Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter September 25, 2015

Malondialdehyde; Lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human Schistosoma mansoni infection

Inas Abdel Aziz, Mariam Yacoub, Laila Rashid and Ahmad Solieman
From the journal Acta Parasitologica

Abstract

Schistosomiasis is a debilitating parasitic disease, affects large number of host species. Currently affects 250-300 million people in tropic areas. Schistosoma pathogenic impact is hepatic periportal fibrosis; the parasite-induced inflammatory cellular activation promotes oxidative stress, resulting in lipid peroxidation (LPO), with subsequent increase in inflammatory mediators as malondialdehyde (MDA). This study was set up to reveal possible contribution of lipid peroxidation byproducts MDA in hepatic pathophysiology. Results displayed that MDA don’t tend to change in relation with either age, nor hepatic transaminases AST & ALT, while exhibited a significant increase in MDA levels in human schistosomiasis versus control group P<0.0001 (Mn. ± St.dev. 7.77 ± 3.59, 1.21 ± 0.28 nmol/ml) respectively. Moreover; MDA plasma levels in Schistosoma infected group correlated significantly with two hepatic fibrosis parameters; (a) ultrasonography graded periportal fibrosis P< 0.0001. Levels of MDA in hepatic fibrosis grades 0, I, II, III in Schistosoma infected group were (Mn. ± St.dev. 2.8 ± 0.64, 4.3 ± 1.2, 9.3 ± 1.6 and 10.8 ± 1.3 nmol/ml) respectively, (b) serum Hyaluronic acid (HA) P<0.0001 (spearman r = 0.77) as a reliable hepatic fibrosis marker. This implies a considerable role of LPO byproducts in schistosomiasis pathogenicity, and proposing malondialdehyde as a biomarker for schistosomiasis morbidity.

References

Abdallahi O.M., Hanna S., De Reggi M., Gharib B. 1999. Visualization of oxygen radical production in mouse liver in response to infection with Schistosoma mansoni. Liver, 19, 495-50010.1111/j.1478-3231.1999.tb00082.xSearch in Google Scholar

Abou-El-Naga I.F., 2013. Biomphalaria alexandrina in Egypt: Past, present and future. Journal of Biosciences, 38, 665-672. DOI: 10.1007/s12038-013-9329-410.1007/s12038-013-9329-4Search in Google Scholar

Barros A.F., Oliveira S.A., Carvalho C.L., Silva F.L., de Souza V.A., Da Silva A.L., De Araujo R.E., Souza, B., S., Soares M.B.P., Costa V.M., Coutinho E.D. 2014. Low transformation growth factor-β1 production and collagen synthesis correlate with the lack of hepatic periportal fibrosis development in undernourished mice infected with Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz, 109, 210-219. DOI: 10.1590/0074-027614026610.1590/0074-0276140266Search in Google Scholar

Coutinho E.M., Silva F.L., Barros A.F., Araujo R.E., Oliveira S.A.L., Carlos F.B., Aryon A.A., Zilton A. 2007. Repeated infections with Schistosoma mansoni and liver fibrosis in undernourished mice. Acta Tropica, 101, 15-24. DOI: 10.1016/j.actatropica.2006.03.00610.1016/j.actatropica.2006.03.006Search in Google Scholar

Coutinho H.M., McGarvey S.T., Acosta L.P., Manalo D.L., Langdon G.C., Leenstra T., Kanzaria H.K., Solomon J., Wu H., Olveda R., Kurtis J.D., Friedman J.F. 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. The Journal of Infectious Diseases, 192, 528-36. DOI: 10.1086/43092910.1086/430929Search in Google Scholar

Cunha G.M., Silva V.M.A., Bessa K.D.G., Bitencourt M.A.O., Macedo U.B.O., Freire-Neto F.P., Martins R.R., Assis C.F., Lemos T.M.A.M., Almeida M.G., Freire A.C.G. 2012. Levels of oxidative stress markers: correlation with hepatic function and worm burden patients with schistosomiasis. Acta Parasitologica, 57, 160-166. DOI: 10.2478/s11686-012-0026-510.2478/s11686-012-0026-5Search in Google Scholar

Dessein A.J., Marquet S., Henri S., E.l., Wali N.E., Hillaire D., Rodrigues V., Prata A., Ali Q.M., Gharib, B., de Reggi M., Magzoub M.M., Saeed O.K., Abdelhameed A.A., Abel L. 1999. Infection and disease in human schistosomiasis mansoni are under distinct major gene control. Microbes and Infection, 1, 561-56710.1016/S1286-4579(99)80096-3Search in Google Scholar

Domingues A.L.C., Medeiros T.B., Lopes E.P. de A. 2011. Ultrasound versus biological markers in the evaluation of periportal fibrosis in human Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz, 106, 802-80710.1590/S0074-02762011000700004Search in Google Scholar

Eboumbou C., Steghens J.P., Abdallahi O.M.S., Mirghani A., Gallian P., van Kappel A., Qurashi A., Gharib B., De Reggi M. 2005. Circulating markers of oxidative stress and liver fibrosis in Sudanese subjects at risk of schistosomiasis and hepatitis. Acta Tropica, 94, 99-106. DOI: 10.1016/j.actatropica.2005.03.00110.1016/j.actatropica.2005.03.001Search in Google Scholar

Elsammak M.Y., Al-Sharkaweey R.M., Ragab M.S., Amin G.A., Kandil M.H. 2008. IL-4 and reactive oxygen species are elevated in Egyptian patients affected with schistosomal liver disease. Parasite Immunology, 30, 603-609. DOI: 10.1111/ j.1365-3024.2008.01061.x Esterbauer H., Schaur R.J., Zollner H. 1991. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology and Medicine, 11, 81-128Search in Google Scholar

Esterbauer H. 1993. Cytotoxicity and genotoxicity of lipid-oxidation products. The American Journal of Clinical Nutrition, 57, 779S-785S 10.1093/ajcn/57.5.779SSearch in Google Scholar

Facundo H.T.F., Brandt C.T., Owen J.S., Lima V.L.M. 2004. Elevated levels of erythrocyte-conjugated dienes indicate increased lipid peroxidation in schistosomiasis mansoni patients. Brazilian Journal Of Medical and Biological Research, 37, 957-962. DOI: /S0100-879X200400070000310.1590/S0100-879X2004000700003Search in Google Scholar

Gil L., Siems W., Mazurek B., Gross J., Schroeder P., Voss P., Grune T. 2006. Age-associated analysis of oxidative stress parameters in human plasma and erythrocytes. Free Radic Res, 40, 495-505. DOI: 10.1080/1071576060059296210.1080/10715760600592962Search in Google Scholar

Gordon C.C., and Alimuddin I.Z. 2003. Manson’s Tropical Diseases. W.B. Saunders, USA, PhiladelphiaSearch in Google Scholar

Grigorescu M., 2006. Noninvasive Biochemical Markers of Liver Fibrosis. Journal of Gastrointestinal and Liver Diseases, 15, 149-159Search in Google Scholar

Gutteridge J.M., Halliwell B. 1990. The measurement and mechanism of lipid peroxidation in biological systems. Trends in Biochemical Sciences, 15, 129-13510.1016/0968-0004(90)90206-QSearch in Google Scholar

Halfon P., Bourliere M., Penaranda G., Deydier R., Renou C., Botta- Fridlund D., Tran A., Portal I., Allemand I., Rosenthal-Allieri A., Ouzan D. 2005. Accuracy of hyaluronic acid level for predicting liver fibrosis stages in patients with hepatitis C virus. Comparative Hepatology, 4, 6. DOI: 10.1186/1476-5926-4-610.1186/1476-5926-4-6Search in Google Scholar

Hotez P.J., Molyneux D.H., Fenwick A., Ottesen E., Ehrlich Sachs S., Sachs Je. D. 2006. Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med, 3, e102. DOI: 10. 1371/journal.pmed.003010210.1371/journal.pmed.0030102Search in Google Scholar

King C.H., Dickman K., Tisch D.J. 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disabilityrelated outcomes in endemic schistosomiasis. Lancet, 365, 1561-1569. DOI: 10.1016/S0140-6736(05)66457-410.1016/S0140-6736(05)66457-4Search in Google Scholar

Köpke-Aguiar L., Martins J.R., Passerotti C., Toledo C.F., Nader H.B., Borges D.R. 2002. Serum hyaluronic acid as a comprehensive marker to assess severity of liver disease in schistosomiasis. Acta Tropica, 84, 117-126. DOI: 10.1016/S0001-706X(02)00136-510.1016/S0001-706X(02)00136-5Search in Google Scholar

Lefèvre G., Beljean-Leymarie M., Beyerle F., Bonnefont-Rousselot D., Cristol J.P., Thérond P., Torreilles J. 1998. Evaluation of lipid peroxidation by measuring thiobarbituric acid reactive substances. Annales De Biologie Clinique (Paris), 56, 305-319Search in Google Scholar

Maia M.D., Lopes E.P.A., Ferraz A.A.B., Barros, Fábio M.R., Domingues A.L.C., Ferraz E.M. 2007. Evaluation of splenomegaly in the hepatosplenic form of mansonic schistosomiasis. Acta Tropica, 101, 183-186. DOI: 10.1016/j.actatropica.2007.01.00410.1016/j.actatropica.2007.01.004Search in Google Scholar

Marnett L.J. 2000. Oxyradicals and DNA damage. Carcinogenesis, 21, 361-370. DOI:10.1093/carcin /21.3.361Search in Google Scholar

Mendoza-Núñez V.M., Ruiz-Ramos M., Sánchez-Rodríguez M., Retana- Ugalde R., Muñoz-Sánchez J.L. 2007. Aging-related oxidative stress in healthy humans. Tohoku Journal of Experimental Medicine, 213, 261-268. DOI: 10.1620/tjem.213.26110.1620/tjem.213.261Search in Google Scholar

Nielsen F., Mikkelsen B.B., Nielsen J.B., Andersen H.R. 1997. Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clinical Chemistry, 1214, 1209-121410.1093/clinchem/43.7.1209Search in Google Scholar

Pearce E.J., MacDonald A.S. 2002. The immunobiology of schistosomiasis. Nature Reviews Immunology, 2, 499-511. DOI: 10.1038/nri843 10.1038/nri843Search in Google Scholar

Pontinha N., Pessegueiro H., Barros H. 1999. Serum hyaluronan as a marker of liver fibrosis in asymptomatic chronic viral hepatitis B. Scandinavian Journal of Clinical and Laboratory Investigation, 59 343-34710.1080/00365519950185535Search in Google Scholar

Richter J., Lúcia A., Domingues C., Barata C.H., Prata A.R., Lambertucci J.R., 2001. Report of the Second Satellite Symposium on Ultrasound in Schistosomiasis. Memórias do Instituto Oswaldo Cruz, 96, 151-15610.1590/S0074-02762001000900023Search in Google Scholar

Richter J., 2000. Evolution of schistosomiasis-induced pathology after therapy and interruption of exposure to schistosomes: a review of ultrasonographic studies. Acta Tropica, 77, 111-13110.1016/S0001-706X(00)00125-XSearch in Google Scholar

Santos V.N. dos., Leite-Mór M.M.B., Kondo M., Martins J.R., Nader H., Lanzoni V.P., Parise E.R. 2005. Serum laminin, type IV collagen and hyaluronan as fibrosis markers in non-alcoholic fatty liver disease. Brazilian Journal Of Medical and Biological Research, 38, 747-753. DOI: 10.1590/S0100-879X200 5000500012Search in Google Scholar

Sies H., Cadenas E., Symons M.C.R., Scott G., 1985. Oxidative Stress: Damage to Intact Cells and Organs [and Discussion]. Philosophical Transactions of the Royal Society B: Biological Sciences, 311, 617-631. DOI: 10.1098/rstb.1985.016810.1098/rstb.1985.0168Search in Google Scholar

Taccone-Gallucci M., Lubrano R., Meloni C., Morosetti M., Adolfo C.M.C.C. 1998. Malonyldialdehyde content of cell membranes is the most important marker of oxidative stress in haemodialysis patients. Nephrology Dialysis Transplantation, Oct; 13, 2711-271210.1093/ndt/13.10.2711Search in Google Scholar

Vanheule E., Geerts A.M., Van Huysse J., Schelfhout D., Praet M., Van Vlierberghe H., De Vos M., Colle I. 2008. An intravital microscopic study of the hepatic microcirculation in cirrhotic mice models: relationship between fibrosis and angiogenesis. International Journal of Experimental Pathology, 89, 419-432. DOI: 10.1111/j.1365-2613.2008.00608.x 10.1111/j.1365-2613.2008.00608.xSearch in Google Scholar

Zhou X.N., Wang L.Y., Chen M.G., Wu X.H., Jiang Q.W., Chen X.Y., Zheng J. Utzinger J. 2005. The public health significance and control of schistosomiasis in China-then and now. Acta Tropica, 96, 97-105. DOI: 10.1016/j.actatropica.2005.07.005 10.1016/j.actatropica.2005.07.005Search in Google Scholar

Received: 2014-12-13
Revised: 2015-5-29
Accepted: 2015-6-1
Published Online: 2015-9-25
Published in Print: 2015-12-1

W. Stefański Institute of Parasitology, PAS