Introduction: Hepatitis C virus (HCV) is a viral infection affecting 71 million people worldwide. A high prevalence of co-infection has been observed with parasitic infections, such as Schistosoma mansoni, Fasciola sp., and Toxoplasma gondii, all of which can contribute to the progression of liver disease. This study aimed to investigate the prevalence of co-parasitic infections with HCV-positive individuals within Egyptian populations and the resulting biochemical changes in liver and kidney biomarkers. Materials and Methods: A total of three hundred and thirty-seven blood samples were screened molecularly for HCV and immunologically for parasitic infections using PCR and ELISA, respectively. Liver functions were monitored by measuring serum levels of glutamic oxaloacetic aminotransferase (GOT), glutamate pyruvate alanine aminotransferase (GPT), gamma-glutamyl transferase (GGT), total protein (TP), albumin (Alb), total bilirubin (T Bil), and alkaline phosphatase (ALK). Kidney functions were evaluated by measuring creatinine, uric acid, urea, sodium (Na), and potassium (K) levels. Patients were categorized by gender and age <21, 21-50, and >50 years. Results indicated that 120 out of 287 HCV-infected cases (41.8%) have Schistosoma infection, of which 57, 31, 24, and 8 cases were mono-infected and co-infected with Fasciola, Toxoplasma, and Fasciola/Toxoplasma, respectively Additionally, 99 patients (34.5%) were infected with Fasciola hepatica infection, of which 51 were mono-infected and 9 were co-infected with Toxoplasma. Results: A total of 87 patients (30.3%) tested positive for T. gondii infection, of which 46 cases were mono-infected. Additionally, the proportion of male patients with monoparasitic infection ranged from 78.2% (Toxoplasma) and 84.3% (S. mansoni or F. hepatica). On the other hand, the highest incidences of single infections among males (Fasciola and Toxoplasma) were over the age of 50 years for Fasciola (43.1%) and Toxoplasma (39.1%), respectively. In contrast, S. mansoni mono-infection was most prevalent (42.1%) among males aged 21–50 years. Conclusion: Liver enzyme levels (GPT, GOT, Alk, and GGT) and kidney parameters (creatinine and urea) were significantly affected by the type (mono or mixed) and species of parasitic infections in HCV patients. Additionally, most serological parameters were significantly in cases of viral/parasitic co-infections, especially, among patients with high viral loads. |
References
- World Health Organization. Global hepatitis report. Geneva: World Health Organization; 2017. [Link]
- Kouyoumjian SP, Chemaitelly H, Abu-Raddad LJ. Characterizing hepatitis C virus epidemiology in Egypt: Systematic reviews, meta-analyses, and meta-regressions. Sci Rep. 2018; 8(1):1661. [DOI:10.1038/s41598-017-17936-4] [PMID]
- Hajarizadeh B, Grebely J, Dore GJ. Epidemiology and natural history of HCV infection. Nat Rev Gastroenterol Hepatol. 2013; 10(9):553-62. [DOI:10.1038/nrgastro.2013.107] [PMID]
- el-Hawy AM, Massoud A, el-Badrawy N, Elgaram A, Khalil A, Metwally A. Hepatic histochemistry and electron microscopy of hamsters infected with S. mansoni and treated with praziquantel therapy. J Egypt Soc Parasitol. 1985; 15(1):249-62. [PMID]
- Weitberg AB, Alper JC, Diamond I, Fligiel Z. Acute granulomatous hepatitis in the course of acquired toxoplasmosis. N Engl J Med. 1979; 300(19):1093-6. [DOI:10.1056/NEJM197905103001907] [PMID]
- World Health Organization. Research priorities for zoonoses and marginalized infections. Geneva: World Health Organization; 2012. [Link]
- Machicado C, Machicado JD, Maco V, Terashima A, Marcos LA. Association of Fasciola hepatica Infection with Liver Fibrosis, Cirrhosis, and Cancer: A systematic review. PLoS Negl Trop Dis. 2016; 10(9):e0004962. [DOI:10.1371/journal.pntd.0004962] [PMID]
- Chang Wong MR, Pinto Elera JO, Guzman Rojas P, Terashima Iwashita A, Samalvides Cuba F. [Demographic and clinical aspects of hepatic fascioliasis between 2013-2010 in National Hospital Cayetano Heredia, Lima, Peru (Spanish)]. Rev Gastroenterol Peru. 2016; 36(1):23-8. [PMID]
- Ma H, Shieh KJ. ELISA technique. Nat Sci. 2006; 4(2):36-7. [Link]
- Chisango TJ, Ndlovu B, Vengesai A, Nhidza AF, Sibanda EP, Zhou D, et al. Benefits of annual chemotherapeutic control of schistosomiasis on the development of protective immunity. BMC Infect Dis. 2019; 19(1):219. [DOI:10.1186/s12879-019-3811-z] [PMID]
- Tefera A, Belay T, Bajiro M. Epidemiology of Schistosoma mansoni infection and associated risk factors among school children attending primary schools nearby rivers in Jimma town, an urban setting, Southwest Ethiopia. Plos One. 2020; 15(2):e0228007. [DOI:10.1371/journal.pone.0228007] [PMID]
- Faust CL, Osakunor DNM, Downs JA, Kayuni S, Stothard JR, Lamberton PHL, et al. Schistosomiasis Control: Leave No Age Group Behind. Trends Parasitol. 2020; 36(7):582-91.[DOI:10.1016/j.pt.2020.04.012] [PMID]
- Parkinson M, O’neill SM, Dalton JP Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol Infect. 2007; 135(4):669-74. [DOI:10.1017/S095026880600728X] [PMID]
- Curtale F, Hassanein YAW, Barduagni P, Yousef MM, Wakeel AE, Hallaj Z, et al. Human fascioliasis infection: Gender differences within school-age children from endemic areas of the Nile Delta, Egypt. Trans R Soc Trop Med Hyg. 2007; 101(2):155-60. [DOI:10.1016/j.trstmh.2006.05.006] [PMID]
- Božo Š, Katarina M, Jakovac S, Jurica A. Seroprevalence of Toxoplasma gondii among general population in Bosnia and Herzegovina: 10-Years single center experience. Clin Epidemiol Glob Health. 2023; 22:101336-6. [DOI:10.1016/j.cegh.2023.101336]
- Raso G, Vounatsou P, McManus DP, N'Goran EK, Utzinger J. A Bayesian approach to estimate the age-specific prevalence of Schistosoma mansoni and implications for schistosomiasis control. Int J Parasitol. 2007; 37(13):1491-500. [DOI:10.1016/j.ijpara.2007.05.004] [PMID]
- Naus CW, Booth M, Jones FM, Kemijumbi J, Vennervald BJ, Kariuki CH, et al. The relationship between age, sex, egg-count and specific antibody responses against Schistosoma mansoni antigens in a Ugandan fishing community. Trop Med Int Health. 2003; 8(6):561-8. [DOI:10.1046/j.1365-3156.2003.01056.x.] [PMID]
- Egoro ET, Ilegbedion GI, Loveday ZU, Shonibare MS. Blood biochemical and haematological alterations in Schistosoma mansoni infected patients in Ijora-Badia Nigeria. European J Biomed Pharm Sci. 2017; 4(11):148-52. [Link]
- Silva IS, Ferraz ML, Perez RM, Lanzoni VP, Figueiredo VM, Silva AE. Role of gamma-glutamyl transferase activity in patients with chronic hepatitis C virus infection. J Gastroenterol Hepatol. 2004; 19(3):314-8. [DOI:10.1111/j.1440-1746.2003.03256.X] [PMID]
- Gajewska A, Smaga-Kozłowska K, Wiśniewski M. [Pathological changes of liver in infection of Fasciola hepatica (Polish)]. Wiad Parazytol. 2005; 51(2):115-23. [PMID]
- Shaker Y, Samy N, Ashour E. Hepatobiliary Schistosomiasis. J Clin Transl Hepatol. 2014; 2(3):212-6. [DOI:10.14218/JCTH.2014.00018] [PMID]
- Xue Q, Wang Y, Liu Y, Hua H, Zhou X, Xu Y, et al. Dysregulated glucuronidation of bilirubin exacerbates liver inflammation and fibrosis in schistosomiasis Japonica through the NF-κB Signaling Pathway. Pathogens. 2024; 13(4):287. [DOI:10.3390/pathogens13040287] [PMID]
- Mihm S, Hartmann H, Ramadori G. A reevaluation of the association of hepatitis C virus replicative intermediates with peripheral blood cells including granulocytes by a tagged reverse transcription/polymerase chain reaction technique. J Hepatol. 1996; 24(4):491-7. [DOI:10.1016/s0168-8278(96)80171-1] [PMID]
- Giannini EG, Testa R, Savarino V. Liver enzyme alteration: A guide for clinicians. CMAJ. 2005; 172(3):367-79. [DOI:10.1503/cmaj.1040752] [PMID]
- Giannini E, Botta F, Fasoli A, Romagnoli P, Mastracci L, Ceppa P, et al. Increased levels of gammaGT suggest the presence of bile duct lesions in patients with chronic hepatitis C: Absence of influence of HCV genotype, HCV-RNA serum levels, and HGV infection on this histological damage. Dig Dis Sci. 2001; 46(3):524-9. [DOI:10.1023/A:1005534929304] [PMID]
- Hwang SJ, Luo JC, Lai CR, Chu CW, Tsay SH, Lu CL, et al. Clinical, virologic and pathologic significance of elevated serum gamma-glutamyl transpeptidase in patients with chronic hepatitis C. Zhonghua Yi Xue Za Zhi (Taipei). 2000; 63(7):527-35. [PMID]
- Babekir A, Mostafa S, Minor RC, Williams LL, Harrison SH, Obeng-Gyasi E. The Association of Toxoplasma gondii IgG and Liver Injury in US Adults. Int J Environ Res Public Health. 2022; 19(12):7515. [DOI:10.3390/ijerph19127515] [PMID]
- Sukthana Y, Waree P, Pongponratn E, Chaisri U, Riganti M. Pathologic study of acute toxoplasmosis in experimental animals. Southeast Asian J Trop Med Public Health. 2003; 34(1):16-21. [PMID]
- Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004; 363(9425):1965-76. [DOI:10.1016/S0140-6736(04)16412-X] [PMID]
- Al Mofarreh MA, Al Akwaa AY, Al Mofleh IA. Gammaglutamyl transpeptidase activity in patients with schistosomiasis. Saudi J Gastroenterol. 2003; 9(1):15-9. [PMID]
- Shrimali RG, Patel MD, Patel RM. Comparative efficacy of anthelmintics and their effects on hemato-biochemical changes in fasciolosis of goats of South Gujarat. Vet World. 2016; 9(5):524-9. [DOI:10.14202/vetworld.2016.524-529] [PMID]
- Latt N, Alachkar N, Gurakar A. Hepatitis C virus and its renal manifestations: A review and update. Gastroenterol. Hepatol. (N Y). 2012; 8(7):434-45. [PMID]
- Fabrizi F, Messa P. The epidemiology of HCV infection in patients with advanced CKD/ESRD: A global perspective. Semin Dial. 2019; 32(2):93-8. [DOI:10.1111/sdi.12757] [PMID]
- Imarenezor EPK, Iyamu MI, Nmorsi O, Godwin P. Interleukin (IL) - 1α, IL - 7 and IL - 13 profiles among enwan community, Edo State, Nigeria with Schistosoma haematobium infection. Int Res J Med Med Sci. 2017; 4(3):21-5. [DOI:10.30918/IRJMMS.51.17.013]
- Naqvi R, Ahmad E, Akhtar F, Naqvi A, Rizvi A. Outcome in severe acute renal failure associated with malaria. Nephrol Dial Transplant. 2003; 18(9):1820-3. [DOI:10.1093/ndt/gfg260] [PMID]
- Madwar MA, Voller A. Circulating soluble antigens and antibody in schistosomiasis. Br Med J. 1975; 1(5955):435-6. [DOI:10.1136/bmj.1.5955.435] [PMID]
- Jassim A, Catty D, Hassan K. Antibody isotypes of immune complexes in schistosomiasis mansoni in Sudan. Parasite Immunol. 1987; 9(6):651-65. [DOI:10.1111/j.1365-3024.1987.tb00536.x] [PMID]
- Da Silva GB, Duarte DB, Barros EJG, Daher EDF. Schistosomiasisassociated kidney disease: A review. Asian Pac J Trop Dis. 2013; 3(1):79-84. [DOI:10.1016/S2222-1808(13)60018-3]
- Dincel GC, Atmaca HT. Role of oxidative stress in the pathophysiology of Toxoplasma gondii infection. Int J Immunopathol Pharmacol. 2016; 29(2):226-40.[DOI:10.1177/0394632016638668] [PMID]
- Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative Stress: Harms and benefits for human health. Oxid Med Cell Longev. 2017; 2017:8416763. [DOI:10.1155/2017/8416763] [PMID]
- Gianotti RJ, Cardenas A. Hyponatraemia and cirrhosis. Gastroenterol Rep (Oxf). 2014; 2(1):21-6. [DOI:10.1093/gastro/got037] [PMID]
- Rizk M, Fayed TA, Badawy M, Sabaa El-Regal N Effect of different durations of Schistosoma mansoni infection on the levels of some antioxidants in mice. Trend Med Res. 2006; 1(1):66-74. [DOI:10.3923/tmr.2006.66.74]
- Matzner N, Zemtsova IM, Nguyen TX, Duszenko M, Shumilina E, Lang F. Ion channels modulating mouse dendritic cell functions. J Immunol. 2008; 181(10):6803-9. [DOI:10.4049/jimmunol.181.10.6803] [PMID]
- Reeves EP, Lu H, Jacobs HL, Messina CG, Bolsover S, Gabella G, et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature. 2002; 416(6878):291-7. [DOI:10.1038/416291a] [PMID]
- Eriksen PL, Vilstrup H, Rigbolt K, Suppli MP, Sørensen M, Heebøll S, et al. Non-alcoholic fatty liver disease alters expression of genes governing hepatic nitrogen conversion. Liver Int. 2019; 39(11):2094-101. [DOI:10.1111/liv.14205] [PMID]
- Richette P, Bardin T. Gout. Lancet. 2010; 375(9711):318-28. [DOI:10.1016/S0140-6736(09)60883-7] [PMID]
- Hediger MA, Johnson RJ, Miyazaki H, Endou H. Molecular physiology of urate transport. Physiology (Bethesda). 2005; 20:125-33. [DOI:10.1152/physiol.00039.2004] [PMID]
- Prasad Sah OS, Qing YX. Associations Between Hyperuricemia and Chronic Kidney Disease: A Review. Nephrourol Mon. 2015; 7(3):e27233. [DOI:10.5812/numonthly.7(3)2015.27233] [PMID]
- Al-Jowari S, Hussein D. Effect of toxoplasmosis infection on liver and kidney functions among pregnant women in Abo-Gharib district-Iraq. Iraqi J Sci. 2014; 55(1):101-5. [Link]
- Daher EF, da Silva Junior GB, Trivedi M, Fayad T, Srisawat N, Nair S, et al. Kidney complications of parasitic diseases. Nat Rev Nephrol. 2022; 18(6):396-406. [DOI:10.1038/s41581-022-00558-z] [PMID]
|