Pathology of periportal fibrosis involution in human schistosomiasis

Andrade, Zilton A.; Peixoto, Ediriomar

doi:10.1590/S0036-46651992000400001

Abstracts

Optical and electron microscopical evidences of focal matrix degradation were frequently seen in liver sections of periportal fibrosis caused by schistosomiasis mansoni in man. The material came from 14 wedge hepatic biopsies taken from patients with chronic advanced hepatosplenic disease and undergoing operations for the relief of portal hypertension. Besides the presence of focal areas of rarefaction, fragmentation and dispersion of collagen fibers, the enlarged portal spaces also showed hyperplasia of elastic tissue and disarray of smooth muscle fibers following destruction of portal vein branches. Eggs were scanty in the tissue sections, and matrix degradation probably represented involuting changes related to the progressive diminution of parasite-related aggression, which occurs spontaneously with age or after cure by chemotherapy. The changes indicative of matrix degradation now described are probably the basic morphological counterpart of periportal fibrosis involution currently being documented by ultrasonography in hepatosplenic patients submitted to curative chemotherapy.

Matrix degradation; Fibrosis; Schistosomiasis; Collagen; Chemotherapy

Um estudo feito com microscopia ótica e eletrônica permitiu verificar sinais de degradação da matriz extracelular na fibrose periportal humana causada pela esquistossomose avançada. O material de estudo proveio de 14 biópsias hepáticas em cunha feitas em portadores de esquistossomose hepato-esplênica, no momento em que eles foram submetidos a cirurgia para o alívio das manifestações de hipertensão porta. Além da presença de áreas focais de rarefação, fragmentação e dispersão dos feixes colgenos, os espaços porta alargados e fibrosados também mostraram hiperplasia do tecido elástico e dissociação de fibras musculares lisas em seguida à destruição de ramos da veia porta. Os ovos do parasito eram escassos nas secções histológicas. A degradação da matriz provavelmente representa processo involutivo relacionado com a progressiva diminuição da agressão parasitária, o que pode ocorrer espontaneamente em casos de longa duração ou após a cura pela quimioterapia. As alterações indicativas de degradação da matriz aqui descritas representam provavelmente a face morfológica da involução da fibrose periportal que vem sendo atualmente documentada pela ultrasonografia em pacientes hepato-esplênicos submetidos à quimioterapia curativa.

ORIGINAL ARTICLES

Pathology of periportal fibrosis involution in human schistosomiasis

Patologia da involução da fibrose periportal na esquistossomose humana

Zilton A. Andrade^I; Ediriomar Peixoto^II

^IResearcher. Centro de Pesquisas Gonçalo Moniz (FIOCRUZ). Rua Valdemar Falcão, 121, 41.495 Salvador, Bahia, Brazil

^IISurgeon. Hospital Central Roberto Santos, Salvador, BA, Brazil

^{Address for correspondence} Address for correspondence: Zilton A. Andrade M.D. Centro de Pesquisas Gonçalo Moniz (FIOCRUZ) Rua Valdemar Falcão, 121 (Brotas) 41.495 Salvador, Bahia - BRAZIL Telephone: (55.71) 359.4320 Fax: (55.71) 359.4292

SUMMARY

Optical and electron microscopical evidences of focal matrix degradation were frequently seen in liver sections of periportal fibrosis caused by schistosomiasis mansoni in man. The material came from 14 wedge hepatic biopsies taken from patients with chronic advanced hepatosplenic disease and undergoing operations for the relief of portal hypertension. Besides the presence of focal areas of rarefaction, fragmentation and dispersion of collagen fibers, the enlarged portal spaces also showed hyperplasia of elastic tissue and disarray of smooth muscle fibers following destruction of portal vein branches.

Eggs were scanty in the tissue sections, and matrix degradation probably represented involuting changes related to the progressive diminution of parasite-related aggression, which occurs spontaneously with age or after cure by chemotherapy. The changes indicative of matrix degradation now described are probably the basic morphological counterpart of periportal fibrosis involution currently being documented by ultrasonography in hepatosplenic patients submitted to curative chemotherapy.

Keywords: Matrix degradation; Fibrosis, Schistosomiasis; Collagen; Chemotherapy.

RESUMO

Um estudo feito com microscopia ótica e eletrônica permitiu verificar sinais de degradação da matriz extracelular na fibrose periportal humana causada pela esquistossomose avançada. O material de estudo proveio de 14 biópsias hepáticas em cunha feitas em portadores de esquistossomose hepato-esplênica, no momento em que eles foram submetidos a cirurgia para o alívio das manifestações de hipertensão porta. Além da presença de áreas focais de rarefação, fragmentação e dispersão dos feixes colgenos, os espaços porta alargados e fibrosados também mostraram hiperplasia do tecido elástico e dissociação de fibras musculares lisas em seguida à destruição de ramos da veia porta. Os ovos do parasito eram escassos nas secções histológicas. A degradação da matriz provavelmente representa processo involutivo relacionado com a progressiva diminuição da agressão parasitária, o que pode ocorrer espontaneamente em casos de longa duração ou após a cura pela quimioterapia. As alterações indicativas de degradação da matriz aqui descritas representam provavelmente a face morfológica da involução da fibrose periportal que vem sendo atualmente documentada pela ultrasonografia em pacientes hepato-esplênicos submetidos à quimioterapia curativa.

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ACKNOWLEDGEMENT

Thanks are due to Dr. Jean-Alexis Grimaud and Mme. Sylviane Guerret (Institute Pasteur, Lyon, France) for making possible the immunofluorescent studies.

Recebido para publicação em 12/12/1991

Aceito para publicação em 28/05/1992

1. ANDRADE, Z.A. - Pathogenesis of pipe-stem fibrosis of the liver. (Experimental observations on murine schistosomiasis). Mem. Inst. Oswaldo Cruz, 82: 325-334, 1987.
2. ANDRADE, Z.A. & BINA, J.C. - The changing pattern of pathology due to Schistosoma mansoni infection. Mem. Inst. Oswaldo Cruz, 80: 363-366, 1985.
3. ANDRADE, Z.A. & GRIMAUD, J.A. - Evolution of schistosomal hepatic lesions in mice after curative chemotherapy. Amer. J. Path., 124: 59-65, 1986.
4. ANDRADE, Z.A. & GRIMAUD, J.A. - Morphology of chronic collagen resorption. A study on the late stages of schistosomal granuloma involution. Amer. J. Path. 132: 389-399, 1988.
5. BENNETT, J.L. & DEPENBUSCH, J.W. - The chemotherapy of schistosomiasis. In: MANSFIELD, J.M., ed. Parasitic Diseases. New York, Marcel Deker, 1984. v.2 p. 73-131.
6. BIEMPICA, L.; TAKAHASHI, S.; BIEMPICA, S. & KOBAYASHI, M. - Imniunohistochemical localization of collagenase in hepatic murine schistosomiasis. J. Histochem. Cytochem., 31: 488-494, 1983.
7. BINA, J.C. & PRATA, A. - Regressăo da hepatosplenomegalia pelo tratamento específico da esquistossomose. Rev. Soc. bras. Med. trop. 16: 213-218, 1983.
8. CAMERON, G.R. & GANGULY, N.C. - An experimental study of the pathogenesis and reversibility of schistosoinal hepatic fibrosis. J. Path. Bact., 87: 217-237, 1964.
9. COUTINHO, A. - Editorial. A new dynamic approach to the diagnosis of Symmers' fibrosis in schistosomiasis by ultrasound. Rev. Inst. Med. trop. S. Paulo, 32: 73-77, 1990.
10. COUTINHO, A.D.; DOMINGUES, A.L.C.; FLORENCIO, J.N. & ALMEIDA, S.T. - Tratamento da esquistossomose mansônica hepatesplenica com praziquantel. Rev. Inst. Med. trop. S. Paulo, 26: 38-50, 1984.
11. CZAJA, M.J.; WEINER, F.R.; FLANDERS, K.C.; GIAMBRONE, M.A.; WIND, R.; BIEMPICA, L. & ZERN, M.A. - In vitro and in vivo association of transforming growth factor - B1 with hepatic fibrosis. J. cell Biol., 108: 2477-2482, 1989.
12. DAVIDSON, J.M. - Elastin. Structure and biology. In: UITTO, J. & PEREJDA, A.J. ed. Connective tissue disease. Molecular pathology of the extracellular matrix. New York, Marcel Dekker, 1987. p.29-53.
13. DIETZE, R.S. & PRATA. A. - Rate of reversion of hepatosplenic schistosomiasis after specific chemotherapy. Rev. Soc. bras. Med. trop., 19: 69-73, 1986.
14. DUNN, M.A.; ROJKIND, M.; WARREN, K.S.; HAIT, P.K.; RIFAS, L, & SEIFTER, S. - Liver collagen synthesis in murine schistosomiasis. J. clin. Invest., 59: 666-674, 1977.
15. EMONARD, H. & GRIMAUD, J.A. - Active and latent collagenase activity during reversal of hepatic fibrosis in murine schistosomiasis. Hepatology, 10: 77-83, 1989.
16. GRIMAUD, J.A. & BOROJEVIC, R. - Myofibroblasts in hepatic schistosomal fibrosis. Experiencia, 33: 890-892, 1977.
17. HOMEIDA, M.A.; FENWICK, A.; DeFALLA, A.A.; SULLIMAN, S.; KARDMANN, M.W.; El TOM, I.; NASH, T. & BENNETT, J.L. - Effect of anti-schistosomal chemotherapy on prevalence of Symmers' periportal fibrosis in Sudanese villages. Lancet, 11: 437-439, 1988.
18. HOMEIDA, M.; AHMED, S.; DAFALLA, A.; SULLIMAN, S.; El TOM, I.; NASH, T. & BENNETT, J.L. - Morbidity associated with Schistosoma mansoni infection as determined by ultrasound: a study in Gezira, Sudan. Amer. J. trop. Med. Hyg., 39: 196-201, 1988.
19. KATZ, N. & BRENER, Z. - Evoluçăo clínica de 112 casos de esquistossomose mansoni observados após dez anos de permanęncia em focos endęmicos de Minas Gerais. Rev. Inst. Med. trop. S. Paulo, 8: 138-142, 1966.
20. KOVACS, E.J. - Fibrogenic cytokines: the role of immune mediators in the development of scar tissue. Immunol. today, 12: 17-23, 1991.
21. LETHIAS, C.; HARTMAN, D.J.; MASMEJEAN, M.; RAVAZZOLA, M.; SABBAGH, I.; VILLE, G; HERBAGE, D. & ELOY, R. - Ultrastructural immunolocalization of elastic fibers in rat blood vessels using the protein A-gold technique. J. Histochem. Cytochem., 35: 15-21, 1987.
22. MAHOMED-ALI, Q.; DOEHRING-SCHWERDTFEGER, E.; ABDEL-RAHIM, I.M.; SCHLAKE, J.; KARDOFF, R.; FRANKE, D.; KAISER, C.; ELSHEIKH, M.; ABDALLA, M.; SCHAFER, P. & EHRICH, J.H.H. - Ultrasonographical investigation of periportal fibrosis in children with Schistosoma mansoni infection: reversibility of morbidity seven months after treatment with praziquantel. Amer. J. trop. Med. Hyg., 44: 444-451, 1991.
23. OGAWA, K.; SUZUKI, J.; MUKAI, H. & MORI, M. - Sequential change of extracellular matrix and proliferation of Ito cells with enhanced expression of desmin and actin in focal hepatic injury. Amer. J. Path., 125: 611-619, 1986.
24. PEREZ-TAMAYO, R. - Some aspects of connective tissue of the liver. In: POPPER, H. & SCHAFFNER, F. Progress in liver disease. London, Churchill & Livingstone, 1965. p. 192-210.
25. ROJKIND, M. - Editorial. From regeneration to scar formation. The collagen way. Lab. Invest., 64: 131-134, 1991.
26. TANAKA, Y.; KIM, M. & LIEBER, C.S. - Immunohistochemical detection of proliferating lipocytes in regenerating rat liver. J. Path., 160: 129-134, 1990.
27. WARREN, K.S. - The influence of treatment on the development and course of murine hepato-splenic schistosomiasis mansoni. Trans. roy. Soc. trop. Med. Hyg., 56: 510-519, 1962.
28. WARREN, K.S. & KLEIN, L. - Chronic murine hepatosplenic schistosomiasis mansoni: relative irreversibility after treatment. Trans. roy. Soc. trop. Med. Hyg., 63: 333-337, 1969.
29. WYLER, D.J.; PRAKASHI, S. & LIBBY, P. - Mesenchymal target cell specificity of egg granuloma-derived fibroblast growth factor in schistosomiasis. J. infect. Dis., 155: 728-736, 1987.

Address for correspondence:

Zilton A. Andrade

M.D. Centro de Pesquisas Gonçalo Moniz (FIOCRUZ)

Rua Valdemar Falcão, 121 (Brotas)

41.495 Salvador, Bahia - BRAZIL

Telephone: (55.71) 359.4320 Fax: (55.71) 359.4292

Publication Dates

Publication in this collection
12 Sept 2006
Date of issue
Aug 1992

History

Accepted
28 May 1992
Received
12 Dec 1991

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

[1] 1. ANDRADE, Z.A. - Pathogenesis of pipe-stem fibrosis of the liver. (Experimental observations on murine schistosomiasis). Mem. Inst. Oswaldo Cruz, 82: 325-334, 1987.

[2] 2. ANDRADE, Z.A. & BINA, J.C. - The changing pattern of pathology due to Schistosoma mansoni infection. Mem. Inst. Oswaldo Cruz, 80: 363-366, 1985.

[3] 3. ANDRADE, Z.A. & GRIMAUD, J.A. - Evolution of schistosomal hepatic lesions in mice after curative chemotherapy. Amer. J. Path., 124: 59-65, 1986.

[4] 4. ANDRADE, Z.A. & GRIMAUD, J.A. - Morphology of chronic collagen resorption. A study on the late stages of schistosomal granuloma involution. Amer. J. Path. 132: 389-399, 1988.

[5] 5. BENNETT, J.L. & DEPENBUSCH, J.W. - The chemotherapy of schistosomiasis. In: MANSFIELD, J.M., ed. Parasitic Diseases. New York, Marcel Deker, 1984. v.2 p. 73-131.

[6] 6. BIEMPICA, L.; TAKAHASHI, S.; BIEMPICA, S. & KOBAYASHI, M. - Imniunohistochemical localization of collagenase in hepatic murine schistosomiasis. J. Histochem. Cytochem., 31: 488-494, 1983.

[7] 7. BINA, J.C. & PRATA, A. - Regressăo da hepatosplenomegalia pelo tratamento específico da esquistossomose. Rev. Soc. bras. Med. trop. 16: 213-218, 1983.

[8] 8. CAMERON, G.R. & GANGULY, N.C. - An experimental study of the pathogenesis and reversibility of schistosoinal hepatic fibrosis. J. Path. Bact., 87: 217-237, 1964.

[9] 9. COUTINHO, A. - Editorial. A new dynamic approach to the diagnosis of Symmers' fibrosis in schistosomiasis by ultrasound. Rev. Inst. Med. trop. S. Paulo, 32: 73-77, 1990.

[10] 10. COUTINHO, A.D.; DOMINGUES, A.L.C.; FLORENCIO, J.N. & ALMEIDA, S.T. - Tratamento da esquistossomose mansônica hepatesplenica com praziquantel. Rev. Inst. Med. trop. S. Paulo, 26: 38-50, 1984.

[11] 11. CZAJA, M.J.; WEINER, F.R.; FLANDERS, K.C.; GIAMBRONE, M.A.; WIND, R.; BIEMPICA, L. & ZERN, M.A. - In vitro and in vivo association of transforming growth factor - B1 with hepatic fibrosis. J. cell Biol., 108: 2477-2482, 1989.

[12] 12. DAVIDSON, J.M. - Elastin. Structure and biology. In: UITTO, J. & PEREJDA, A.J. ed. Connective tissue disease. Molecular pathology of the extracellular matrix. New York, Marcel Dekker, 1987. p.29-53.

[13] 13. DIETZE, R.S. & PRATA. A. - Rate of reversion of hepatosplenic schistosomiasis after specific chemotherapy. Rev. Soc. bras. Med. trop., 19: 69-73, 1986.

[14] 14. DUNN, M.A.; ROJKIND, M.; WARREN, K.S.; HAIT, P.K.; RIFAS, L, & SEIFTER, S. - Liver collagen synthesis in murine schistosomiasis. J. clin. Invest., 59: 666-674, 1977.

[15] 15. EMONARD, H. & GRIMAUD, J.A. - Active and latent collagenase activity during reversal of hepatic fibrosis in murine schistosomiasis. Hepatology, 10: 77-83, 1989.

[16] 16. GRIMAUD, J.A. & BOROJEVIC, R. - Myofibroblasts in hepatic schistosomal fibrosis. Experiencia, 33: 890-892, 1977.

[17] 17. HOMEIDA, M.A.; FENWICK, A.; DeFALLA, A.A.; SULLIMAN, S.; KARDMANN, M.W.; El TOM, I.; NASH, T. & BENNETT, J.L. - Effect of anti-schistosomal chemotherapy on prevalence of Symmers' periportal fibrosis in Sudanese villages. Lancet, 11: 437-439, 1988.

[18] 18. HOMEIDA, M.; AHMED, S.; DAFALLA, A.; SULLIMAN, S.; El TOM, I.; NASH, T. & BENNETT, J.L. - Morbidity associated with Schistosoma mansoni infection as determined by ultrasound: a study in Gezira, Sudan. Amer. J. trop. Med. Hyg., 39: 196-201, 1988.

[19] 19. KATZ, N. & BRENER, Z. - Evoluçăo clínica de 112 casos de esquistossomose mansoni observados após dez anos de permanęncia em focos endęmicos de Minas Gerais. Rev. Inst. Med. trop. S. Paulo, 8: 138-142, 1966.

[20] 20. KOVACS, E.J. - Fibrogenic cytokines: the role of immune mediators in the development of scar tissue. Immunol. today, 12: 17-23, 1991.

[21] 21. LETHIAS, C.; HARTMAN, D.J.; MASMEJEAN, M.; RAVAZZOLA, M.; SABBAGH, I.; VILLE, G; HERBAGE, D. & ELOY, R. - Ultrastructural immunolocalization of elastic fibers in rat blood vessels using the protein A-gold technique. J. Histochem. Cytochem., 35: 15-21, 1987.

[22] 22. MAHOMED-ALI, Q.; DOEHRING-SCHWERDTFEGER, E.; ABDEL-RAHIM, I.M.; SCHLAKE, J.; KARDOFF, R.; FRANKE, D.; KAISER, C.; ELSHEIKH, M.; ABDALLA, M.; SCHAFER, P. & EHRICH, J.H.H. - Ultrasonographical investigation of periportal fibrosis in children with Schistosoma mansoni infection: reversibility of morbidity seven months after treatment with praziquantel. Amer. J. trop. Med. Hyg., 44: 444-451, 1991.

[23] 23. OGAWA, K.; SUZUKI, J.; MUKAI, H. & MORI, M. - Sequential change of extracellular matrix and proliferation of Ito cells with enhanced expression of desmin and actin in focal hepatic injury. Amer. J. Path., 125: 611-619, 1986.

[24] 24. PEREZ-TAMAYO, R. - Some aspects of connective tissue of the liver. In: POPPER, H. & SCHAFFNER, F. Progress in liver disease. London, Churchill & Livingstone, 1965. p. 192-210.

[25] 25. ROJKIND, M. - Editorial. From regeneration to scar formation. The collagen way. Lab. Invest., 64: 131-134, 1991.

[26] 26. TANAKA, Y.; KIM, M. & LIEBER, C.S. - Immunohistochemical detection of proliferating lipocytes in regenerating rat liver. J. Path., 160: 129-134, 1990.

[27] 27. WARREN, K.S. - The influence of treatment on the development and course of murine hepato-splenic schistosomiasis mansoni. Trans. roy. Soc. trop. Med. Hyg., 56: 510-519, 1962.

[28] 28. WARREN, K.S. & KLEIN, L. - Chronic murine hepatosplenic schistosomiasis mansoni: relative irreversibility after treatment. Trans. roy. Soc. trop. Med. Hyg., 63: 333-337, 1969.

[29] 29. WYLER, D.J.; PRAKASHI, S. & LIBBY, P. - Mesenchymal target cell specificity of egg granuloma-derived fibroblast growth factor in schistosomiasis. J. infect. Dis., 155: 728-736, 1987.

Brasil

Brasil

Pathology of periportal fibrosis involution in human schistosomiasis

Patologia da involução da fibrose periportal na esquistossomose humana

Abstracts

Address for correspondence:

Publication Dates

History