Status of anti-HEV IgG and IgM antibodies among the hemodialysis patients in southwest region of Iran
-
Roya Pirmoradi
,
Manoochehr Makvandi
,
Azadeh Haghi Navand
,
Shokouh Shayanpour
,
Heshmatolah Shahbazian
,
Kimia Makvandi
,
Saeed Eynali Varnosfaderani
,
Sepideh Nasimzadeh
Abstract
Background and Objectives: Hepatitis E Virus (HEV) account for acute hepatitis, fulminant liver failure and chronic hepatitis worldwide. Several high risk groups including hemodialysis (HD) patients are at risk of HEV infection. Based on consequences of HEV infection it is important to determine the serological and molecular epidemiology of HEV in HD patients. The aim of this study was to evaluate the frequency of HEV antibodies and HEV RNA in HD patients.
Materials and Methods: The sera of 84 HD patients were collected and tested for anti- HEV IgG and anti IgM antibodies using enzyme-linked immunosorbent assay (ELISA) at Golestan hospital in Ahvaz city during October 2014 and November 2014. HEV RNA was tested in HD patients using RT PCR. The prevalence of anti- HEV IgG was evaluated in the age group (52/84) > 50 and (31/84) < 50 years.
Results: Out of 84 patients, 52 (61.9%) were males and 32 (38.1%) females. The mean age of participants was 52 ± 1.57 years. 43/84 (51.19%) cases including 26/52 (50%) males and 17/32 (53.1%) females were positive for anti-HEV IgG (p=0.95). Among the 43 cases positive anti-HEV IgG 8 cases including 5 (9.61%) males and 3 (9.37%) females tested positive for anti-HEV IgM (p=0.729) while the HEV RNA was negative in HD patients. The distribution of anti- HEV IgG was 62.75% and 33.33% among the age group >50 and <50 respectively (p=0.015).
Conclusion: This study showed high prevalence of anti-HEV IgG antibodies (51.19%) were observed among the HD patients while the HEV RNA tested negative in HD patients. The rate of HEV IgG is significantly higher with increased age. Further investigation require to identify the factors account for high seroprevalence of HEV in Ahvaz HD units.
1. Wedemeyer H, Pischke S, Manns MP. Pathogenesis and treatment of hepatitis e virus infection. Gastroenterology 2012; 142: 1388-1397.e1.
2. Kraef C, Schlein C, Hiller J, Westhölter D, Denzer U, Horvatits T, Peine S, Lohse AW, Lütgehetmann M, Polywka S, Pischke S. Course of HEV viremia and anti-HEV IgM/IgG response in asymptomatic blood donors. J Clin Virol 2018;105:26-30.
3. Riezebos-Brilman A, Puchhammer-Stöckl E, van der Weide HY, Haagsma EB, Jaksch P, Bejvl I, et al. Chronic hepatitis E infection in lung transplant recipients. J Heart Lung Transplant 2013; 32: 341-346.
4. Halac U, Béland K, Lapierre P, Patey N, Ward P, Brassard J, et al. Chronic hepatitis E infection in children with liver transplantation. Gut 2012; 61: 579-603.
5. Schlosser B, Stein A, Neuhaus R, Pahl S, Ramez B, Kruger DH, et al. Liver transplant from a donor with occult HEV infection induced chronic hepatitis and cirrhosis in the recipient. J Hepatol 2012; 56: 500-502.
6. Cheung MC, Maguire J, Carey I, Wendon J, Agarwal K. Review of the neurological manifestations of hepatitis E infection. Ann Hepatol 2012; 11: 618-622.
7. Aggarwal R. Hepatitis E: clinical presentation in disease-endemic areas and diagnosis. Semin Liver Dis 2013; 33: 30-40.
8. Nimgaonkar I, Ding Q, Schwartz RE, Ploss A. Hepatitis E virus: advances and challenges. Nat Rev
Gastroenterol Hepatol 2018; 15: 96-110.
9. Smith DB, Simmonds P, Jameel S, Emerson SU, Harrison TJ, Meng X-J, et al. Consensus proposals for classification of the family Hepeviridae. J Gen Virol 2014; 95: 2223-2232.
10. Nair VP, Anang S, Subramani C, Madhvi A, Bakshi K, Srivastava A, et al. Endoplasmic reticulum stress induced synthesis of a novel viral factor mediates efficient replication of genotype-1 hepatitis E virus. PLoS Pathog 2016; 12(4): e1005521.
11. Lee G-H, Tan B-H, Teo EC-Y, Lim S-G, Dan Y-Y, Wee A, et al. Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology 2016; 150(2):355-357.e3.
12. Sridhar S, Lo SK, Xing F, Yang J, Ye H, Chan JF et al. Clinical characteristics and molecular epidemiology of hepatitis E in Shenzhen, China: a shift toward foodborne transmission of hepatitis E virus infection. Emerg Microbes Infect 2017; 6(12): e115.
13. Woo PCY, Lau SKP, Teng JLL, Tsang AKL, Joseph M, Wong EYM, et al. New hepatitis E virus genotype in camels, the Middle East. Emerg Infect Dis 2014; 20: 1044-1048.
14. Woo PCY, Lau SKP, Teng JLL, Cao K-Y, Wernery U, Schountz T, et al. New hepatitis E virus genotype in Bactrian camels, Xinjiang, China, 2013. Emerg Infect Dis 2016; 22: 2219-2221.
15. Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J. Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 2012; 50: 2708-2713.
16. Baylis SA, Gärtner T, Nick S, Ovemyr J, Blümel J. Occurrence of hepatitis E virus RNA in plasma donations from Sweden, Germany and the United States. Vox Sang 2012; 103: 89-90.
17. Gotanda Y, Iwata A, Ohnuma H, Yoshikawa A, Mizoguchi H, Endo K, et al. Ongoing subclinical infection of hepatitis E virus among blood donors with an elevated alanine aminotransferase level in Japan. J Med Virol 2007; 79: 734-742.
18. Intharasongkroh D, Thongmee T, Sa-Nguanmoo P, Klinfueng S, Duang-In A, Wasitthankasem R, et al. Hepatitis E virus infection in Thai blood donors. Transfusion 2019; 59: 1035-1043.
19. Katiyar H, Goel A, Sonker A, Yadav V, Sapun S, Chaudhary R, et al. Prevalence of hepatitis E virus viremia and antibodies among healthy blood donors in India. Indian J Gastroenterol 2018, 37: 342-346.
20. Huang S, Zhang X, Jiang H, Yan Q, Ai X, Wang Y, et al. Profile of acute infectious markers in sporadic hepatitis E. PLoS One 2010; 5(10): e13560.
21. Kamar N, Dalton HR, Abravanel F, Izopet J. Hepatitis E virus infection. Clin Microbiol Rev 2014; 27: 116-138.
22. Alavian SM, Ataei B, Ebrahimi A, Pirhaji O, Azad R, Olya B, et al. Anti-hepatitis E antibody in hemodialysis patients in Isfahan, Iran: prevalence and risk factors. Hepat Mon 2015; 15(9): e23633.
23. Zekavat OR, Makarem A, Karami MY, Amanat A, Mohandes M, Habibagahi M. Serological investigation for hepatitis E virus infection in the patients with chronic maintenance hemodialysis from southwest of Iran. Asian J Transfus Sci 2013; 7: 21-25.
24. Parsa R, Adibzadeh S, Behzad Behbahani A, Farhadi A, Yaghobi R, Rafiei Dehbidi GR, et al. Detection of hepatitis E virus genotype 1 among blood donors from southwest of Iran. Hepat Mon 2016; 16(6): e34202.
25. Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H. Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods 2006; 137: 325-333.
26. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, et al. Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol 2002; 40: 1326-1332.
27. Pisano MB, Balderramo D, Wassaf MM, Lotto M, Carlino Y, Re VE, et al. Hepatitis E virus infection in patients on dialysis and in solid organ transplant recipients in Argentina: exploring associated risk factors. Arch Virol 2017; 162: 787-792.
28. Harrison A, Scobie L, Crossan C, Parry R, Johnston P, Stratton J, et al. Hepatitis E seroprevalence in recipients of renal transplants or haemodialysis in southwest England: a case-control study. J Med Virol 2013; 85: 266-271.
29. Ismail MB, Al Kassaa I, El Safadi D, Al Omari S, Mallat H, Dabboussi F, et al. Prevalence of anti-hepatitis E virus IgG antibodies in sera from hemodialysis patients in Tripoli, Lebanon. PLoS One 2020; 15(5):e0233256.
30. Mrzljak A, Dinjar-Kujundzic P, Knotek M, Kudumija B, Ilic M, Gulin M, et al. Seroepidemiology of hepatitis E in patients on haemodialysis in Croatia. Int Urol Nephrol 2020; 52: 371-378.
31. Scotto G, Aucella F, Grandaliano G, Martinelli D, Querques M, Gesuete A, et al. Hepatitis E in hemodialysis and kidney transplant patients in south-east Italy. World J Gastroenterol 2015; 21: 3266-3273.
32. Crossan C, Scobie L, Godwin J, Hunter JG, Hawkes T, Dalton HR. Hepatitis E virus and porcine-derived heparin. Emerg Infect Dis 2013; 19: 686-688.
33. Hirth RA, Turenne MN, Wilk AS, Wheeler JR, Sleeman KK, Zhang W, et al. Blood transfusion practices in dialysis patients in a dynamic regulatory environment. Am J Kidney Dis 2014; 64: 616-621.
34. Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J. Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 2012; 50: 2708-2713.
35. Gallian P, Couchouron A, Dupont I, Fabra C, Piquet Y, Djoudi R, et al. Comparison of hepatitis E virus nucleic acid test screening platforms and RNA prevalence in French blood donors. Transfusion 2017; 57: 223-224.
36. Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaaijer HL. Silent hepatitis E virus infection in Dutch blood donors, 2011 to 2012. Euro Surveill 2013; 18: 20550.
37. Hewitt PE, Ijaz S, Brailsford SR, Brett R, Dicks S, Haywood B, et al. Hepatitis E virus in blood components: a prevalence and transmission study in Southeast England. Lancet 2014; 384: 1766-1773.
38. Auleda S, Ong E, Bes M, Janssen A, Cory R, Babizki M, et al. Seroprevalence of hepatitis E virus (HEV) and detection of HEV RNAwith a transcription-mediated amplification assay in blood donors from Catalonia (Spain). Transfusion 2015; 55: 972-929.
39. Domanović D, Tedder R, Blümel J, Zaaijer H, Gallian P, Niederhauser C, et al. Hepatitis E and blood donation safety in selected European countries: a shift to screening? Euro Surveill 2017; 22: 30514.
40. Hazam RK, Singla R, Kishore J, Singh S, Gupta RK, Kar P. Surveillance of hepatitis E virus in sewage and drinking water in a resettlement colony of Delhi: what has been the experience? Arch Virol 2010; 155: 1227-1233.
41. Tripathy AS, Sharma M, Deoshatwar AR, Babar P, Bharadwaj R, Bharti OK. Study of a hepatitis E virus outbreak involving drinking water and sewage contamination in Shimla, India, 2015–2016. Trans R Soc Trop Med Hyg 2019; 113: 789-796.
42. La Rosa G, Proroga YTR, De Medici D, Capuano F, Iaconelli M, Della Libera S, et al. First detection of hepatitis E virus in shellfish and in seawater from production areas in Southern Italy. Food Environ Virol 2018; 10: 127-131.
43. Grodzki M, Schaeffer J, Piquet JC, Le Saux JC, Chevé J, Ollivier J, et al. Bioaccumulation efficiency, tissue distribution, and environmental occurrence of hepatitis E virus in bivalve shellfish from France. Appl Environ Microbiol 2014; 80: 4269-4276.
44. Cui W, Sun Y, Xu A, Gao R, Gong L, Zhang L, et al. Hepatitis E seroprevalence and related risk factors among seafood processing workers: a cross-sectional survey in Shandong Province, China. Int J Infect Dis 2016; 49:62-66.
2. Kraef C, Schlein C, Hiller J, Westhölter D, Denzer U, Horvatits T, Peine S, Lohse AW, Lütgehetmann M, Polywka S, Pischke S. Course of HEV viremia and anti-HEV IgM/IgG response in asymptomatic blood donors. J Clin Virol 2018;105:26-30.
3. Riezebos-Brilman A, Puchhammer-Stöckl E, van der Weide HY, Haagsma EB, Jaksch P, Bejvl I, et al. Chronic hepatitis E infection in lung transplant recipients. J Heart Lung Transplant 2013; 32: 341-346.
4. Halac U, Béland K, Lapierre P, Patey N, Ward P, Brassard J, et al. Chronic hepatitis E infection in children with liver transplantation. Gut 2012; 61: 579-603.
5. Schlosser B, Stein A, Neuhaus R, Pahl S, Ramez B, Kruger DH, et al. Liver transplant from a donor with occult HEV infection induced chronic hepatitis and cirrhosis in the recipient. J Hepatol 2012; 56: 500-502.
6. Cheung MC, Maguire J, Carey I, Wendon J, Agarwal K. Review of the neurological manifestations of hepatitis E infection. Ann Hepatol 2012; 11: 618-622.
7. Aggarwal R. Hepatitis E: clinical presentation in disease-endemic areas and diagnosis. Semin Liver Dis 2013; 33: 30-40.
8. Nimgaonkar I, Ding Q, Schwartz RE, Ploss A. Hepatitis E virus: advances and challenges. Nat Rev
Gastroenterol Hepatol 2018; 15: 96-110.
9. Smith DB, Simmonds P, Jameel S, Emerson SU, Harrison TJ, Meng X-J, et al. Consensus proposals for classification of the family Hepeviridae. J Gen Virol 2014; 95: 2223-2232.
10. Nair VP, Anang S, Subramani C, Madhvi A, Bakshi K, Srivastava A, et al. Endoplasmic reticulum stress induced synthesis of a novel viral factor mediates efficient replication of genotype-1 hepatitis E virus. PLoS Pathog 2016; 12(4): e1005521.
11. Lee G-H, Tan B-H, Teo EC-Y, Lim S-G, Dan Y-Y, Wee A, et al. Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology 2016; 150(2):355-357.e3.
12. Sridhar S, Lo SK, Xing F, Yang J, Ye H, Chan JF et al. Clinical characteristics and molecular epidemiology of hepatitis E in Shenzhen, China: a shift toward foodborne transmission of hepatitis E virus infection. Emerg Microbes Infect 2017; 6(12): e115.
13. Woo PCY, Lau SKP, Teng JLL, Tsang AKL, Joseph M, Wong EYM, et al. New hepatitis E virus genotype in camels, the Middle East. Emerg Infect Dis 2014; 20: 1044-1048.
14. Woo PCY, Lau SKP, Teng JLL, Cao K-Y, Wernery U, Schountz T, et al. New hepatitis E virus genotype in Bactrian camels, Xinjiang, China, 2013. Emerg Infect Dis 2016; 22: 2219-2221.
15. Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J. Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 2012; 50: 2708-2713.
16. Baylis SA, Gärtner T, Nick S, Ovemyr J, Blümel J. Occurrence of hepatitis E virus RNA in plasma donations from Sweden, Germany and the United States. Vox Sang 2012; 103: 89-90.
17. Gotanda Y, Iwata A, Ohnuma H, Yoshikawa A, Mizoguchi H, Endo K, et al. Ongoing subclinical infection of hepatitis E virus among blood donors with an elevated alanine aminotransferase level in Japan. J Med Virol 2007; 79: 734-742.
18. Intharasongkroh D, Thongmee T, Sa-Nguanmoo P, Klinfueng S, Duang-In A, Wasitthankasem R, et al. Hepatitis E virus infection in Thai blood donors. Transfusion 2019; 59: 1035-1043.
19. Katiyar H, Goel A, Sonker A, Yadav V, Sapun S, Chaudhary R, et al. Prevalence of hepatitis E virus viremia and antibodies among healthy blood donors in India. Indian J Gastroenterol 2018, 37: 342-346.
20. Huang S, Zhang X, Jiang H, Yan Q, Ai X, Wang Y, et al. Profile of acute infectious markers in sporadic hepatitis E. PLoS One 2010; 5(10): e13560.
21. Kamar N, Dalton HR, Abravanel F, Izopet J. Hepatitis E virus infection. Clin Microbiol Rev 2014; 27: 116-138.
22. Alavian SM, Ataei B, Ebrahimi A, Pirhaji O, Azad R, Olya B, et al. Anti-hepatitis E antibody in hemodialysis patients in Isfahan, Iran: prevalence and risk factors. Hepat Mon 2015; 15(9): e23633.
23. Zekavat OR, Makarem A, Karami MY, Amanat A, Mohandes M, Habibagahi M. Serological investigation for hepatitis E virus infection in the patients with chronic maintenance hemodialysis from southwest of Iran. Asian J Transfus Sci 2013; 7: 21-25.
24. Parsa R, Adibzadeh S, Behzad Behbahani A, Farhadi A, Yaghobi R, Rafiei Dehbidi GR, et al. Detection of hepatitis E virus genotype 1 among blood donors from southwest of Iran. Hepat Mon 2016; 16(6): e34202.
25. Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H. Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods 2006; 137: 325-333.
26. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, et al. Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol 2002; 40: 1326-1332.
27. Pisano MB, Balderramo D, Wassaf MM, Lotto M, Carlino Y, Re VE, et al. Hepatitis E virus infection in patients on dialysis and in solid organ transplant recipients in Argentina: exploring associated risk factors. Arch Virol 2017; 162: 787-792.
28. Harrison A, Scobie L, Crossan C, Parry R, Johnston P, Stratton J, et al. Hepatitis E seroprevalence in recipients of renal transplants or haemodialysis in southwest England: a case-control study. J Med Virol 2013; 85: 266-271.
29. Ismail MB, Al Kassaa I, El Safadi D, Al Omari S, Mallat H, Dabboussi F, et al. Prevalence of anti-hepatitis E virus IgG antibodies in sera from hemodialysis patients in Tripoli, Lebanon. PLoS One 2020; 15(5):e0233256.
30. Mrzljak A, Dinjar-Kujundzic P, Knotek M, Kudumija B, Ilic M, Gulin M, et al. Seroepidemiology of hepatitis E in patients on haemodialysis in Croatia. Int Urol Nephrol 2020; 52: 371-378.
31. Scotto G, Aucella F, Grandaliano G, Martinelli D, Querques M, Gesuete A, et al. Hepatitis E in hemodialysis and kidney transplant patients in south-east Italy. World J Gastroenterol 2015; 21: 3266-3273.
32. Crossan C, Scobie L, Godwin J, Hunter JG, Hawkes T, Dalton HR. Hepatitis E virus and porcine-derived heparin. Emerg Infect Dis 2013; 19: 686-688.
33. Hirth RA, Turenne MN, Wilk AS, Wheeler JR, Sleeman KK, Zhang W, et al. Blood transfusion practices in dialysis patients in a dynamic regulatory environment. Am J Kidney Dis 2014; 64: 616-621.
34. Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J. Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 2012; 50: 2708-2713.
35. Gallian P, Couchouron A, Dupont I, Fabra C, Piquet Y, Djoudi R, et al. Comparison of hepatitis E virus nucleic acid test screening platforms and RNA prevalence in French blood donors. Transfusion 2017; 57: 223-224.
36. Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaaijer HL. Silent hepatitis E virus infection in Dutch blood donors, 2011 to 2012. Euro Surveill 2013; 18: 20550.
37. Hewitt PE, Ijaz S, Brailsford SR, Brett R, Dicks S, Haywood B, et al. Hepatitis E virus in blood components: a prevalence and transmission study in Southeast England. Lancet 2014; 384: 1766-1773.
38. Auleda S, Ong E, Bes M, Janssen A, Cory R, Babizki M, et al. Seroprevalence of hepatitis E virus (HEV) and detection of HEV RNAwith a transcription-mediated amplification assay in blood donors from Catalonia (Spain). Transfusion 2015; 55: 972-929.
39. Domanović D, Tedder R, Blümel J, Zaaijer H, Gallian P, Niederhauser C, et al. Hepatitis E and blood donation safety in selected European countries: a shift to screening? Euro Surveill 2017; 22: 30514.
40. Hazam RK, Singla R, Kishore J, Singh S, Gupta RK, Kar P. Surveillance of hepatitis E virus in sewage and drinking water in a resettlement colony of Delhi: what has been the experience? Arch Virol 2010; 155: 1227-1233.
41. Tripathy AS, Sharma M, Deoshatwar AR, Babar P, Bharadwaj R, Bharti OK. Study of a hepatitis E virus outbreak involving drinking water and sewage contamination in Shimla, India, 2015–2016. Trans R Soc Trop Med Hyg 2019; 113: 789-796.
42. La Rosa G, Proroga YTR, De Medici D, Capuano F, Iaconelli M, Della Libera S, et al. First detection of hepatitis E virus in shellfish and in seawater from production areas in Southern Italy. Food Environ Virol 2018; 10: 127-131.
43. Grodzki M, Schaeffer J, Piquet JC, Le Saux JC, Chevé J, Ollivier J, et al. Bioaccumulation efficiency, tissue distribution, and environmental occurrence of hepatitis E virus in bivalve shellfish from France. Appl Environ Microbiol 2014; 80: 4269-4276.
44. Cui W, Sun Y, Xu A, Gao R, Gong L, Zhang L, et al. Hepatitis E seroprevalence and related risk factors among seafood processing workers: a cross-sectional survey in Shandong Province, China. Int J Infect Dis 2016; 49:62-66.
| Files | ||
| Issue | Vol 14 No 5 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i5.10972 | |
| Keywords | ||
| Hepatitis E virus; Hemodialysis patients; Enzyme-linked immunosorbent assay | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Pirmoradi R, Makvandi M, Haghi Navand A, Shayanpour S, Shahbazian H, Makvandi K, Eynali Varnosfaderani S, Nasimzadeh S. Status of anti-HEV IgG and IgM antibodies among the hemodialysis patients in southwest region of Iran. Iran J Microbiol. 2022;14(5):759-764.
