistosomiasis mansoni in relation to intensity of infection: study of a community in Kisumu, Kenya. Amer. J. trop. Med. Hyg., 28: 220-229, 1979.
47. TANNER, J.M. - The measurement of body fat in man. Proc. Nutr. Soc., 18: 148-155, 1959.
48. WALKER, A.R.P.; WALKER, B.F. & RICHARDSON, B.D. - Studies on schistosomiasis in a South African Bantu school children population. Amer. J. trop. Med. Hyg., 19: 792-814, 1970.

Address for correspondence:

Dr. Carlos M. F. Antunes

Departamento de Parasitologia ICB/UFMG

Av. Antonio Carlos 6627

Cx. Postal 2486. 31270 - Belo Horizonte MG., Brasil

Publication Dates

Publication in this collection
13 Sept 2006
Date of issue
Oct 1992

History

Accepted
14 Apr 1992
Received
22 Jan 1992

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. BINA, J.C.; TAVARES-NETO, J.; PRATA, A. & AZEVEDO, E.S. - Greater resistance to development of severe schistosomiasis in Brazilian negroes. Hum. Biol., 50: 41-49, 1978.

[2] 2. BRASIL. - Consumo alimentar, antropometria. In: Estudo Nacional da Despeza Familiar. Rio de Janeiro, Fundaçăo Instituto de Geografia e Estatística, 1977.

[3] 3. BRENER, Z. & MOURĂO, O.G. - Inquéritos clínicos-epidemilógicos em focos endęmicos da esquistossomose mansoni em Minas Gerais. Rev. bras. Malar., 8: 519-526, 1956.

[4] 4. CAMPOS-FILHO, N. & FRANCO, E.L. - A microcomputer program for multiple logistic regression by unconditional and conditional maximum likelihood methods. Amer. J. Epidem., 129: 439-444, 1989.

[5] 5. CHEEVER, A.W.A. - Quantitative post-mortem study of schistosomiasis mansoni in man. Amer. J. trop. Med. Hyg., 17: 38-75, 1968.

[6] 6. CLINE, B.L.; RYMZO, W.T.; HIATT, W.B.; KNIGHT, W.B. & BERRIOS-DURAN, L.A. - Morbidity from Schistosoma mansoni in a Puerto Rican community: a population based study. Amer. J. trop. Med. Hyg., 26: 109-117, 1977.

[7] 7. COOK, J.A.; BAKER, S.T.; WARREN, K.S. & JORDAN, P.A. - A controlled study of morbidity of schistosomiasis mansoni in Santa Lucia children, based on quantitative egg excretion. Amer. J. trop. Med. Hyg., 23: 625-633, 1974.

[8] 8. COUTINHO, E.; BARBOSA, F.S.; BARBOSA, J.M.; PESSOA, D.; PINTO, R.F.; OLIVEIRA, P.A. & RODRIGUES, B.A. - Inquérito clínico-nutricional e antropométrico preliminar, em áreas endęmicas de esquistossomose mansoni, no nordeste do Brasil. Rev. Soc. bras. Med. trop., 6: 211-236, 1972.

[9] 9. DEAN, J.A.; DEAN A.G.; BURTON A. & DICKER, R. - EpiInfo Version 5. A Word Processing, Database, and Statistics System for Epidemiology on Microcomputer. Georgia, USD Inc, Stone Mountain, 1990.

[10] 10. FLEISS, J.L. - Statistical Methods for Rates and Proportions. 2. ed. New York, John Wiley and Sons, 1981. (Wiley Series in Probability and Mathematical Statistics).

[11] 11. GUIMARĂES, M.D.C.; BARROS, H.L. & KATZ, N. - A clinical epidemiological study in a schistosomiasis mansoni endemic area (Tuparece, Minas Gerais). Rev. Inst. Med. trop. S. Paulo, 27: 123-131, 1985.

[12] 12. GURNEY, J.M. & JELLIFFE, D.B. - Arm anthropometry in nutritional assessment: normogram for rapid calculation of muscle circumference and cross sectional muscle and fat areas. Amer. J. clin. Nutr., 26: 912-915, 1973.

[13] 13. HIATT, R.A. - Morbidity from Schistosoma mansoni infections: an epidemiological study based on quantitative analysis of egg excretion in two highlands Ethiopian villages. Amer. J. trop. Med. Hyg., 25: 808-817, 1976.

[14] 14. HIATT, R.A. & GEBRE-MEDHIN, M. - Morbidity from Schistosoma mansoni infections: an epidemiological study based on quantitative analysis of egg excretion in Ethiopian children. Amer. J. trop. Med. Hyg., 26: 473-481, 1977.

[15] 15. JELLIFFE, D.B. - The assessment of nutritional status of the community. Geneva, World Health Organization, 1963. (World Health Organization Monograph Series nş 53)

[16] 16. JORDAN, P. - Epidemiology and control of schistosomiasis. Brit. med. Bull., 28: 55-59, 1972.

[17] 17. KAMEL, I.A.; ELWI, A.M.; CHEEVER, A.W.; MOSIMANN, J.E. & DANNER, R. - Schistosoma mansoni and Schistosoma hematobium infections in Eqypt. IV. Hepatic lesions. Amer. J. trop. Med. Hyg., 27: 931-938, 1978.

[18] 18. KATZ, N.; MOTTA, E.; OLIVEIRA, V.B. & CARVALHO, E.F. - Prevalęncia da esquistossomose em escolares no Estado de Minas Gerais. In: CONGRESSO DA SOCIEDADE BRASILEIRA DE MEDICINA TROPICAL, 14. Joăo Pessoa, PB, 1978. Resumos. p. 102.

[19] 19. KATZ, N. & ZICKER, F. - Correlation between symptomatology and intensity of Schistosoma mansoni infection in inhabitants from endemic areas in Minas Gerais State Brazil. Bras. méd., 11: 55-59, 1975.

[20] 20. KEYS, A. - Recommendations concerning body measurement for the characterization of nutritional status. Hum. Biol., 28: 111-123, 1956.

[21] 21. KLOETZEL, K. - Splenomegaly in schistosomiasis mansoni. Amer. J. trop. Med. Hyg., 11: 472-476, 1962.

[22] 22. KRIEGER, H.; MORTON, N.E.; MI, M.P.; AZEVEDO, E.S.; FREIRE MAIA, A. & YASUDA, N. - Racial admixture in Northeastern Brazil. Ann. hum. Genet., 29: 113-125, 1965.

[23] 23. LEHMAN, J.S.; MOTT, K.E.; MORROW, R.H.; MUNIZ, T.M. & BOYER, M.H. - The intensity and effects of infection with Schistosoma mansoni in a rural community Northeast Brazil. Amer. J. trop. Med. Hyg., 25: 285-294, 1976.

[24] 24. LIMA E COSTA, M.F.F. de; LEITE, M.L.C.; ROCHA, R.S.; MAGALHĂES, M.H.A. & KATZ, N. - Anthropometric measures in relation to schistosomiasis mansoni and socioeconomic variables. Int. J. Epidem., 17: 880-886, 1988.

[25] 25. LIMA E COSTA, M.F.F. de; MAGALHĂES, M.H.A.; ROCHA, R.S.; ANTUNES, C.M.F. & KATZ, N. - Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull. Wld. Hlth. Org., 65: 57-66, 1987.

[26] 26. LIMA E COSTA, M.F.F. de; ROCHA, R.S. & KATZ, N. - Morbidade da esquistossomose e sua relaçăo com a contagem de ovos de Schistosoma mansoni em uma zona hiperendemica do Estado de Minas Gerais. Rev. Inst. Med. trop. S. Paulo, 27: 66-75, 1985.

[27] 27. LIMA E COSTA, M.F.F. de; ROCHA, R.S.; MAGALHĂES, M.H.A. & KATZ, N. - A clinico-epidemiological survey of schistosomiasis mansoni in a hyperendemic area in Minas Gerais State (Comercinho, Brazil). I. Differences in manifestations of schistosomiasis in the town center and in the environs. Trans. roy. Soc. trop. Med. Hyg., 79: 539-545, 1985.

[28] 28. McMAHON, J.E. - A study of some clinico-pathological manifestations in Schistosoma mansoni infection in Tanzania. Ann. trop. Med. Parasit., 61: 302-309, 1967.

[29] 29. MENEZES, A.P. & COURA, J.R. - Estudo seccional sobre esquistossomose mansonica no município de Riachuelo, Estado de Sergipe. Rev. Soc. bras. Med. trop., 13: 1-15. 1979/80.

[30] 30. NAKAMURA, R.M. - Immunopathology Clinical Laboratory Concepts and Methods. Boston, Little Brown and Company, 1974.

[31] 31. NIE, N.H.; HULL, C.H.; JENKINS, J.G.; STEINBRENNER, K. & BENT, D.H. - SPSS Statistical Package for the Social Sciences. 2. ed. New York, Mc Graw-Hill, 1975.

[32] 32. OMER, A.H.S.; HAMILTON, P.J.S.; MARSHALL, T.F.C. & DRAPER, C.C. - Infection with Schistosoma mansoni in the Gezira area of the Sudan. J. trop. Med. Hyg., 79: 151-157, 1976.

[33] 33. ONGON, V.L. & BRADLEY, D.J. - The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. I. Field studies of a community at Panayagoro. Trans. roy. Soc. trop. Med. Hyg., 66: 835-851, 1972.

[34] 34. PESSOA, S.B. & AMORIM, J.P. - Contribuiçăo para historia natural da esquistossomose mansonica no nordeste brasileiro e sugestőes para sua profilaxia. Rev. bras. Malar., 9: 5-18, 1957.

[35] 35. PESSOA, S.B. & COUTINHO, J.O. - Nota sobre incidencia de parasitoses intestinais em Aracaju-Sergipe, com especial referencia a esquistosomose. Rev. clín. S. Paulo, 28: 11-22, 1952.

[36] 36. PESSOA, S.B. & MARTINS, A.V. - Parasitologia Médica. 11Ş ed. Rio de Janeiro, Guanabara Koogan, 1982.

[37] 37. POPE, R.T.; KLINE, B.L. & EL ALAMY, M.A. - Evaluations of schistosomal morbidity in subjects with high intensities infections in Qalyub, Egypt. Amer. J. trop. Med. Hyg., 29: 416-425, 1980.

[38] 38. PRATA, A. - Esquistossomose mansoni. In: VERONESI, R. Doenças Infecciosas e Parasitarias. 7Ş ed. Rio de Janeiro, Guanabara Koogan S.A., 1982. Cap. 94, p.884.

[39] 39. PRATA, A. & SCHROEDER, S.A. - Comparison of whites and negroes infected with Schistosoma mansoni in a hyperendemic area. Gaz. méd. Bahia, 67: 93-98, 1967.

[40] 40. PRATA, A. & TAVARES NETO, J. - Forma hepatosplęnica da esquistossomose mansônica, em relaçăo ŕ composiçăo racial e ao nível sócio-econômico, em Catolândia, Bahia. Rev. Soc. bras. Med. trop., 23: 37-42, 1990.

[41] 41. PROIETTI, F.A. & ANTUNES, C.M.F. - Sensitivity, specificity and positive predictive value of selected clinical signs and symptoms associated with schistosomiasis mansoni. Int. J. Epidem., 18: 680-683, 1989.

[42] 42. ROTHMAN, K.J. & BOICE Jr., J.D. - Epidemiologic Analysis with a Programmable Calculator. Washington, US Department of Health, Education and Welfare, 1979. (National Institute of Health. NIH Publication nş 79-1649).

[43] 43. RUIZ, L.; COLLEY, J.R.T. & HAMILTON, P.J.S. - Measurement of triceps skinfold thickness. An investigation of sources of variation. Brit. J. prev. soc. Med., 25: 165-167, 1971.

[44] 44. SCHLESSELMAN, J.J. - Case Control Studies. Design, Conduct, Analysis. New York, Oxford University Press, 1982.

[45] 45. SIONGOK, T.K.A.; MAHAMOUD, A.A.F.; OUMA, J.H.; WARREN, K.S.; MULLER, A.S.; HANDA, A.K. & HOUSER, H.B. - Morbidity in schistosomiasis mansoni in relation to intensity of infection: study of a community in Machakos, Kenya. Amer. J. trop. Med. Hyg., 25: 273-284, 1976.

[46] 46. SMITH, D.H.; WARREN, K.S. & MAHAMOUD, A.A.F. - Morbidity in schistosomiasis mansoni in relation to intensity of infection: study of a community in Kisumu, Kenya. Amer. J. trop. Med. Hyg., 28: 220-229, 1979.

[47] 47. TANNER, J.M. - The measurement of body fat in man. Proc. Nutr. Soc., 18: 148-155, 1959.

[48] 48. WALKER, A.R.P.; WALKER, B.F. & RICHARDSON, B.D. - Studies on schistosomiasis in a South African Bantu school children population. Amer. J. trop. Med. Hyg., 19: 792-814, 1970.

Brasil