Serum hyaluronan and collagen IV as non-invasive markers of liver fibrosis in patients from an endemic area for schistosomiasis mansoni: A field-based study in Brazil

Memorias do Instituto Oswaldo Cruz

Volumn 105, Issue 4, 2010, Pages 471-478

  Marinho, Carolina Coimbra ^a   Bretas, Thales ^a   Voieta, Izabela ^a   de Queiroz, Leonardo Campos ^a   Ruiz Guevara, Raiza ^b   Teixeira, Antônio Lúcio ^a   Antunes, Carlos Maurício ^a   Prata, Aluízio ^b   Lambertucci, José Roberto ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF TRIÂNGULO MINEIRO   (Brazil)

Author keywords

Fibrosis markers; Hepatosplenic schistosomiasis; Liver fibrosis; Schistosomiasis; Ultrasound

Indexed keywords

EID: 77955503741     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/S0074-02762010000400020     Document Type: Article

References (74)

1. Abdel-Wahab MF, Esmat G, Farrag A, el-Boraey YA, Strickland GT 1992. Grading of hepatic schistosomiasis by the use of ultra- sonography. Am J Trop Med Hyg 46: 403-408.
2. Abdel-Wahab MF, Esmat G, Milad M, Abdel-Razek S, Strickland GT 1989. Characteristic sonographic pattern of schistosomal hepatic fibrosis. Am J Trop Med Hyg 40: 72-76.
3. Abdel-Wahab MF, Strickland GT 1993. Abdominal ultrasonography for assessing morbidity from schistosomiasis 2. Hospital studies. Trans R Soc Trop Med Hyg 87: 135-137.
4. Afdhal NH 2004. Biopsy or biomarkers: is there a gold standard for diagnosis of liver fibrosis? Clin Chem 50: 1299-1300.
5. Afdhal NH, Nunes D 2004. Evaluation of liver fibrosis: a concise re- view. Am J Gastroenterol 99: 1160-74.
6. Andrade ZA 2004. Schistosomal hepatopathy. Mem Inst Oswaldo Cruz 99 (Suppl.1): 51-57.
7. Andrade ZA, Silva LM, de Souza MM 1997. An experimental ap- proach to the pathogenesis of "pipestem" fibrosis (Symmers' fi- brosis of the liver). Mem Inst Oswaldo Cruz 92: 699-706.
8. Blazejewski S, preaux AM, Mallat A, Brocheriou I, Mavier P, Dhumeaux D, Hartmann D, Schuppan D, Rosenbaum J 1995. Human myofibroblastlike cells obtained by outgrowth are rep- resentative of the fibrogenic cells in the liver. Hepatology 22: 788 -798.
9. Bogliolo L 1957. The anatomical picture of the liver in hepatosplenic schistosomiasis mansoni. Ann Trop Med Parasitol 51: 1-14.
10. Burchard GD, Guissé-Sow F, Diop M, Ly A, Lanuit R, Gryseels B, Gressner AM 1998. Schistosoma mansoni infection in a recently exposed community in Senegal: lack of correlation between liver morphology in ultrasound and connective tissue metabolites in serum. Trop Med Int Health 3: 234-241.
11. Cheung KJ, Tilleman K, Deforce D, Colle I, Van Vlierberghe H 2008. proteomics in liver fibrosis is more than meets the eye. Eur J Gastroenterol Hepatol 20: 450-464.
12. Cota GF, pinto-Silva RA, Antunes CM, Lambertucci JR 2006. Ultra- sound and clinical investigation of hepatosplenic schistosomiasis: evaluation of splenomegaly and liver fibrosis four years after mass chemotherapy with oxamniquine. Am J Trop Med Hyg 74: 103-107.
13. Doehring-Schwerdtfeger E, Mohamed-Ali G, Abdel-Rahim IM, Kardorff R, Franke D, Kaiser C, Elsheikh M, Ehrich JH 1989. Son- omorphological abnormalities in Sudanese children with Schisto- soma mansoni infection: a proposed staging-system for field diag- nosis of periportal fibrosis. Am J Trop Med Hyg 41: 63-69.
14. Eboumbou C, Steghens Jp, Abdallahi OM, Mirghani A, Gallian p, van Kappel A, Qurashi A, Gharib B, De Reggi M 2005. Cir- culating markers of oxidative stress and liver fibrosis in Su- danese subjects at risk of schistosomiasis and hepatitis. Acta Trop 94: 99-106.
15. Fraser JR, Engström-Laurent A, Nyberg A, Laurent TC 1986. Remov- al of hyaluronic acid from the circulation in rheumatoid disease and primary biliary cirrhosis. J Lab Clin Med 107: 79-85.
16. Fraser JR, Laurent TC, Laurent UB 1997. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med 242: 27-33.
17. Friedman SL 1993. Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N Engl J Med 328: 1828-1835.
18. Friedman SL 1999. Cytokines and fibrogenesis. Semin Liver Dis 19: 129-140.
19. Friedman SL 2000. Molecular regulation of hepatic fibrosis, an integrat- ed cellular response to tissue injury. J Biol Chem 275: 2247-2250.
20. Friedman SL 2003. Liver fibrosis - from bench to bedside. J Hepatol 38 (Suppl. 1): S38-53
21. Gressner AM 1998. The cell biology of liver fibrogenesis - an imbalance of proliferation, growth arrest and apoptosis of myofibroblasts. Cell Tissue Res 292: 447-452.
22. Gressner AM, Bachem MG 1990. Cellular sources of noncollagenous matrix proteins: role of fat-storing cells in fibrogenesis. Semin Liver Dis 10: 30-46.
23. Grigorescu M 2006. Noninvasive biochemical markers of liver fibro- sis. J Gastrointestin Liver Dis 15: 149-159.
24. Grimaud JA 1987. Cell-matrix interactions in schistosomal portal fibrosis: a dynamic event. Mem Inst Oswaldo Cruz 82 (Suppl. 4): 55-65.
25. Gryseels B, polman K, Clerinx J, Kestens L 2006. Human schistosomiasis. Lancet 368: 1106-1118.
26. Guangjin S, Mingdao J, Qiyang L, Hui X, Jiangming H, Xiaomei Y 2002. Study on histopathology, ultrasonography and some special serum enzymes and collagens for 38 advanced patients of schistosomiasis japonica. Acta Trop 82: 235-246.
27. Guéchot J, Laudat A, Loria A, Serfaty L, poupon R, Giboudeau J 1996. Diagnostic accuracy of hyaluronan and type III procollagen aminoterminal peptide serum assays as markers of liver fibrosis in chronic viral hepatitis C evaluated by ROC curve analysis. Clin Chem 42: 558-563.
28. Halfon p, Bourlière M, pénaranda G, Cacoub p 2006. Les marqueurs sanguins non invasifs de fibrose hépatique au cours de l'infection chronique par le virus de l'hépatite C. Rev Med Interne 27: 751-761.
29. Hiramatsu N, Hayashi N, Kasahara A, Hagiwara H, Takehara T, Haruna Y, Naito M, Fusamoto H, Kamada T 1995. Improvement of liver fibrosis in chronic hepatitis C patients treated with natural inter- feron alpha. J Hepatol 22: 135-142.
30. Homeida M, Abdel-Gadir AF, Cheever AW, Bennett JL, Arbab BM, Ibrahium SZ, Abdel-Salam IM, Dafalla AA, Nash TE 1988. Di- agnosis of pathologically confirmed Symmers' periportal fibro- sis by ultrasonography: a prospective blinded study. Am J Trop Med Hyg 38: 86-91.
31. Kardorff R, Mugashe C, Gabone RM, Mahlert C, Doehring E 1999. Diagnostic value of connective tissue metabolites in Schistosoma mansoni related liver disease. Acta Trop 73: 153-164.
32. Kariuki HC, Mbugua G, Magak P, Bailey JA, Muchiri EM, Thiongo FW, King CH, Butterworth AE, Ouma JH, Blanton RE 2001. prevalence and familial aggregation of schistosomal liver mor- bidity in Kenya: evaluation by new ultrasound criteria. J Infect Dis 183: 960-966.
33. Katz N, Chaves A, pellegrino J 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397-400.
34. Kisseleva T, Brenner DA 2007. Role of hepatic stellate cells in fibro- genesis and the reversal of fibrosis. J Gastroenterol Hepatol 22 (Suppl. 1): S73-S78.
35. Köpke-Aguiar LA, Martins JR, passerotti CC, Toledo CF, Nader HB, Borges DR 2002. Serum hyaluronic acid as a comprehensive marker to assess severity of liver disease in schistosomiasis. Acta Trop 84: 117-126.
36. Lambertucci JR 1993. Schistosoma mansoni: pathological and clini- cal aspects. In p Jordan, G Webbe (eds.), Human schistosomiasis, Cab International, Wallingford, p. 195-225.
37. Lambertucci JR, Andrade LM, pinto-Silva RA 2002. Magnetic reso- nance imaging of the liver in hepatosplenic schistosomiasis man- soni. Rev Soc Bras Med Trop 35: 679-680.
38. Lambertucci JR, Cota GF, pinto-Silva RA, Serufo JC, Gerspacher- Lara R, Drummond SC, Antunes CM, Nobre V, Rayes A 2001. Hepatosplenic schistosomiasis in field-based studies: a combined clinical and sonographic definition. Mem Inst Oswaldo Cruz 96 (Suppl.1): 147-150.
39. Lambertucci JR, dos Santos Silva LC, Andrade LM, de Queiroz LC, Carvalho VT, Voieta I, Antunes CM 2008. Imaging techniques in the evaluation of morbidity in schistosomiasis mansoni. Acta Trop 108: 209-217.
40. Lambertucci JR, Serufo JC, Gerspacher-Lara R, Rayes AA, Teixeira R, Nobre V, Antunes CM 2000. Schistosoma mansoni: assessment of morbidity before and after control. Acta Trop 77: 101-109.
41. Lambertucci JR, Silva LC, Andrade LM, de Queiroz LC, pinto-Silva RA 2004. Magnetic resonance imaging and ultrasound in hepatosplenic schistosomiasis mansoni. Rev Soc Bras Med Trop 37: 333-337.
42. Lenzi HL, Kimmel E, Schechtman H, pelajo-Machado M, Romanha WS, pacheco RG, Mariano M, Lenzi JA 1998. Histoarchitecture of schistosomal granuloma development and involution: morpho- genetic and biomechanical approaches. Mem Inst Oswaldo Cruz 93 (Suppl. I): 141-151.
43. Lenzi HL, Kimmel E, Schechtman H, pelajo-Machado M, Vale BS, panasco MS, Lenzi JA 1999. Collagen arrangement in hepatic granuloma in mice infected with Schistosoma mansoni: depen- dence on fiber radiation centers. Braz J Med Biol Res 32: 639-643.
44. Li YS, Sleigh AC, Ross AG, Li Y, Williams GM, Tanner M, McManus Dp 2000. Two-year impact of praziquantel treatment for Schisto- soma japonicum infection in China: re-infection, subclinical dis- ease and fibrosis marker measurements. Trans R Soc Trop Med Hyg 94: 191-197.
45. Marinho CC, Voieta I, Azeredo LM, Nishi Mp, Batista TS, pereira AC, Serufo JC, Queiroz LC, Ruiz-Guevara R, Antunes CM, prata A, Lambertucci JR 2006. Clinical versus ultrasound examination in the evaluation of hepatosplenic schistosomiasis mansoni in en- demic areas. Mem Inst Oswaldo Cruz 101 (Suppl. I): 317-321.
46. Murawaki Y, Koda M, Okamoto K, Mimura K, Kawasaki H 2001. Di- agnosis value of serum type IV collagen test in comparison with platelet count for predicting the fibrotic stage in patients with chronic hepatitis C. J Gastroenterol Hepatol 16: 777-781.
47. Nakatsukasa H, Nagy p, Evarts R p, Hsia CC, Marsden E, Thorgeirsson SS 1990. Cellular distribution of transforming growth factor-beta 1 and procollagen types I, III and IV transcripts in carbon tetrachlo- ride-induced rat liver fibrosis. J Clin Invest 85: 1833-1843.
48. Niamey Working Group 2000. Ultrasound in schistosomiasis. A practical guide to the standardized use of ultrasonography for the assessment of schistosomiasis related morbidity, World Health Organization, TDR/STR/SCH/00.1, Geneva.
49. parés A, Deulofeu R, Giménez A, Caballería L, Bruguera M, Caballería J, Ballesta AM, Rodés J 1996. Serum hyaluronate reflects hepatic fibrogenesis in alcoholic liver disease and is useful as a marker of fibrosis. Hepatology 24: 1399-1403.
50. pascal M, Abdallahi OM, Elwali NE, Mergani A, Qurashi MA, Magzoub M, de Reggi M, Gharib B 2000. Hyaluronate levels and markers of oxidative stress in the serum of Sudanese subjects at risk of infection with Schistosoma mansoni. Trans R Soc Trop Med Hyg 94: 66-70.
51. pereira TN, Lewindon pJ, Smith JL, Murphy TL, Lincoln DJ, Shepherd RW, Ramm GA 2004. Serum markers of hepatic fibrogenesis in cystic fibrosis liver disease. J Hepatol 41: 576-583.
52. pinto-Silva RA, Abrantes WL, Antunes CM, Lambertucci JR 1994. Sonographic features of portal hypertension in schistotomiasis mansoni. Rev Inst Med Trop Sao Paulo 36: 355-361.
53. Ricard-Blum S, Hartmann DJ, Grenard p, Ravaoalimalala VE, Boisier p, Esterre p 1999. Relationships between several markers of ex- tracellular matrix turn-over and ultrasonography in human schis- tosomiasis mansoni. Am J Trop Med Hyg 60: 658-663.
54. Richter J 2000. Evolution of schistosomiasis-induced pathology after therapy and interruption of exposure to schistosomes: a review of ultrasonographic studies. Acta Trop 77: 111-131.
55. Richter J, Zwingenberger K, Ali QM, Lima W de M, Dacal AR, de Siqueira GV, Doehring-Schwerdtfeger E, Feldmeier H 1992. Hepatosplenic schistosomiasis; comparison of sonographic find- ings in Brazilian and Sudanese patients - correlation of sonograph- ic findings with clinical symptoms. Radiology 184: 711-716.
56. Ruiz-Guevara R, de Noya BA, Valero SK, Lecuna p, Garassini M, Noya O 2007. Clinical and ultrasound findings before and after praziquantel treatment among Venezuelan schistosomiasis pa- tients. Rev Soc Bras Med Trop 40: 505-511.
57. Ruiz-Guevara RJR 2005. Esquistossomose na área hiperendêmica de Brejo do Espírito Santo, com seguimento de 29 anos. phD Thesis, Universidade Federal do Triângulo Mineiro, Uberaba, 239 pp.
58. Sakugawa H, Nakayoshi T, Kobashigawa K, Yamashiro T, Maeshiro T, Miyagi S, Shiroma J, Toyama A, Nakayoshi T, Kinjo F, Saito A 2005. Clinical usefulness of biochemical markers of liver fibrosis in patients with nonalcoholic fatty liver disease. World J Gastro- enterol 11: 255-259.
59. Santos VN, Leite-Mór MM, Kondo M, Martins JR, Nader H, Lanzoni V p, parise ER 2005. Serum laminin, type IV collagen and hy- aluronan as fibrosis markers in non-alcoholic fatty liver disease. Braz J Med Biol Res 38: 747-753.
60. Shahin M, Schuppan D, Waldherr R, Risteli J, Risteli L, Savolainen ER, Oesterling C, Abdel Rahman HM, el Sahly AM, Abdel Razek SM, El Ruby O, Koch A, Seitz HK 1992. Serum procol- lagen peptides and collagen type VI for the assessment of activity and degree of hepatic fibrosis in schistosomiasis and alcoholic liver disease. Hepatology 15: 637-644.
61. Silva LC, pereira AC, Queiroz LC, Andrade LM, Antunes CM, Lam- bertucci JR 2006. Disagreement between ultrasound and magnetic resonance imaging in the identification of schistosomal periportal fibrosis. Mem Inst Oswaldo Cruz 101 (Suppl. I): 279-282.
62. Stickel F, poeschl G, Schuppan D, Conradt C, Strenge-Hesse A, Fuchs FS, Hofmann WJ, Seitz HK 2003. Serum hyaluronate correlates with histological progression in alcoholic liver disease. Eur J Gastroenterol Hepatol 15: 945-950.
63. Stone PJ 2000. Potential use of collagen and elastin degradation markers for monitoring liver fibrosis in schistosomiasis. Acta Trop 77: 97-99.
64. Suzuki A, Angulo p, Lymp J, Li D, Satomura S, Lindor K 2005. Hyaluronic acid, an accurate serum marker for severe hepatic fibrosis in patients with non-alcoholic fatty liver disease. Liver Int 25: 779-786.
65. Tao J, peng HQ, Cai WM, Dong FQ, Weng HL, Liu RH 2003. Influence factors of serum fibrosis markers in liver fibrosis. World J Gastroenterol 9: 2497-2500.
66. Torre F, Bellis L, Delfino A, pelli N, Contini p, Basso M, puoti C, picciotto A 2008. Peripheral blood serum markers for apoptosis and liver fibrosis: are they trustworthy indicators of liver real- ness? Dig Liver Dis 40: 441-445.
67. Voieta I 2008. Comparação entre a fibrose periportal diagnosticada pelo ultra-som e pela ressonância magnética e a histologia hepática na hipertensão porta esquistossomótica. MSc Thesis, Universidade Federal de Minas Gerais, Belo Horizonte, 94 pp.
68. WMA - World Medical Association Declaration of Helsinki 1964 Ethical principles for medical research involving human subjects. [updated 2008 Oct 22; cited 2009 Mai 04]. Available from: http://www.wma.net/e/policy/b3.htm.
69. Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM 2004. Immunopathogenesis of schistosomiasis. Immunol Rev 201: 156-167.
70. Wyszomirska RM, Lacet C da C, Tenório LR, Nishimura NF, Mesquita MA, Neto JB, Oliveira F, Balwani M do C, Almeida JR, Soares EC 2006. Decrease of type IV collagen and TIMp-1 serum levels after splenectomy in patients with schistosomiasis mansoni. Acta Trop 97: 301-308.
71. Wyszomirska RM, Nishimura NF, Almeida JR, Yamanaka A, Soares EC 2005. High serum laminin and type IV collagen levels in schistosomiasis mansoni. Arq Gastroenterol 42: 221-225.
72. Yoneda M, Mawatari H, Fujita K, Yonemitsu K, Kato S, Takahashi H, Kirikoshi H, Inamori M, Nozaki Y, Abe Y, Kubota K, Saito S, Iwasaki T, Terauchi Y, Togo S, Maeyama S, Nakajima A 2007. Type IV collagen 7s domain is an independent clinical marker of the severity of fibrosis in patients with nonalcoholic steatohepati- tis before the cirrhotic stage. J Gastroenterol 42: 375-381.
73. Zheng M, Cai WM, Weng HL, Liu RH 2002. ROC curves in evalua- tion of serum fibrosis indices for hepatic fibrosis. World J Gas- troenterol 8: 1073-1076.
74. Zheng M, Cai WM, Zhao JK, Zhu SM, Liu RH 2005. Determination of serum levels of YKL-40 and hyaluronic acid in patients with hepatic fibrosis due to schistosomiasis japonica and appraisal of their clinical value. Acta Trop 96: 148-152.