Published online Feb 14, 2009. doi: 10.3748/wjg.15.641
Revised: July 15, 2008
Accepted: July 22, 2008
Published online: February 14, 2009
Hepatitis C virus (HCV) infection is highly prevalent among patients on hemodialysis (HD). The prevalence of HCV infection in HD patients varies markedly from country to country. Some factors are especially related to these high prevalence rates, such as blood transfusions and length of dialysis time. Nosocomial routes of transmission including the use of contaminated equipment and patient-to-patient exposure is considered more important. Several prophylactic measures have been suggested to avoid infection by HCV in the HD environment.
- Citation: Alavian SM. A shield against a monster: Hepatitis C in hemodialysis patients. World J Gastroenterol 2009; 15(6): 641-646
- URL: https://www.wjgnet.com/1007-9327/full/v15/i6/641.htm
- DOI: https://dx.doi.org/10.3748/wjg.15.641
Hepatitis C virus (HCV) infection is considered a major public health problem worldwide. Patients with chronic renal failure who are on hemodialysis (HD) have a high prevalence of HCV. They are among the highest risk groups for the acquisition of HCV infection[1–3]. Prevalence of HCV infection has decreased in this group in recent years[4], but still remains a significant public health concern. HCV-infected patients on HD have significant liver disease and a decreased life expectancy[56]. The relative risk for death in HCV-infected patients on HD compared with non-infected patients is greater than 1.4[6–8]. In addition, HCV infection leads to decreased graft and patient survival in renal transplant recipients[910]. On the other hand, due to the increased prevalence of non-communicable diseases such as diabetes mellitus and hypertension, and their complications, chronic renal failure has become a more serious health issue throughout the world[11]. Therefore, the clinical importance of HCV has been increasingly recognized in the dialysis community.
HCV prevalence in HD varies geographically, both within and between countries[12]. The reported anti-HCV seropositivity since 1999 ranges from low (1.9%) in the Slovenian 2001 Annual Report[13] to high (80%) in Senegal[14]. HCV seroprevalence in the HD population was 59% in Bosnia and Herzegovina[15] , 6.8% in Belgium[16], 16.3% in France[2], 6.1% in Germany[17], 10%-29% in Greece[18–20], 22.5%-32.1% in Italy[2122], 75% in Moldavia[23], 3.4% in the Netherlands[24], 1.9% in Slovenia[13], 11% in Sweden[25], 7%-23.3% in the USA[26–30], 4% in the UK[31] 20.5% in Libya[32], 71% in Kuwait[31] 80% in Senegal[14], 23.7% in Sudan[33], 19%-41.7% in Tunisia[3435], 8.4%-43.2% in Brazil[36–39], 6.7% in Mexico[40], 59.3% in Peru[41], 3.5% in Puerto Rico[42] and 13.2% in Iran[43]. Some investigators have suggested a decline in HCV prevalence among HD patients in recent years, mostly attributable to strict adherence to universal precautions with[1644–49] or without[5051] observing isolation measures. This decrease is more significant in the USA and European countries[4164752]. Studies that have prospectively followed HD patients for their HCV serostatus have yielded annual incidence rates of de novo HCV infection of 0.4% in France[53], 0.5% in Tunisia[54], 0.5% in the Netherlands[24], 0.83% in Italy[55], 1.38%[56] and 2.1%[57] in the USA, 0.33%[58], 2.59%[59], 3.1% in Japan[60], 3.7%[61] 5.5% in Brazil[62], and 6.2% in Greece[20]. This variation in different countries and different centers underlines the importance of infection control. New infection was evidently more frequent at centers that had higher anti-HCV prevalence and failure in infection control measures. In some countries, both prevalence and incidence remain very high, indicating major ongoing nosocomial transmission, probably due to the limited resources available to treat a rapidly growing HD population[6364].
The high prevalence of HCV seropositivity among HD patients was initially attributed to blood transfusions for the treatment of uremic anemia in this population, which were often necessary[4165–68]. Historically, the number of blood transfusions received was consistently reported in the literature to be associated with an increased prevalence of HCV-positive dialysis patients[31]. However, several recent reports have failed to recognize blood transfusion as an independent risk factor in HCV spread among HD subjects[220232430336269–74]. Indeed, from the late 1980s onward, the prescription of erythropoietin reduced the need for blood transfusion in HD patients. Furthermore, the introduction of sensitive tests for screening blood donors has markedly reduced the risk of HCV transmission through blood product transfusion. These two reasons may explain recent findings on the lack of association between blood transfusion and HCV infection. Nonetheless, considering the fact that new HCV infections do still occur in patients without a history of transfusion, the duration of HD is increasingly being considered as a risk factor for HCV infection[7576]. Almost all recent surveys on the subject have congruently suggested that the length of time on HD is a risk factor for HCV seropositivity[1720232930333639436069–7177–80]. Nosocomial patient-to-patient transmission of HCV infection among HD patients has been suggested by several investigators who performed phylogenetic analysis of HCV viral isolates[2425535481–84]. Lack of strict adherence to universal precautions by staff and sharing of articles such as multidose drugs might be the main mode of nosocomial HCV spread among HD patients[548284–86]. Although some studies found that nosocomial spread of HCV declined when HCV-infected patients were treated in dedicated HD units[44–498788], other investigators could control nosocomial spread of HCV among HD patients by the strict application of hygienic precautions, without isolation of HCV-infected subjects or machine segregation[125089]. Indeed, the observed efficacy of isolation might simply be due to the prevented sharing of articles between patients and might reflect a better implementation of other hygienic precautions.
The spread of HCV infection in HD units is mainly due to nosocomial transmission between patients[538890–94]. The importance of this route of transmission is demonstrated by the high HCV prevalence in some HD units and by the lower infection rate in patients on peritoneal dialysis compared with those on HD. A high prevalence of patients with HCV infection in HD facilities has been considered a risk factor for transmission of the infection. However, there is no consensus on the necessity for infection control isolation of HCV-positive patients for at least two reasons: firstly, the infectivity of HCV is lower than that of the hepatitis B virus; and secondly, the criteria for patients to be isolated remain to be defined. On the contrary, some HD patients are infected with HCV but do not have antibodies. Detection of viral RNA by reverse-transcription polymerase chain reaction (RT-PCR) is the only method to confirm HCV infection, however, this technique is not available at all centers.
Several prophylactic measures have been suggested to avoid infection by HCV in the HD environment, and range from isolating patients with HCV infection[4447488895], to adopting a series of biosafety measures specific for HD, such as preparing medications in a separate area, cleaning and disinfecting dialysis station surfaces, washing hands and changing gloves between patient contacts, and items dedicated for use only with a single patient[12395096]. Strict adherence to universal infection control precautions seems to be enough to control the spread of disease in HD units[12508997–99]. Some reports have recommended the adoption of infection control isolation measures at centers with a high HCV prevalence[4787100101] or if the staff/patient ratio at the center is lower than 28/100[102]. At centers with a high prevalence of HCV infection and in developing countries, universal precautions may not always be possible to implement. Thus isolation measures for HCV-positive patients should be implemented[47]. The CDC recommends that special precautions be observed in dialysis units including the wearing and changing of gloves and water-proof gowns between patients; systematic decontamination of the equipment, circuits, and surfaces after each patient treatment; no sharing of instruments (e.g. tourniquets) or medications (e.g. multiuse vials of heparin) among patients; and the assignment of patients to specific HD units[97]. Clearly, it is necessary to attempt, one step at a time, to minimize intradialytic or intracenter HCV transmission.
In summary, despite the marked decrease in anti-HCV prevalence in HD patients in many countries, the disappearance of HCV from HD units should not be expected for decades. Universal infection control precautions are the keystone in the prevention of nosocomial HCV transmission in HD units; however, isolation measures, including health care monitoring of infected patients and providing care in a dedicated section of the unit, improve prevention results. Those HD units with a high HCV prevalence or in which there is no fulltime infection control personnel dedicated to the infected patients during HD sessions may have a greater risk of seroconversion. Therefore, isolation in special units or dialyzing patients in specific sessions must be considered[44]. As HCV-infected HD patients serve as a reservoir of infection for other patients, HD staff, and the transplant team[28103104] at HD centers must be aware of new HCV infections in order to review their practices and increase vigilance. Public health authorities should be aware about the prevalence and incidence of HCV infection in HD patients in different cities in their respective countries, so that changes can be proposed and the risks of infection among patients can be assessed. Implementation of surveillance systems and continuing education of the unit’s personnel on recommended infection control measures in HD units are necessary. The treatment of most HCV-infected patients with interferon alpha can significantly contribute to decreasing HCV infection in this group in the future[105]. Successful control of infection requires further studies to assess the effectiveness of different preventive policies.
1. | Barril G. Hepatitis C virus-induced liver disease in dialysis patients. Nephrol Dial Transplant. 2000;15 Suppl 8:42-45. |
2. | Salama G, Rostaing L, Sandres K, Izopet J. Hepatitis C virus infection in French hemodialysis units: a multicenter study. J Med Virol. 2000;61:44-51. |
3. | Alavian SM, Hosseini-Moghaddam SM, Rahnavardi M. Hepatitis C among hemodialysis patients: a review on epidemiologic, diagnostic, and therapeutic features. Hep Mon. 2007;7:153-162. |
4. | Espinosa M, Martn-Malo A, Ojeda R, Santamara R, Soriano S, Aguera M, Aljama P. Marked reduction in the prevalence of hepatitis C virus infection in hemodialysis patients: causes and consequences. Am J Kidney Dis. 2004;43:685-689. |
5. | Mathurin P, Mouquet C, Poynard T, Sylla C, Benalia H, Fretz C, Thibault V, Cadranel JF, Bernard B, Opolon P. Impact of hepatitis B and C virus on kidney transplantation outcome. Hepatology. 1999;29:257-263. |
6. | Stehman-Breen CO, Emerson S, Gretch D, Johnson RJ. Risk of death among chronic dialysis patients infected with hepatitis C virus. Am J Kidney Dis. 1998;32:629-634. |
7. | Pereira BJ, Natov SN, Bouthot BA, Murthy BV, Ruthazer R, Schmid CH, Levey AS. Effects of hepatitis C infection and renal transplantation on survival in end-stage renal disease. The New England Organ Bank Hepatitis C Study Group. Kidney Int. 1998;53:1374-1381. |
8. | Hanafusa T, Ichikawa Y, Kishikawa H, Kyo M, Fukunishi T, Kokado Y, Okuyama A, Shinji Y, Nagano S. Retrospective study on the impact of hepatitis C virus infection on kidney transplant patients over 20 years. Transplantation. 1998;66:471-476. |
9. | Gentil MA, Rocha JL, Rodríguez-Algarra G, Pereira P, López R, Bernal G, Muñoz J, Naranjo M, Mateos J. Impaired kidney transplant survival in patients with antibodies to hepatitis C virus. Nephrol Dial Transplant. 1999;14:2455-2460. |
10. | Knoll GA, Tankersley MR, Lee JY, Julian BA, Curtis JJ. The impact of renal transplantation on survival in hepatitis C-positive end-stage renal disease patients. Am J Kidney Dis. 1997;29:608-614. |
11. | Aghighi M, Heidary Rouchi A, Zamyadi M, Mahdavi-Mazdeh M, Norouzi S, Rajolani H, Ahrabi S, Zamani M. Dialysis in Iran. IJKD. 2008;2:11-15. |
12. | Jadoul M, Cornu C, van Ypersele de Strihou C. Universal precautions prevent hepatitis C virus transmission: a 54 month follow-up of the Belgian Multicenter Study. The Universitaires Cliniques St-Luc (UCL) Collaborative Group. Kidney Int. 1998;53:1022-1025. |
13. | Buturovic-Ponikvar J. Renal replacement therapy in Slovenia: annual report 2001. Nephrol Dial Transplant. 2003;18 Suppl 5:v53-v55. |
14. | Diouf ML, Diouf B, Niang A, Ka EH, Pouye A, Seck A, Raphenon G, Moreira-Diop T. [Prevalence of hepatitis B and C viruses in a chronic hemodialysis center in Dakar]. Dakar Med. 2000;45:1-4. |
15. | Ahmetagic S, Muminhodzic K, Cickusic E, Stojic V, Petrovic J, Tihic N. Hepatitis C infection in risk groups. Bosn J Basic Med Sci. 2006;6:13-17. |
16. | Jadoul M, Poignet JL, Geddes C, Locatelli F, Medin C, Krajewska M, Barril G, Scheuermann E, Sonkodi S, Goubau P. The changing epidemiology of hepatitis C virus (HCV) infection in haemodialysis: European multicentre study. Nephrol Dial Transplant. 2004;19:904-909. |
17. | Hinrichsen H, Leimenstoll G, Stegen G, Schrader H, Fölsch UR, Schmidt WE. Prevalence and risk factors of hepatitis C virus infection in haemodialysis patients: a multicentre study in 2796 patients. Gut. 2002;51:429-433. |
18. | Rigopoulou EI, Stefanidis I, Liaskos C, Zervou EK, Rizos C, Mina P, Zachou K, Syrganis C, Patsidis E, Kyriakopoulos G. HCV-RNA qualitative assay based on transcription mediated amplification improves the detection of hepatitis C virus infection in patients on hemodialysis: results from five hemodialysis units in central Greece. J Clin Virol. 2005;34:81-85. |
19. | Garinis G, Spanakis N, Theodorou V, Gorgoulis V, Manolis E, Karameris A, Valis D. Comparison of the enzyme-linked immunosorbant assay III, recombinant immunoblot third generation assay, and polymerase chain reaction method in the detection of hepatitis C virus infection in haemodialysis patients. J Clin Lab Anal. 1999;13:122-125. |
20. | Sypsa V, Psichogiou M, Katsoulidou A, Skoutelis G, Moutafis S, Hadjiconstantinou V, Kakavas J, Kalapothaki V, Boletis J, Hatzakis A. Incidence and patterns of hepatitis C virus seroconversion in a cohort of hemodialysis patients. Am J Kidney Dis. 2005;45:334-343. |
21. | Lombardi M, Cerrai T, Geatti S, Negroni S, Pertusini L, Pegoraro M, Di Lullo G. Results of a national epidemiological investigation of HCV infection in dialysis patients. EDTNA ERCA J. 1999;25:38-42. |
22. | Petrosillo N, Gilli P, Serraino D, Dentico P, Mele A, Ragni P, Puro V, Casalino C, Ippolito G. Prevalence of infected patients and understaffing have a role in hepatitis C virus transmission in dialysis. Am J Kidney Dis. 2001;37:1004-1010. |
23. | Covic A, Iancu L, Apetrei C, Scripcaru D, Volovat C, Mititiuc I, Covic M. Hepatitis virus infection in haemodialysis patients from Moldavia. Nephrol Dial Transplant. 1999;14:40-45. |
24. | Schneeberger PM, Keur I, van Loon AM, Mortier D, de Coul KO, van Haperen AV, Sanna R, van Der Heijden TG, van Den Hoven H, van Hamersvelt HW. The prevalence and incidence of hepatitis C virus infections among dialysis patients in the Netherlands: a nationwide prospective study. J Infect Dis. 2000;182:1291-1299. |
25. | Almroth G, Ekermo B, Månsson AS, Svensson G, Widell A. Detection and prevention of hepatitis C in dialysis patients and renal transplant recipients. A long-term follow up (1989-January 1997). J Intern Med. 2002;251:119-128. |
26. | Kelley VA, Everett-Kitchens J, Brannon LE, Connor K, Martinez EJ, Pearson TC, Nolte FS. Lack of seronegative hepatitis C virus infections in patients with chronic renal failure. Transplantation. 2002;74:1473-1475. |
27. | Kalantar-Zadeh K, Miller LG, Daar ES. Diagnostic discordance for hepatitis C virus infection in hemodialysis patients. Am J Kidney Dis. 2005;46:290-300. |
28. | Saab S, Martin P, Brezina M, Gitnick G, Yee HF Jr. Serum alanine aminotransferase in hepatitis c screening of patients on hemodialysis. Am J Kidney Dis. 2001;37:308-315. |
29. | Kalantar-Zadeh K, Kilpatrick RD, McAllister CJ, Miller LG, Daar ES, Gjertson DW, Kopple JD, Greenland S. Hepatitis C virus and death risk in hemodialysis patients. J Am Soc Nephrol. 2007;18:1584-1593. |
30. | Sivapalasingam S, Malak SF, Sullivan JF, Lorch J, Sepkowitz KA. High prevalence of hepatitis C infection among patients receiving hemodialysis at an urban dialysis center. Infect Control Hosp Epidemiol. 2002;23:319-324. |
31. | Wreghitt TG. Blood-borne virus infections in dialysis units--a review. Rev Med Virol. 1999;9:101-109. |
32. | Daw MA, Elkaber MA, Drah AM, Werfalli MM, Mihat AA, Siala IM. Prevalence of hepatitis C virus antibodies among different populations of relative and attributable risk. Saudi Med J. 2002;23:1356-1360. |
33. | El-Amin HH, Osman EM, Mekki MO, Abderlraheem MB, Ismail MO, Yousif MEA, Abass A, Elhaj HS, Ammar HK. Hepatitis C virus infection in hemodialysis patients in Sudan:Two centers report. Saudi J Kidney Dis Transplant. 2007;18:101-106. |
34. | Bouzgarrou N, Fodha I, Othman SB, Achour A, Grattard F, Trabelsi A, Pozzetto B. Evaluation of a total core antigen assay for the diagnosis of hepatitis C virus infection in hemodialysis patients. J Med Virol. 2005;77:502-508. |
35. | Ayed K, Gorgi Y, Ben Abdallah T, Aouadi H, Jendoubi-Ayed S, Sfar I, Makni H. Hepatitis C virus infection in hemodialysis patients from Tunisia: national survey by serologic and molecular methods. Transplant Proc. 2003;35:2573-2575. |
36. | Albuquerque AC, Coêlho MR, Lopes EP, Lemos MF, Moreira RC. Prevalence and risk factors of hepatitis C virus infection in hemodialysis patients from one center in Recife, Brazil. Mem Inst Oswaldo Cruz. 2005;100:467-470. |
37. | Lopes EP, Gouveia EC, Albuquerque AC, Sette LH, Mello LA, Moreira RC, Coelho MR. Determination of the cut-off value of serum alanine aminotransferase in patients undergoing hemodialysis, to identify biochemical activity in patients with hepatitis C viremia. J Clin Virol. 2006;35:298-302. |
38. | Mello Lde A, de Melo-Junior MR, de Albuquerque AC, Coelho MR. [Hepatitis C serum prevalence in hemodialyzed patients]. Rev Soc Bras Med Trop. 2007;40:290-294. |
39. | Carneiro MA, Martins RM, Teles SA, Silva SA, Lopes CL, Cardoso DD, Vanderborght BO, Yoshida CF. Hepatitis C prevalence and risk factors in hemodialysis patients in Central Brazil: a survey by polymerase chain reaction and serological methods. Mem Inst Oswaldo Cruz. 2001;96:765-769. |
40. | Méndez-Sánchez N, Motola-Kuba D, Chavez-Tapia NC, Bahena J, Correa-Rotter R, Uribe M. Prevalence of hepatitis C virus infection among hemodialysis patients at a tertiary-care hospital in Mexico City, Mexico. J Clin Microbiol. 2004;42:4321-4322. |
41. | Sanchez JL, Sjogren MH, Callahan JD, Watts DM, Lucas C, Abdel-Hamid M, Constantine NT, Hyams KC, Hinostroza S, Figueroa-Barrios R. Hepatitis C in Peru: risk factors for infection, potential iatrogenic transmission, and genotype distribution. Am J Trop Med Hyg. 2000;63:242-248. |
42. | López-Navedo PJ, Lebrón-Rivera R, González-Trápaga J, Weber-Acevedo J, Lefevre-Ramos E, Flores-de Hostos E, Jaume-Anselmi F, Ramírez-Rivera J. Prevalence of hepatitis C virus infection at three hemodialysis units in the western region of Puerto Rico. Bol Asoc Med P R. 1999;91:100-102. |
43. | Alavian SM, Einollahi B, Hajarizadeh B, Bakhtiari S, Nafar M, Ahrabi S. Prevalence of hepatitis C virus infection and related risk factors among Iranian haemodialysis patients. Nephrology (Carlton). 2003;8:256-260. |
44. | Yang CS, Chang HH, Chou CC, Peng SJ. Isolation effectively prevents the transmission of hepatitis C virus in the hemodialysis unit. J Formos Med Assoc. 2003;102:79-85. |
45. | Gallego E, López A, Pérez J, Llamas F, Lorenzo I, López E, Illescas ML, Andrés E, Olivas E, Gómez-Roldan C. Effect of isolation measures on the incidence and prevalence of hepatitis C virus infection in hemodialysis. Nephron Clin Pract. 2006;104:c1-c6. |
46. | Carneiro MA, Teles SA, Dias MA, Ferreira RC, Naghettine AV, Silva SA, Lampe E, Yoshida CF, Martins RM. Decline of hepatitis C infection in hemodialysis patients in Central Brazil: a ten years of surveillance. Mem Inst Oswaldo Cruz. 2005;100:345-349. |
47. | Barril G, Traver JA. Decrease in the hepatitis C virus (HCV) prevalence in hemodialysis patients in Spain: effect of time, initiating HCV prevalence studies and adoption of isolation measures. Antiviral Res. 2003;60:129-134. |
48. | Shamshirsaz AA, Kamgar M, Bekheirnia MR, Ayazi F, Hashemi SR, Bouzari N, Habibzadeh MR, Pourzahedgilani N, Broumand V, Shamshirsaz AH. The role of hemodialysis machines dedication in reducing Hepatitis C transmission in the dialysis setting in Iran: a multicenter prospective interventional study. BMC Nephrol. 2004;5:13. |
49. | Saxena AK, Panhotra BR, Sundaram DS, Naguib M, Venkateshappa CK, Uzzaman W, Mulhim KA. Impact of dedicated space, dialysis equipment, and nursing staff on the transmission of hepatitis C virus in a hemodialysis unit of the middle east. Am J Infect Control. 2003;31:26-33. |
50. | Valtuille R, Moretto H, Lef L, Rendo P, Fernández JL. Decline of high hepatitis C virus prevalence in a hemodialysis unit with no isolation measures during a 6-year follow-up. Clin Nephrol. 2002;57:371-375. |
51. | Aucella F, Vigilante M, Valente GL, Stallone C. Systematic monitor disinfection is effective in limiting HCV spread in hemodialysis. Blood Purif. 2000;18:110-114. |
52. | dos Santos JP, Loureiro A, Cendoroglo Neto M, Pereira BJ. Impact of dialysis room and reuse strategies on the incidence of hepatitis C virus infection in haemodialysis units. Nephrol Dial Transplant. 1996;11:2017-2022. |
53. | Izopet J, Sandres-Sauné K, Kamar N, Salama G, Dubois M, Pasquier C, Rostaing L. Incidence of HCV infection in French hemodialysis units: a prospective study. J Med Virol. 2005;77:70-76. |
54. | Hmaied F, Ben Mamou M, Saune-Sandres K, Rostaing L, Slim A, Arrouji Z, Ben Redjeb S, Izopet J. Hepatitis C virus infection among dialysis patients in Tunisia: incidence and molecular evidence for nosocomial transmission. J Med Virol. 2006;78:185-191. |
55. | Lombardi M, Cerrai T, Geatti S, Negroni S, Pertusini L, Pegoraro M, Di Lullo G. Results of a national epidemiological investigation on HCV infection among dialysis patients. (Survey by the Italian Branch of EDTNA/ERCA). J Nephrol. 1999;12:322-327. |
56. | Fabrizi F, de Vecchi AF, Como G, Lunghi G, Martin P. De novo HCV infection among dialysis patients: a prospective study by HCV core antigen ELISA assay. Aliment Pharmacol Ther. 2005;21:861-869. |
57. | Fabrizi F, Martin P, Dixit V, Brezina M, Russell J, Conrad A, Schmid P, Gerosa S, Gitnick G. Detection of de novo hepatitis C virus infection by polymerase chain reaction in hemodialysis patients. Am J Nephrol. 1999;19:383-388. |
58. | Kumagai J, Komiya Y, Tanaka J, Katayama K, Tatsukawa Y, Yorioka N, Miyakawa Y, Yoshizawa H. Hepatitis C virus infection in 2,744 hemodialysis patients followed regularly at nine centers in Hiroshima during November 1999 through February 2003. J Med Virol. 2005;76:498-502. |
59. | Furusyo N, Hayashi J, Kakuda K, Ariyama I, Kanamoto-Tanaka Y, Shimizu C, Etoh Y, Shigematsu M, Kashiwagi S. Acute hepatitis C among Japanese hemodialysis patients: a prospective 9-year study. Am J Gastroenterol. 2001;96:1592-1600. |
60. | Fissell RB, Bragg-Gresham JL, Woods JD, Jadoul M, Gillespie B, Hedderwick SA, Rayner HC, Greenwood RN, Akiba T, Young EW. Patterns of hepatitis C prevalence and seroconversion in hemodialysis units from three continents: the DOPPS. Kidney Int. 2004;65:2335-2342. |
61. | Moreira R, Pinho JR, Fares J, Oba IT, Cardoso MR, Saraceni CP, Granato C. Prospective study of hepatitis C virus infection in hemodialysis patients by monthly analysis of HCV RNA and antibodies. Can J Microbiol. 2003;49:503-507. |
62. | Santos MA, Souto FJ. Infection by the hepatitis C virus in chronic renal failure patients undergoing hemodialysis in Mato Grosso state, central Brazil: a cohort study. BMC Public Health. 2007;7:32. |
63. | Vladutiu DS, Cosa A, Neamtu A, State D, Braila M, Gherman M, Patiu IM, Dulau-Florea I. Infections with hepatitis B and C viruses in patients on maintenance dialysis in Romania and in former communist countries: yellow spots on a blank map? J Viral Hepat. 2000;7:313-319. |
64. | Rutkowski B. Changing pattern of end-stage renal disease in central and eastern Europe. Nephrol Dial Transplant. 2000;15:156-160. |
65. | Zeldis JB, Depner TA, Kuramoto IK, Gish RG, Holland PV. The prevalence of hepatitis C virus antibodies among hemodialysis patients. Ann Intern Med. 1990;112:958-960. |
66. | Santana GO, Cotrim HP, Mota E, Paraná R, Santana NP, Lyra L. [Antibodies to hepatitis C virus in patients undergoing hemodialysis in Salvador, BA, Brazil]. Arq Gastroenterol. 2001;38:24-31. |
67. | Hruby Z, Sliwinski J, Molin I, Zalewska M, Knysz B, Czyz W, Steciwko A, Bogucki J, Gladysz A. High prevalence of antibodies to hepatitis C virus in three haemodialysis centres in south-western Poland. Nephrol Dial Transplant. 1993;8:740-743. |
68. | Medeiros MT, Lima JM, Lima JW, Campos Hde H, Medeiros MM, Coelho Filho JM. [Prevalence and associated factors to hepatitis C in hemodialysis patients in Brazil]. Rev Saude Publica. 2004;38:187-193. |
69. | Amiri ZM, Shakib AJ, Toorchi M. Seroprevalence of hepatitis C and risk factors in haemodialysis patients in Guilan, Islamic Republic of Iran. East Mediterr Health J. 2005;11:372-376. |
70. | Al-Shohaib SS, Abd-Elaal MA, Zawawi TH, Abbas FM, Shaheen FA, Amoah E. The prevalence of hepatitis C virus antibodies among hemodialysis patients in Jeddah area, Saudi Arabia. Saudi Med J. 2003;2:S125. |
71. | Ben Othman S, Bouzgarrou N, Achour A, Bourlet T, Pozzetto B, Trabelsi A. [High prevalence and incidence of hepatitis C virus infections among dialysis patients in the East-Centre of Tunisia]. Pathol Biol (Paris). 2004;52:323-327. |
72. | Shaheen FA, Huraib SO, Al-Rashed R, AlDrees A, Arif M, Al-Jeffry M, Tashkandy MA, Safwat M. Prevalence of hepatitis C antibodies among hemodialysis patients in Jeddah area, Saudi Arabia. Saudi Med J. 2003;2:S125-S126. |
73. | Othman SB, Trabelsi A, Monnet A, Bouzgarrou N, Grattard F, Beyou A, Bourlet T, Pozzetto B. Evaluation of a prototype HCV NS5b assay for typing strains of hepatitis C virus isolated from Tunisian haemodialysis patients. J Virol Methods. 2004;119:177-181. |
74. | López-Alcorocho JM, Barril G, Ortiz-Movilla N, Traver JA, Bartolomé J, Sanz P, Selgas R, Carreño V. Prevalence of hepatitis B, hepatitis C, GB virus C/hepatitis G and TT viruses in predialysis and hemodialysis patients. J Med Virol. 2001;63:103-107. |
75. | Hardy NM, Sandroni S, Danielson S, Wilson WJ. Antibody to hepatitis C virus increases with time on hemodialysis. Clin Nephrol. 1992;38:44-48. |
77. | Ahmetagić S, Hantalasević L, Tihić N, Jusufović E, Stojić V. [Hepatitis C virus infection in hemodialysis patients in General Hospital Gracanica]. Med Arh. 2006;60:298-300. |
78. | Ansar MM, Kooloobandi A. Prevalence of hepatitis C virus infection in thalassemia and haemodialysis patients in north Iran-Rasht. J Viral Hepat. 2002;9:390-392. |
79. | Bdour S. Hepatitis C virus infection in Jordanian haemodialysis units: serological diagnosis and genotyping. J Med Microbiol. 2002;51:700-704. |
80. | Hussein MM, Mooij JM, Hegazy MS, Bamaga MS. The impact of polymerase chain reaction assays for the detection of hepatitis C virus infection in a hemodialysis unit. Saudi J Kidney Dis Transpl. 2007;18:107-113. |
81. | Sullivan DG, Kim SS, Wilson JJ, Stehman-Breen C, Gretch DR. Investigating hepatitis C virus heterogeneity in a high prevalence setting using heteroduplex tracking analysis. J Virol Methods. 2001;96:5-16. |
82. | Iwasaki Y, Esumi M, Hosokawa N, Yanai M, Kawano K. Occasional infection of hepatitis C virus occurring in haemodialysis units identified by serial monitoring of the virus infection. J Hosp Infect. 2000;45:54-61. |
83. | Kondili LA, Genovese D, Argentini C, Chionne P, Toscani P, Fabro R, Cocconi R, Rapicetta M. Nosocomial transmission in simultaneous outbreaks of hepatitis C and B virus infections in a hemodialysis center. Eur J Clin Microbiol Infect Dis. 2006;25:527-531. |
84. | Delarocque-Astagneau E, Baffoy N, Thiers V, Simon N, de Valk H, Laperche S, Couroucé AM, Astagneau P, Buisson C, Desenclos JC. Outbreak of hepatitis C virus infection in a hemodialysis unit: potential transmission by the hemodialysis machine? Infect Control Hosp Epidemiol. 2002;23:328-334. |
85. | Savey A, Simon F, Izopet J, Lepoutre A, Fabry J, Desenclos JC. A large nosocomial outbreak of hepatitis C virus infections at a hemodialysis center. Infect Control Hosp Epidemiol. 2005;26:752-760. |
86. | Alfurayh O, Sabeel A, Al Ahdal MN, Almeshari K, Kessie G, Hamid M, Dela Cruz DM. Hand contamination with hepatitis C virus in staff looking after hepatitis C-positive hemodialysis patients. Am J Nephrol. 2000;20:103-106. |
87. | Harmankaya O, Cetin B, Obek A, Seber E. Low prevalence of hepatitis C virus infection in hemodialysis units: effect of isolation? Ren Fail. 2002;24:639-644. |
88. | Taskapan H, Oymak O, Dogukan A, Utas C. Patient to patient transmission of hepatitis C virus in hemodialysis units. Clin Nephrol. 2001;55:477-481. |
89. | Gilli P, Soffritti S, De Paoli Vitali E, Bedani PL. Prevention of hepatitis C virus in dialysis units. Nephron. 1995;70:301-306. |
90. | Abacioglu YH, Bacaksiz F, Bahar IH, Simmonds P. Molecular evidence of nosocomial transmission of hepatitis C virus in a haemodialysis unit. Eur J Clin Microbiol Infect Dis. 2000;19:182-186. |
91. | Irish DN, Blake C, Christophers J, Craske JE, Burnapp L, Abbs IC, MacMahon EM, Muir P, Banatvala JE, Simmonds P. Identification of hepatitis C virus seroconversion resulting from nosocomial transmission on a haemodialysis unit: implications for infection control and laboratory screening. J Med Virol. 1999;59:135-140. |
92. | Kokubo S, Horii T, Yonekawa O, Ozawa N, Mukaide M. A phylogenetic-tree analysis elucidating nosocomial transmission of hepatitis C virus in a haemodialysis unit. J Viral Hepat. 2002;9:450-454. |
93. | Olmer M, Bouchouareb D, Zandotti C, de Micco P, de Lamballerie X. Transmission of the hepatitis C virus in an hemodialysis unit: evidence for nosocomial infection. Clin Nephrol. 1997;47:263-270. |
94. | Sánchez-Tapias JM. Nosocomial transmission of hepatitis C virus. J Hepatol. 1999;31 Suppl 1:107-12. |
95. | Rahnavardi M, Hosseini Moghaddam SM, Alavian SM. Hepatitis C in hemodialysis patients: current global magnitude, natural history, diagnostic difficulties, and preventive measures. Am J Nephrol. 2008;28:628-640. |
96. | Recommendations for preventing transmission of infections among chronic hemodialysis patients. MMWR Recomm Rep. 2001;50:1-43. |
97. | Flett A, Teo M, Mah YI, Mortlock F, Choo BB, Challinor SP, Woods HF. Low seroconversion for hepatitis C virus (HCV) antibody achieved by universal precautions alone. EDTNA ERCA J. 1998;24:40-42. |
98. | Jadoul M. Transmission routes of HCV infection in dialysis. Nephrol Dial Transplant. 1996;11 Suppl 4:36-38. |
99. | Natov SN, Pereira BJ. Hepatitis C in dialysis patients. Adv Ren Replace Ther. 1996;3:275-283. |
100. | Arenas Jiménez MD, Sánchez Paya J, González C, Rivera F, Enríquez R. Isolation of HCV patient is efficient in reducing the annual incidence of HCV infection, but is it really necessary? Nephrol Dial Transplant. 1999;14:1337-1339. |
101. | Djordjević V, Stojanović K, Stojanović M, Stefanović V. Prevention of nosocomial transmission of hepatitis C infection in a hemodialysis unit. A prospective study. Int J Artif Organs. 2000;23:181-188. |
102. | Saab S. Hepatitis C virus transmission in the hemodialysis community. Am J Kidney Dis. 2001;37:1052-1055. |
103. | Saab S, Brezina M, Gitnick G, Martin P, Yee HF Jr. Hepatitis C screening strategies in hemodialysis patients. Am J Kidney Dis. 2001;38:91-97. |
104. | Pol S, Romeo R, Zins B, Driss F, Lebkiri B, Carnot F, Berthelot P, Bréchot C. Hepatitis C virus RNA in anti-HCV positive hemodialyzed patients: significance and therapeutic implications. Kidney Int. 1993;44:1097-1100. |