Pulmonary manifestations in the initial phase of schistosomiasis mansoni

Rocha, Manoel Otávio C.; Rocha, Regina Lunardi; Pedroso, Ênio Roberto P.; Greco, Dirceu B.; Ferreira, Cid Sérgio; Lambertucci, José Roberto; Katz, Naftale; Rocha, Roberto S; Rezende, Dilermando F.; Neves, Jayme

doi:10.1590/S0036-46651995000400005

Abstracts

The clinical and radiological pulmonary manifestations in the initial phase of schistosomiasis mansoni were studied in thirty previously healthy individuals who were simultaneously infected. The findings were compared with those concerning a control group and related to possible pathogenetic factors. The respiratory manifestations were of light or of moderate intensity, the dry cough being the most common symptom. The significant radiological alterations were: thickening of bronchial walls and beaded micronodulation, predominantly localized in the lower pulmonary fields. It was observed significant association between wheezing and IgE levels, estimated by the area of immediate intradermal reaction, as well as between the number of blood eosinophils and the occurrence of radiological changes. Moreover, there was correlation between the worm burden and the presence of wheezing, thoracic pain and beaded micronodulation. Thus, the clinical and radiological pulmonary manifestations described are significant part of the initial phase of schistosomiasis mansoni and present the worm burden, eosinophilia and levels of IgE as probable pathogenetic factors.

Schistosomiasis mansoni; Acute schistosomiasis; Lung disease

Foram estudadas as alterações clínicas e radiológicas pulmonares da fase inicial da esquistossomose mansoni em 30 indivíduos previamente sadios, que se infectaram simultaneamente. Os achados foram comparados aos de um grupo - controle e relacionados a possíveis fatores patogenéticos como carga parasitária, eosinofilia sangüínea e área de reação intradérmica imediata, esta como estimativa de IgE ligada a mastócito. As manifestações pulmonares foram de intensidade leve ou moderada, sendo a tosse seca o sintoma mais comum. As alterações radiológicas significativas constaram de espessamento de paredes brônquicas, micronodulação em rosário e micronodulação esparsa, localizadas predominantemente nas porções inferiores dos campos pulmonares. Verificou-se associação significativa de sibilos e área da reação intradérmica imediata, bem como entre o número de eosinófilos sangüíneos e a ocorrência de alterações radiológicas tomadas em conjunto. Houve correlação entre a carga parasitária, expressa pelo número de ovos eliminados nas fezes, e a presença de sibilos, dor torácica e micronodulação em rosário.

SCHISTOSOMIASIS

Pulmonary manifestations in the initial phase of schistosomiasis mansoni

Alterações pulmonares da fase inicial da esquistossomose mansoni

Manoel Otávio C. Rocha; Regina Lunardi Rocha; Ênio Roberto P. Pedroso; Dirceu B. Greco; Cid Sérgio Ferreira; José Roberto Lambertucci; Naftale Katz; Roberto S. Rocha; Dilermando F. Rezende; Jayme Neves

Medical School, Federal University of Minas Gerais, Postgraduate Course of Tropical Medicine, René Rachou Research Center (FIOCRUZ)

^{Correspondence to} Correspondence to: Dr. Manoel Otávio C. Rocha Faculdade de Medicina da UFMG Av. Prof. Alfredo Balena 190 30130-100 Belo Horizonte, MG, Brasil

SUMMARY

The clinical and radiological pulmonary manifestations in the initial phase of schistosomiasis mansoni were studied in thirty previously healthy individuals who were simultaneously infected. The findings were compared with those concerning a control group and related to possible pathogenetic factors.

The respiratory manifestations were of light or of moderate intensity, the dry cough being the most common symptom. The significant radiological alterations were: thickening of bronchial walls and beaded micronodulation, predominantly localized in the lower pulmonary fields.

It was observed significant association between wheezing and IgE levels, estimated by the area of immediate intradermal reaction, as well as between the number of blood eosinophils and the occurrence of radiological changes. Moreover, there was correlation between the worm burden and the presence of wheezing, thoracic pain and beaded micronodulation.

Thus, the clinical and radiological pulmonary manifestations described are significant part of the initial phase of schistosomiasis mansoni and present the worm burden, eosinophilia and levels of IgE as probable pathogenetic factors.

Keywords: Schistosomiasis mansoni; Acute schistosomiasis; Lung disease, parasitic.

RESUMO

Foram estudadas as alterações clínicas e radiológicas pulmonares da fase inicial da esquistossomose mansoni em 30 indivíduos previamente sadios, que se infectaram simultaneamente. Os achados foram comparados aos de um grupo - controle e relacionados a possíveis fatores patogenéticos como carga parasitária, eosinofilia sangüínea e área de reação intradérmica imediata, esta como estimativa de IgE ligada a mastócito. As manifestações pulmonares foram de intensidade leve ou moderada, sendo a tosse seca o sintoma mais comum. As alterações radiológicas significativas constaram de espessamento de paredes brônquicas, micronodulação em rosário e micronodulação esparsa, localizadas predominantemente nas porções inferiores dos campos pulmonares.

Verificou-se associação significativa de sibilos e área da reação intradérmica imediata, bem como entre o número de eosinófilos sangüíneos e a ocorrência de alterações radiológicas tomadas em conjunto. Houve correlação entre a carga parasitária, expressa pelo número de ovos eliminados nas fezes, e a presença de sibilos, dor torácica e micronodulação em rosário.

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

Recebido para publicação em 09/01/1995

Aceito para publicação em 22/05/1995

1. ACKERMAN, S.J.; GLEICH, G.J.; LOEGERING, D.A.; RICHARDSON, B.A. & BUTTERWORTH, A.E. - Comparative loxicity of purified human eosinophil granule cationic proteins for schistosomula of Schistosoma mansoni. Amer. J. trop. Med. Hyg., 34: 735-745, 1985.
2. ARAP SIONGOK, T.K.; MAHMOUD, A.A.F.; OUMA, J.H. et al - 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.
3. BORISH, L. & JOSEPH, B.Z. - Inflammation and the allergic response. Med. Clin. N. Amer., 76: 765-787, 1992.
4. BUTTERWORTH, A.E.; WASSOM, D.L.; GLEICH, G.J.; LOEGERING, D.A. & DAVID, J.R. - Damage to schistosomula of Schistosoma mansoni induced by eosinophil major basic protein. J. Immunol., 122: 221-229, 1979.
5. CHEEVER, A.W. - A quantitative post-mortem study of schistosomiasis mansoni in man. Amer. J. trop. Med. Hyg., 17: 38-64, 1968.
6. COOK, J.A.; BAKER, S.T.; WARREN, K.S. & JORDAN, P. - A controlled study of morbidity of schistosomiasis mansoni in St. Lucian children, based on quantitative egg excretion. Amer. J. trop. Med. Hyg., 23: 625-633, 1974.
7. DÍAZ-RIVERA, R.S.; RAMOS-MORALES, F.; KOPPISCH, E. et al. - Acute Manson's schistosomiasis. Amer. J. Med., 21: 918-943, 1956.
8. DOR, P.J.; ACKERMAN, S.J. & GLEICH, G.J. - Charcot-Leyden crystal protein and eosinophil granule major basic protein in sputum of patients with respiratory diseases. Amer. Rev. resp. Dis., 130: 1072-1077, 1984.
9. ERFAN, M.; ERFAN, H.; MOUSA, A.M. & DEEB, A.A. - Chronic pulmonary schistosomiasis: a clinical and radiological study. Trans. roy. Soc. trop. Med. Hyg., 42: 477-485, 1949.
10. FERREIRA, L.F.; NAVEIRA, J.B. & SILVA, J.R. - Fase toxęmica da esquistossomose mansoni. Consideraçőes a propósito de alguns casos coletivamente contaminados em uma piscina. Rev. Inst. Med. trop. S. Paulo, 68: 714-715, 1960.
11. FILLEY, W.V.; HOLLEY, K.E.; KEPHART, G.M. & GLEICH, G.J. - Identification by immunofluorescence of eosinophil granule major basic protein in lung tissues of patients with bronchial asthma. Lancet, 3: 11-16, 1982.
12. GELFAND, M. - Pulmonary schistosomiasis in the early "Katayama" phase of the disease. J. trop. Med. Hyg., 69: 143-144, 1966.
13. GLEICH, G.J.; FRIGAS, E.; LOEGERING, D.A.; WASSON, D.L. & STEINMULLER, D. - Cytotoxic properties of the eosinophil major basic protein. J. Immunol., 123: 2925-2927, 1979.
14. GLEICH, G.J.; FRIGAS, E.; LOEGERING, D.A. & MALDONADO, J.E. - Identification of a major basic protein in guinea pig eosinophil granules. J. exp. Med., 137: 1459-1471, 1973.
15. GRECO, D.B.; PEDROSO, E.R.P.; LAMBERTUCCI, J.R. el al. - Pulmonary involvement in schistosomiasis mansoni. Mem. Inst. Oswaldo Cruz, 82: 221-227, 1987.
16. HAGAN, P.; BLUMENTHAL, U.J.; DUNN, D.; SIMPSON, A.J.G. & WILKINS, H.A. - Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature (Lond.), 349: 243-245, 1991.
17. HUSSAIN, R.; HOFSTETTER, M.; GOLDSTONE, A.; KNIGHT, W.B. & OTTESEN, E.A. - IgE responses in human schistosomiasis. I-Quantitation of specific IgE by radioimmunoassay and correlation of results with skin test and basophil histamine release. Amer. J. trop. Med. Hyg., 32: 1347-1355, 1983.
18. JARRET, E.E.E. & MILLER, H.R.P. - Production and activities of IgE in helminth infection. Progr. Allergy, 31: 178-233, 1982.
19. JONG, E.C.; MAHMOUD, A.A.F. & KLEBANOFF.S.J. - Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J. Immunol., 126: 468-471, 1981.
20. KATZ, N.; CHAVES, A. & PELLEGRINO, J. - A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev. Inst. Med. trop. S. Paulo, 14: 379-400, 1972.
21. LEHMAN Jr., J.S.; MOTT, K.E.; MORROW Jr., R.H.; MUNIZ, T.M. & BOYER, M.H. - The intensity and effects of infection with Schistosoma mansoni in a rural community in northeast Brazil. Amer. J. trop. Med. Hyg., 25: 285-294, 1976.
22. MAINZER, F. - On a latent pulmonary disease revealed by X-ray in intestinal bilharziasis (Schistosoma mansoni). Puerto Rico J. publ. Hlth., 15: 111-123, 1939.
23. NEVES, J. - Esquistossomose mansoni. Clínica da forma aguda ou toxęmica. Rio de Janeiro, Ed. Medsi, 1986.
24. NEVES, J.; TONELLI, E. & CARVALHO, S.M. - Estudo das manifestaçőes pulmonares da forma toxęmica da esquistosssomose mansoni. Rev. Inst. Med. trop. S. Paulo, 8: 22-29, 1966.
25. O'DONNELL, M.C.; ACKERMAN, S.J.; GLEICH, G.J. & THOMAS, L.L. - Activation of basophil and mast cell histamine release by eosinophil granule major basic protein. J. exp. Med., 157: 1981-1983, 1983.
26. PELLEGRINO, J. & MACEDO, D.G. - Novo criterio de leitura da reaçăo intradérmica na esquistossomose. Rev. bras. Malar., 8: 499-509, 1956.
27. RASO, P. & BOGLIOLO, L. - Patologia. In: CUNHA, A.S. Esquistossomose mansoni. Săo Paulo, Ed.USP, 1970. p.77-130.
28. ROCHA, M.O.C.; PEDROSO, E.R.P.; GRECO, D.B. et al. - Pathogenic factors of acute schistosomiasis mansoni: correlation of worm burden, IgE, blood eosinophilia and intensity of clinical manifestations. J. trop. Med. Hyg., 1995. (in press).
29. ROCHA, R.L. - Estudo da oviposiçăo, estabilidade na postura de ovos, eosinofilia sanguínea, aspectos da morbidade e suas relaçőes com a carga parasitaria e produçăo de anticorpos específicos na esquistossomose mansoni experimental murina. Belo Horizonte, 1993. (Tese de Doutoramento - Faculdade de Medicina da Universidade Federal de Minas Gerais).
30. SANTIAGO, J.M.; NEVES, J. & RATTON, J.L.A. - Evoluçăo da forma toxęmica da esquistosssomose mansoni para o cor pulmonale. Rev. Inst. Med. trop. S. Paulo, 7: 295-304, 1965.
31. WASSOM, D.L.; LOEGERING, D.A.; SOLLEY, G.O. et al. - Elevated serum levels of the eosinophil granule major basic protein in patients with cosinophilia. J. clin. Invest., 67: 651-661, 1971.
32. WELLER, P.F. - The immunobiology of eosinophils. New Engl. J. Med., 324: 1110-1118, 1991.

Correspondence to:

Dr. Manoel Otávio C. Rocha

Faculdade de Medicina da UFMG

Av. Prof. Alfredo Balena 190

30130-100 Belo Horizonte, MG, Brasil

Publication Dates

Publication in this collection
21 Sept 2006
Date of issue
Aug 1995

History

Accepted
22 May 1995
Received
09 Jan 1995

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

[1] 1. ACKERMAN, S.J.; GLEICH, G.J.; LOEGERING, D.A.; RICHARDSON, B.A. & BUTTERWORTH, A.E. - Comparative loxicity of purified human eosinophil granule cationic proteins for schistosomula of Schistosoma mansoni. Amer. J. trop. Med. Hyg., 34: 735-745, 1985.

[2] 2. ARAP SIONGOK, T.K.; MAHMOUD, A.A.F.; OUMA, J.H. et al - 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.

[3] 3. BORISH, L. & JOSEPH, B.Z. - Inflammation and the allergic response. Med. Clin. N. Amer., 76: 765-787, 1992.

[4] 4. BUTTERWORTH, A.E.; WASSOM, D.L.; GLEICH, G.J.; LOEGERING, D.A. & DAVID, J.R. - Damage to schistosomula of Schistosoma mansoni induced by eosinophil major basic protein. J. Immunol., 122: 221-229, 1979.

[5] 5. CHEEVER, A.W. - A quantitative post-mortem study of schistosomiasis mansoni in man. Amer. J. trop. Med. Hyg., 17: 38-64, 1968.

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

[7] 7. DÍAZ-RIVERA, R.S.; RAMOS-MORALES, F.; KOPPISCH, E. et al. - Acute Manson's schistosomiasis. Amer. J. Med., 21: 918-943, 1956.

[8] 8. DOR, P.J.; ACKERMAN, S.J. & GLEICH, G.J. - Charcot-Leyden crystal protein and eosinophil granule major basic protein in sputum of patients with respiratory diseases. Amer. Rev. resp. Dis., 130: 1072-1077, 1984.

[9] 9. ERFAN, M.; ERFAN, H.; MOUSA, A.M. & DEEB, A.A. - Chronic pulmonary schistosomiasis: a clinical and radiological study. Trans. roy. Soc. trop. Med. Hyg., 42: 477-485, 1949.

[10] 10. FERREIRA, L.F.; NAVEIRA, J.B. & SILVA, J.R. - Fase toxęmica da esquistossomose mansoni. Consideraçőes a propósito de alguns casos coletivamente contaminados em uma piscina. Rev. Inst. Med. trop. S. Paulo, 68: 714-715, 1960.

[11] 11. FILLEY, W.V.; HOLLEY, K.E.; KEPHART, G.M. & GLEICH, G.J. - Identification by immunofluorescence of eosinophil granule major basic protein in lung tissues of patients with bronchial asthma. Lancet, 3: 11-16, 1982.

[12] 12. GELFAND, M. - Pulmonary schistosomiasis in the early "Katayama" phase of the disease. J. trop. Med. Hyg., 69: 143-144, 1966.

[13] 13. GLEICH, G.J.; FRIGAS, E.; LOEGERING, D.A.; WASSON, D.L. & STEINMULLER, D. - Cytotoxic properties of the eosinophil major basic protein. J. Immunol., 123: 2925-2927, 1979.

[14] 14. GLEICH, G.J.; FRIGAS, E.; LOEGERING, D.A. & MALDONADO, J.E. - Identification of a major basic protein in guinea pig eosinophil granules. J. exp. Med., 137: 1459-1471, 1973.

[15] 15. GRECO, D.B.; PEDROSO, E.R.P.; LAMBERTUCCI, J.R. el al. - Pulmonary involvement in schistosomiasis mansoni. Mem. Inst. Oswaldo Cruz, 82: 221-227, 1987.

[16] 16. HAGAN, P.; BLUMENTHAL, U.J.; DUNN, D.; SIMPSON, A.J.G. & WILKINS, H.A. - Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature (Lond.), 349: 243-245, 1991.

[17] 17. HUSSAIN, R.; HOFSTETTER, M.; GOLDSTONE, A.; KNIGHT, W.B. & OTTESEN, E.A. - IgE responses in human schistosomiasis. I-Quantitation of specific IgE by radioimmunoassay and correlation of results with skin test and basophil histamine release. Amer. J. trop. Med. Hyg., 32: 1347-1355, 1983.

[18] 18. JARRET, E.E.E. & MILLER, H.R.P. - Production and activities of IgE in helminth infection. Progr. Allergy, 31: 178-233, 1982.

[19] 19. JONG, E.C.; MAHMOUD, A.A.F. & KLEBANOFF.S.J. - Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J. Immunol., 126: 468-471, 1981.

[20] 20. KATZ, N.; CHAVES, A. & PELLEGRINO, J. - A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev. Inst. Med. trop. S. Paulo, 14: 379-400, 1972.

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

[22] 22. MAINZER, F. - On a latent pulmonary disease revealed by X-ray in intestinal bilharziasis (Schistosoma mansoni). Puerto Rico J. publ. Hlth., 15: 111-123, 1939.

[23] 23. NEVES, J. - Esquistossomose mansoni. Clínica da forma aguda ou toxęmica. Rio de Janeiro, Ed. Medsi, 1986.

[24] 24. NEVES, J.; TONELLI, E. & CARVALHO, S.M. - Estudo das manifestaçőes pulmonares da forma toxęmica da esquistosssomose mansoni. Rev. Inst. Med. trop. S. Paulo, 8: 22-29, 1966.

[25] 25. O'DONNELL, M.C.; ACKERMAN, S.J.; GLEICH, G.J. & THOMAS, L.L. - Activation of basophil and mast cell histamine release by eosinophil granule major basic protein. J. exp. Med., 157: 1981-1983, 1983.

[26] 26. PELLEGRINO, J. & MACEDO, D.G. - Novo criterio de leitura da reaçăo intradérmica na esquistossomose. Rev. bras. Malar., 8: 499-509, 1956.

[27] 27. RASO, P. & BOGLIOLO, L. - Patologia. In: CUNHA, A.S. Esquistossomose mansoni. Săo Paulo, Ed.USP, 1970. p.77-130.

[28] 28. ROCHA, M.O.C.; PEDROSO, E.R.P.; GRECO, D.B. et al. - Pathogenic factors of acute schistosomiasis mansoni: correlation of worm burden, IgE, blood eosinophilia and intensity of clinical manifestations. J. trop. Med. Hyg., 1995. (in press).

[29] 29. ROCHA, R.L. - Estudo da oviposiçăo, estabilidade na postura de ovos, eosinofilia sanguínea, aspectos da morbidade e suas relaçőes com a carga parasitaria e produçăo de anticorpos específicos na esquistossomose mansoni experimental murina. Belo Horizonte, 1993. (Tese de Doutoramento - Faculdade de Medicina da Universidade Federal de Minas Gerais).

[30] 30. SANTIAGO, J.M.; NEVES, J. & RATTON, J.L.A. - Evoluçăo da forma toxęmica da esquistosssomose mansoni para o cor pulmonale. Rev. Inst. Med. trop. S. Paulo, 7: 295-304, 1965.

[31] 31. WASSOM, D.L.; LOEGERING, D.A.; SOLLEY, G.O. et al. - Elevated serum levels of the eosinophil granule major basic protein in patients with cosinophilia. J. clin. Invest., 67: 651-661, 1971.

[32] 32. WELLER, P.F. - The immunobiology of eosinophils. New Engl. J. Med., 324: 1110-1118, 1991.