Experimental pulmonary schistosomiasis: lack of morphological evidence of modulation in schistosomal pulmonary granulomas

Souza Vidal, Maura R. F.; Barbosa Jr., Aryon A.; Andrade, Zilton A.

doi:10.1590/S0036-46651993000500007

Abstracts

Numerous pulmonary schistosome egg granulomas were present in mice submitted to partial portal vein ligation (Warren's model). The granulomas were characterized by cellular aggregations formed within alveolar tissue. Main cellular types were macrophages (epithelioid cells), eosinophils, plasma cells and lymphocytes. These cells were supported by scanty fibrous stroma and exhibited close membrane contact points amongst themselves, but without forming specialized adhesion apparatus. When granulomas involved arterial structures, proliferation of cndothelial and smooth muscle cells occurred and fibrosis associated with angiogenesis became more evident. Granulomas formed around mature eggs in the pulmonary alveolar tissue presented approximately the same size and morphology regardless of the time of infection, the latter being 10, 18 and 25 weeks after cercarial exposure. This persistence of morphological appearance suggests that pulmonary granulomas do not undergo immunological modulation, as is the case with the granulomas in the liver and, to a lesser extent, in the intestines. Probably, besides general immunological factors, local (stromal) factors play an important role in schistosomal granuloma modulation.

Experimental schistosomiasis; Pulmonary schistosomiasis; Periovular granuloma; Immunological modulation

Em camundongos submetidos à ligadura parcial da veia porta e infecção pelo Schistosoma mansoni, os granulomas periovulares apareceram em grande número nos pulmões, comprovando a validade do modelo de Warren. Histologicamente os granulomas eram representados por agregados celulares compactos no seio de escasso estroma. Os macrófagos (células epitelióides) e eosinófilos eram os elementos celulares predominantes, vindo em seguida os linfóticos e plasmócitos. Ultraestruturalmenle, as células do granuloma exibiam íntimo contacto de suas membranas, com varios pontos de adesão, mas sem formar estruturas juncionais mais específicas. Os granulomas formados em torno a ovos maduros tinham tamanho, forma e composição celular similares após 10, 18 ou 25 semanas de infecção. Este aspecto contrastava com o que aparecia nos granulomas hepáticos os quais exibiam a clássica modulação. Os granulomas que envolviam as paredes arteriolares exibiam proliferação muscular, endotelial, com formação de novas vias vasculares e fibrose. As diferenças morfológicas observadas nos granulomas formados em diferentes locais e órgãos apontam para a importância de se considerar fatores locais (estromais) no determinismo dos padrões das respostas inflamatórias.

ORIGINAL ARTICLES

Experimental pulmonary schistosomiasis:^* * This paper is an abridged version of a Thesis for the Master's degree in Pathology presented to the Federal University of Bahia by Maura Raquel Ferreira Souza Vidal. lack of morphological evidence of modulation in schistosomal pulmonary granulomas

Esquistossomose pulmonar experimental: falta de evidência morfológica de modulação nos granulomas esquistosomóticos pulmonares

Maura R. F. Souza Vidal; Aryon A. Barbosa Jr.; Zilton A. Andrade

Centro de Pesquisas Gonçalo Moniz (FIOCRUZ). Rua Valdemar Falcão, 121, 40.295-001 Salvador, Bahia - Brazil

^{Address for correspondence} Address for correspondence: Zilton A. Andrade,. M.D. Centro de Pesquisas Gonçalo Moniz (FIOCRUZ) Rua Valdemar Falcão, 121 40.295-001 Salvador, Bahia - Brazil Telephone: (55.71) 359-4320; Fax: (55.71)359-4292

SUMMARY

Numerous pulmonary schistosome egg granulomas were present in mice submitted to partial portal vein ligation (Warren's model). The granulomas were characterized by cellular aggregations formed within alveolar tissue. Main cellular types were macrophages (epithelioid cells), eosinophils, plasma cells and lymphocytes. These cells were supported by scanty fibrous stroma and exhibited close membrane contact points amongst themselves, but without forming specialized adhesion apparatus. When granulomas involved arterial structures, proliferation of cndothelial and smooth muscle cells occurred and fibrosis associated with angiogenesis became more evident.

Granulomas formed around mature eggs in the pulmonary alveolar tissue presented approximately the same size and morphology regardless of the time of infection, the latter being 10, 18 and 25 weeks after cercarial exposure. This persistence of morphological appearance suggests that pulmonary granulomas do not undergo immunological modulation, as is the case with the granulomas in the liver and, to a lesser extent, in the intestines. Probably, besides general immunological factors, local (stromal) factors play an important role in schistosomal granuloma modulation.

Key words: Experimental schistosomiasis; Pulmonary schistosomiasis; Periovular granuloma; Immunological modulation.

RESUMO

Em camundongos submetidos à ligadura parcial da veia porta e infecção pelo Schistosoma mansoni, os granulomas periovulares apareceram em grande número nos pulmões, comprovando a validade do modelo de Warren. Histologicamente os granulomas eram representados por agregados celulares compactos no seio de escasso estroma. Os macrófagos (células epitelióides) e eosinófilos eram os elementos celulares predominantes, vindo em seguida os linfóticos e plasmócitos. Ultraestruturalmenle, as células do granuloma exibiam íntimo contacto de suas membranas, com varios pontos de adesão, mas sem formar estruturas juncionais mais específicas. Os granulomas formados em torno a ovos maduros tinham tamanho, forma e composição celular similares após 10, 18 ou 25 semanas de infecção. Este aspecto contrastava com o que aparecia nos granulomas hepáticos os quais exibiam a clássica modulação. Os granulomas que envolviam as paredes arteriolares exibiam proliferação muscular, endotelial, com formação de novas vias vasculares e fibrose.

As diferenças morfológicas observadas nos granulomas formados em diferentes locais e órgãos apontam para a importância de se considerar fatores locais (estromais) no determinismo dos padrões das respostas inflamatórias.

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

ACKNOWLEDGEMENT

We thank Dr. Eilson Goes Oliveira for his invaluable assistance with the statistical analysis.

Recebido para publicação em 14/04/1993.

Aceito para publicação em 29/06/1993.

1. ALMEIDA, M.A.C. & ANDRADE, Z.A. - Effect of chemotherapy on experimental pulmonary schistosomiasis. Amer. J. trop. Med. Hyg., 32: 1049-1054, 1983.
2. ANDRADE, Z.A. & ANDRADE, S.G. - Pathogenesis of schistosomal pulmonary arteritis. Amer. J. trop. Med. Hyg., 19: 305-310, 1970.
3. ANDRADE, Z.A. & WARREN, K.S. - Mild prolonged schistosomiasis in mice: alterations in host response with time and the development of portal fibrosis. Trans. roy. Soc. trop. Med. Hyg., 58: 53-57, 1964.
4. BOROS, D.L.; PELLEY, R.P. & WARREN, K.S. - Spontaneous modulation of granulomatous hypersensitivity in schistosomiasis mansoni. J. Immunol., 114: 1437-1441, 1975.
5. CHAVES, E. - The pathology of the arterial pulmonary vasculature in Manson's schistosomiasis. Dis. Chest, 50: 72-77, 1966.
6. CHEEVER, A.W. - A comparative study of Schistosoma mansoni infections in mice, gerbils, multimmamate rats, and hamsters. Amer. J. trop. Med. Hyg., 145: 227-238, 1965.
7. CHEEVER, A.W. & WARREN, K.S. - Portal vein ligation in mice: portal hypertension, collateral circulation, and blood flow. J. appl. Physiol., 18: 405-407, 1963.
8. COLLEY, D.G.; LEWIS, F.A. & TODD, C.W. - Adoptive suppression of granuloma formation by T lymphocytes and by lymphoid cells sensitive to cyclophosphamide. Cell. Immunol., 46: 192-200, 1979.
9. COLLEY, D.G.; PARRA, J.C.; MONTESANO, M.A.; LIMA, M.; NASCIMENTO, E.; DOUGHTY, B.L.; GOES, A. & GAZZINELLE, G. - Immunoregulation in human schistosomiasis by idiotypic interactions and lymphokine-mediate mechanisms. Mem. Inst. Oswaldo Cruz, 82: 105-107, 1987.
10. DUVALL, R.H. & DeWITT, W.B. - An improved perfusion technique for recovering adult schistosome from laboratory animals. Amer. J. trop. Med. Hyg., 16: 483-486, 1967.
11. GALLATIN, W.M.; WEISSMAN, T.L. & BUTCHER, E.C. - A cell surface molecule involved in organ-specific homing of lymphocytes. Nature, 304: 30, 1983.
12. IRUSTRA, V.R.C. - Contribuiçăo ao estudo da patologia pulmonar esquistossomótica experimental. Rev. Pal. trop. 71: 203-242, 1978.
13. PHILLIPS, S.M. & LAMMIE, P.J. - Immunopathology of granuloma formation and fibrosis in schistosomiasis. Parasit. today, 2: 296-302, 1986.
14. PIERCE, E.J.; CASPAR, P.; GRZYCH, J-M; LEWIS, F.A. & SHER, A. - Downregulation of Thl cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. exp. Med., 173: 159-166, 1991.
15. PRATA, A. - Biópsia retal na esquistossomose mansoni: bases e aplicaçőes no diagnóstico e tratamento. Rio de Janeiro, Publicaçăo do Serviço de Educaçăo Sanitária, 1957.
16. SADIGURSKY, M. & ANDRADE, Z.A. - Pulmonary changes in schistosomal cor pulmonale. Amer. J. trop. Med. Hyg., 31: 779-784, 1982.
17. SANTOS, R.O.; BARBOSA Jr., A.A. & ANDRADE, Z.A. - Dynamics of fibrosis production and resorption in intestinal schistosomiasis of mice. Mem. Inst. Oswaldo Cruz, 87: 25-31, 1992.
18. WARREN, K.S. - Experimental pulmonary schistosomiasis. Trans. roy. Soc. trop. Med. Hyg., 52: 228-233, 1964.
19. WARREN, K.S.; DOMINGOS, E.O. & COWAN, R.B.T. - Granuloma formation around schistosomose eggs as a manifestation of delayed hypersensitivity. Amer. J. Path., 51: 735-756, 1967.
20. WEIBEL, E.R. - Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol., 26: 235-302, 1969.
21. WEINSTOCK, J.V. & BOROS, D.L. - Heterogeneity of the granulomatous response in the liver, colon, ileum, and il eal Payer's patches to schistosome eggs in murine schistosomiasis. J. Immunol., 127: 1906-1909, 1981.
22. WEINSTOCK, J.V. & BOROS, D.L. - Organ-dependent differences in composition and function observed in hepatic and intestinal granulomas isolated from mice with schistosomiasis mansoni. J. Immunol., 130: 418-422, 1983.

Address for correspondence:

Zilton A. Andrade,. M.D.

Centro de Pesquisas Gonçalo Moniz (FIOCRUZ)

Rua Valdemar Falcão, 121

40.295-001 Salvador, Bahia - Brazil

Telephone: (55.71) 359-4320; Fax: (55.71)359-4292

*

This paper is an abridged version of a Thesis for the Master's degree in Pathology presented to the Federal University of Bahia by Maura Raquel Ferreira Souza Vidal.

Publication Dates

Publication in this collection
14 July 2006
Date of issue
Oct 1993

History

Received
14 Apr 1993
Accepted
29 June 1993

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

[1] 1. ALMEIDA, M.A.C. & ANDRADE, Z.A. - Effect of chemotherapy on experimental pulmonary schistosomiasis. Amer. J. trop. Med. Hyg., 32: 1049-1054, 1983.

[2] 2. ANDRADE, Z.A. & ANDRADE, S.G. - Pathogenesis of schistosomal pulmonary arteritis. Amer. J. trop. Med. Hyg., 19: 305-310, 1970.

[3] 3. ANDRADE, Z.A. & WARREN, K.S. - Mild prolonged schistosomiasis in mice: alterations in host response with time and the development of portal fibrosis. Trans. roy. Soc. trop. Med. Hyg., 58: 53-57, 1964.

[4] 4. BOROS, D.L.; PELLEY, R.P. & WARREN, K.S. - Spontaneous modulation of granulomatous hypersensitivity in schistosomiasis mansoni. J. Immunol., 114: 1437-1441, 1975.

[5] 5. CHAVES, E. - The pathology of the arterial pulmonary vasculature in Manson's schistosomiasis. Dis. Chest, 50: 72-77, 1966.

[6] 6. CHEEVER, A.W. - A comparative study of Schistosoma mansoni infections in mice, gerbils, multimmamate rats, and hamsters. Amer. J. trop. Med. Hyg., 145: 227-238, 1965.

[7] 7. CHEEVER, A.W. & WARREN, K.S. - Portal vein ligation in mice: portal hypertension, collateral circulation, and blood flow. J. appl. Physiol., 18: 405-407, 1963.

[8] 8. COLLEY, D.G.; LEWIS, F.A. & TODD, C.W. - Adoptive suppression of granuloma formation by T lymphocytes and by lymphoid cells sensitive to cyclophosphamide. Cell. Immunol., 46: 192-200, 1979.

[9] 9. COLLEY, D.G.; PARRA, J.C.; MONTESANO, M.A.; LIMA, M.; NASCIMENTO, E.; DOUGHTY, B.L.; GOES, A. & GAZZINELLE, G. - Immunoregulation in human schistosomiasis by idiotypic interactions and lymphokine-mediate mechanisms. Mem. Inst. Oswaldo Cruz, 82: 105-107, 1987.

[10] 10. DUVALL, R.H. & DeWITT, W.B. - An improved perfusion technique for recovering adult schistosome from laboratory animals. Amer. J. trop. Med. Hyg., 16: 483-486, 1967.

[11] 11. GALLATIN, W.M.; WEISSMAN, T.L. & BUTCHER, E.C. - A cell surface molecule involved in organ-specific homing of lymphocytes. Nature, 304: 30, 1983.

[12] 12. IRUSTRA, V.R.C. - Contribuiçăo ao estudo da patologia pulmonar esquistossomótica experimental. Rev. Pal. trop. 71: 203-242, 1978.

[13] 13. PHILLIPS, S.M. & LAMMIE, P.J. - Immunopathology of granuloma formation and fibrosis in schistosomiasis. Parasit. today, 2: 296-302, 1986.

[14] 14. PIERCE, E.J.; CASPAR, P.; GRZYCH, J-M; LEWIS, F.A. & SHER, A. - Downregulation of Thl cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. exp. Med., 173: 159-166, 1991.

[15] 15. PRATA, A. - Biópsia retal na esquistossomose mansoni: bases e aplicaçőes no diagnóstico e tratamento. Rio de Janeiro, Publicaçăo do Serviço de Educaçăo Sanitária, 1957.

[16] 16. SADIGURSKY, M. & ANDRADE, Z.A. - Pulmonary changes in schistosomal cor pulmonale. Amer. J. trop. Med. Hyg., 31: 779-784, 1982.

[17] 17. SANTOS, R.O.; BARBOSA Jr., A.A. & ANDRADE, Z.A. - Dynamics of fibrosis production and resorption in intestinal schistosomiasis of mice. Mem. Inst. Oswaldo Cruz, 87: 25-31, 1992.

[18] 18. WARREN, K.S. - Experimental pulmonary schistosomiasis. Trans. roy. Soc. trop. Med. Hyg., 52: 228-233, 1964.

[19] 19. WARREN, K.S.; DOMINGOS, E.O. & COWAN, R.B.T. - Granuloma formation around schistosomose eggs as a manifestation of delayed hypersensitivity. Amer. J. Path., 51: 735-756, 1967.

[20] 20. WEIBEL, E.R. - Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol., 26: 235-302, 1969.

[21] 21. WEINSTOCK, J.V. & BOROS, D.L. - Heterogeneity of the granulomatous response in the liver, colon, ileum, and il eal Payer's patches to schistosome eggs in murine schistosomiasis. J. Immunol., 127: 1906-1909, 1981.

[22] 22. WEINSTOCK, J.V. & BOROS, D.L. - Organ-dependent differences in composition and function observed in hepatic and intestinal granulomas isolated from mice with schistosomiasis mansoni. J. Immunol., 130: 418-422, 1983.

Brasil

Brasil

Experimental pulmonary schistosomiasis: lack of morphological evidence of modulation in schistosomal pulmonary granulomas

Esquistossomose pulmonar experimental: falta de evidência morfológica de modulação nos granulomas esquistosomóticos pulmonares

Abstracts

Publication Dates

History