Title: Universal precautions prevent hepatitis C virus transmission: A 54 month follow-up of the Belgian multicenter study
Abstract: Universal precautions prevent hepatitis C virus transmission: A 54 month follow-up of the Belgian multicenter study. The isolation of anti-hepatitis C virus (HCV) in hemodialyzed (HD) patients has been repeatedly advocated to prevent nosocomial HCV transmission. We evaluated the incidence of seroconversion for HCV in Belgian HD patients, and demonstrate the complete prevention of HCV transmission by adherence to the universal precautions advocated by the Centers for Disease Control (Atlanta, GA, USA). All (N = 963) HD patients from 15 units, none of which isolates anti-HCV positive patients, were tested by a second or third generation enzyme-linked immunosorbent assay (with confirmation by a second- or third-generation recombinant immunoblot assay or the polymerase chain reaction) every 18 months from May 1991 to November 1995. Follow-up was available in 488 patients (drop-outs resulting from death or transplantation mainly). The yearly incidence of seroconversion for HCV over the initial 18 months was 1.41%, with evidence suggestive of nosocomial HCV transmission. Universal precautions were therefore reinforced. The incidence of seroconversion subsequently fell to 0.56% and 0%, respectively (P = 0.014), despite the facts that the average transfusion load and the proportion of patients with dialyzer reuse or with monitors disinfected after each session did not change significantly. We conclude that the strict enforcement of universal precautions fully prevents HCV transmission to HD patients. The isolation of anti-HCV positive patients is not warranted. Universal precautions prevent hepatitis C virus transmission: A 54 month follow-up of the Belgian multicenter study. The isolation of anti-hepatitis C virus (HCV) in hemodialyzed (HD) patients has been repeatedly advocated to prevent nosocomial HCV transmission. We evaluated the incidence of seroconversion for HCV in Belgian HD patients, and demonstrate the complete prevention of HCV transmission by adherence to the universal precautions advocated by the Centers for Disease Control (Atlanta, GA, USA). All (N = 963) HD patients from 15 units, none of which isolates anti-HCV positive patients, were tested by a second or third generation enzyme-linked immunosorbent assay (with confirmation by a second- or third-generation recombinant immunoblot assay or the polymerase chain reaction) every 18 months from May 1991 to November 1995. Follow-up was available in 488 patients (drop-outs resulting from death or transplantation mainly). The yearly incidence of seroconversion for HCV over the initial 18 months was 1.41%, with evidence suggestive of nosocomial HCV transmission. Universal precautions were therefore reinforced. The incidence of seroconversion subsequently fell to 0.56% and 0%, respectively (P = 0.014), despite the facts that the average transfusion load and the proportion of patients with dialyzer reuse or with monitors disinfected after each session did not change significantly. We conclude that the strict enforcement of universal precautions fully prevents HCV transmission to HD patients. The isolation of anti-HCV positive patients is not warranted. The unequivocal demonstration of a nosocomial transmission of the hepatitis C virus (HCV)1.Stuyver L. Claeys H. Wyseur A. Van Arnhem W. de Beenhouwer H. Uytendaele S. Beckers J. Matthijs D. Leroux Roels G. Maertens G. de Paepe M. Hepatitis C virus in a hemodialysis unit: Molecular evidence for nosocomial transmission.Kidney Int. 1996; 49: 889-895Abstract Full Text PDF PubMed Scopus (113) Google Scholar, 2.Allander T. Medin C. Jacobson S.H. Grillner L. 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Hepatitis C virus in the hemodialysis setting: A review with recommendations for control.Semin Dial. 1994; 7: 124-127Crossref Scopus (60) Google Scholar, 13.Gilli P. Soffritti S. de Paoli Vitali E. Bedani P.L. Prevention of hepatitis C virus in dialysis units.Nephron. 1995; 70: 301-306Crossref PubMed Scopus (63) Google Scholar have stressed that nosocomial transmission probably resulted mainly from an inadequate application of the universal precautions delineated by the Centers for Disease Control (Atlanta, GA, USA)14.Mmwr Update Universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and other bloodborne pathogens in health-care settings.JAMA. 1988; 260 (10.1001/jama.260.4.462): 462-465Crossref Scopus (52) Google Scholar, and concluded that prevention of HCV nosocomial transmission would be better achieved by strict adherence to the universal precautions by staff members, than by the cumbersome, not fully secure, segregation of patients. We have taken advantage of an ongoing prospective Belgian multicenter study to evaluate the benefits of the latter policy in the absence of patient isolation. We demonstrate the full prevention of HCV transmission. All 15 units involved in the initial 18-month phase of the study10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar accepted to participate for two further 18-month periods, for a total follow-up of 54 months. A single small unit was closed as of September 1993, and most of its patients were transferred to another participating unit. None of the units isolated anti-HCV (+) patients. As the results of the initial 18 month survey strongly suggested nosocomial transmission of HCV10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar, staff meetings were held in participating units in order to explain the universal precautions14.Mmwr Update Universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and other bloodborne pathogens in health-care settings.JAMA. 1988; 260 (10.1001/jama.260.4.462): 462-465Crossref Scopus (52) Google Scholar and identify potential breaks in their implementation. All patients given chronic hemodialysis either in hospital-based or in low-care facilities were included. They were tested for anti-HCV antibodies every 18 months from May 1991 to November 1995. Patients on home HD or peritoneal dialysis were not included. No patient was an intravenous drug abuser or had antibodies against the human immunodeficiency virus. Screening was performed by second generation enzyme-linked immunosorbent assay (ELISA 2; Ortho Diagnostic Systems, Raritan, NJ, USA) in May 1991 and November 1992, and by the more sensitive15.Goffin E. Pirson Y. Cornu C. Jadoul M. Van Ypersele de Strihou C. Significance of NS3, NS5 antigens in screening for HCV antibody.Lancet. 1994; 343: 853-854Google Scholar,16.Courouce A.M. Le Marrec N. Girault A. Ducamp S. Simon N. Anti-hepatitis C virus (anti-HCV) seroconversion in patients undergoing hemodialysis: Comparison of second- and third-generation anti-HCV assays.Transfusion. 1994; 34: 790-795Crossref PubMed Scopus (102) Google Scholar third generation ELISA (ELISA 3; Ortho) in May 1994 and November 1995. In order to facilitate comparisons between the three consecutive 18-month periods, only patients tested at these 18 month intervals were included. Thus, in contrast with our initial 18 month study10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar in which patients were tested (and included) every six months, patients tested only in November 1991 and/or May 1992 were not included. ELISA 2 positive patients were tested by the second-generation recombinant immunoblot assay (RIBA 2; Ortho). ELISA 3 positive patients were tested by the third generation RIBA15.Goffin E. Pirson Y. Cornu C. Jadoul M. Van Ypersele de Strihou C. Significance of NS3, NS5 antigens in screening for HCV antibody.Lancet. 1994; 343: 853-854Google Scholar and/or the reverse transcriptase nested polymerase chain-reaction (RT-PCR) for the detection of HCV-RNA17.Goffin E. Pirson Y. Cornu C. Geubel A. Squifflet J.P. van Ypersele de Strihou C. Outcome of HCV infection after renal transplantation.Kidney Int. 1994; 45: 551-555Abstract Full Text PDF PubMed Scopus (51) Google Scholar. The detection of antibodies against at least one HCV antigen or of HCV-RNA was considered as confirmatory. In order to differentiate true seroconversion from an apparent seroconversion resulting from the higher sensitivity of ELISA 3, the ELISA 2 (-) sera of patients who became subsequently ELISA 3 (+) were retested by the ELISA 3. All genotyping of the HCV strains was performed by Inno-Lipa II18.Stuyver L. Wyseur A. van Arnhem W. Hernandez F. Maertens G. Second-generation Line Probe assay for hepatitis C virus genotyping.J Clin Microbiol. 1996; 34: 2259-2266PubMed Google Scholar. Blood transfusions administered throughout the study were recorded for each patient as previously described10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar. Each unit was asked to fill in a form detailing HD practices such as the frequency of disinfection of HD monitors and the existence of a program of dialyzer reuse, during each 18-month period, and to state the actual proportion of patients concerned. Standard statistical tests were performed as indicated. P values < 0.05 were considered as significant. A total of 963 patients (545 males) were included. At the time of inclusion, they had a median age of 60 years (range, 12 to 88 years old) and had been on HD for a median of 11 months (range, < 1 to 257 months). Four hundred and eighty-eight patients were tested more than once and were included in both the longitudinal and prevalence studies. The other 475 were added to the prevalence study only, as they were tested only once as a result of death (N = 170), renal transplantation (N = 85), transfer to CAPD (N = 4) or to non-participating HD units (N = 16), recovery of renal function (N = 3) or inclusion in November 1995 (N = 197). During the three consecutive 18-month periods, the yearly seroconversion rate dropped from 1.41% (5 of 236 patients at risk) to 0.56% (2 of 238 patients at risk) and 0% (0 of 269 patients at risk) (X2 for trend, P = 0.014). The five seroconversions observed during the initial 18 months were detected in three unrelated HD units: unit A, N = 2; unit B, N = 2; unit C, N = 1. The subsequent two seroconversions were detected in two unrelated HD units: unit A and unit D. The genotypes of HCV strains of patients with seroconversion from units A and B were 1b, 4 and 4 c/d one each (unit A) and 1b for both patients (unit B). Anti-HCV antibodies persisted in all patients throughout the follow-up period, for a total follow-up of 169 patient-years. The prevalence of confirmed anti-HCV (+) patients dropped from 13.5% (54 of 399) in May 1991 to 11.8% (51 of 433) in November 1992, 12.7% (61 of 481) in May 1994 and 9.4% (48 of 510) in November 1995. This drop in prevalence between May 1991 and November 1995 barely reached significance (X2, P = 0.0507). During the three consecutive 18-month periods, no significant change was observed in the percentage of patients with dialyzer reuse (37, 37 and 35% respectively; X2 for trend, NS) and in that of patients whose HD monitors were disinfected after each session (25, 28 and 31%, respectively; X2 for trend, NS). The same was true when only the percentage of involved units was considered (Table 1; X2 for trend, NS).Table 1Incidence of seroconversion and evolution of hemodialysis (HD) practices over three consecutive 18 month periods The number of blood transfusions administered to patients at risk of seroconversion did not change during the three consecutive periods: 1.4 ± 3.7 (SD) unit/18 months/patient, 1.7 ± 4.3 and 1.3 ± 3.8, respectively (Mann-Whitney U-test, NS; Table 1). Of note, three of the seven patients with seroconversion (2 of 5 and 1 of 2 during the first and second 18-month studies, respectively) had not been transfused during the preceding 18 months. In our multicenter study, the incidence of seroconversion for HCV in HD patients fell progressively to zero over a 54 month period. This observation is even more impressive as ELISA tests were more sensitive in the last two periods than in the first one. Admittedly, rare new HCV infection(s) might have been missed by the ELISA tests, as recently reported in abstract form19.Martin P. Brezina M. Dixit V. Russell J. Conrad A. Schmid P. Gitnick G. Detection of de novo hepatitis C virus infection by polymerase chain reaction in hemodialysis patients.Hepatology. 1996; 24 (abstract): 544ACrossref Google Scholar. Still, in the few cases of unexplained alanine aminotransferase increase, which were tested by PCR, HCV-RNA was not detected (data not shown). Possible explanations for our results should be discussed. Better prevention of transfusional HCV transmission is not a likely explanation as the average transfusional load did not change over the three periods. Admittedly, the testing of blood donors improved substantially over the 54 months, the first generation tests being replaced by the more sensitive second and, eventually, third generation tests. The risk of transfusional transmission of HCV has clearly decreased with recent screening tests20.Schreiber G.B. Busch M.P. Kleinman S.H. Korelitz J.J. The risk of transfusion-transmitted viral infections. The Retrovirus Epidemiology Donor Study.N Engl J Med. 1996; 334 (10.1056/NEJM199606273342601): 1685-1690Crossref PubMed Scopus (1603) Google Scholar,21.Couroucé A.M. Pillonel J. For The Retrovirus, Viral Hepatitis Working Groups of the French Society of Blood Transfusion Transfusion-transmitted viral infections.N Engl J Med. 1996; 335: 1609-1610Crossref PubMed Scopus (54) Google Scholar. However, three of the seven detected seroconversions occurred in non-transfused patients; furthermore, our initial study strongly pointed to nosocomial HCV infection in some of our patients10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar. Changes in dialyzer reuse are also unlikely to have contributed to the fall of the incidence of HCV seroconversion. Dialyzer reuse was not a risk factor for seroconversion over the initial 18-month period10.Jadoul M. Cornu C. Van Ypersele de Strihou C. the UCL Collaborative Group: Incidence and risk factors for hepatitis C seroconversion in hemodialysis: A prospective study.Kidney Int. 1993; 44: 1322-1326Abstract Full Text PDF PubMed Scopus (215) Google Scholar. Furthermore, in contrast to the progressive fall in the incidence of seroconversion over the entire 54 months, the overall reuse policy did not change, as illustrated by the stability of the % of patients with reuse. Interestingly, most units with reuse do not use a separate room for the reuse of dialyzers in HCV (+) patients (data not shown), a finding in contrast with the recent suggestion that the absence of this precaution may be a risk factor for seroconversion22.Pinto dos Santos J. Loureiro A. Cendoroglo Neto M. Pereira B.J.G. Impact of dialysis room and reuse strategies on the incidence of hepatitis C virus infection in haemodialysis units.Nephrol Dial Transplant. 1996; 11: 2017-2022Crossref Scopus (102) Google Scholar. The prevention of HCV transmission through contaminated HD monitors is also unlikely to account for the decreasing incidence of seroconversion. Indeed, no new case of HCV transmission occurred despite an unchanged (and poor) disinfection policy of monitors: over the 54 months, over 70% of the patients were dialyzed in units whose monitors were not disinfected after each session. This observation argues against a significant role of monitors in HCV transmission at all! The role of infected staff members as a significant source of HCV infection for patients appears also unlikely. Indeed, the number of HCV (+) nurses working in participating units decreased only slightly from six23.Jadoul M. El Akrout M. Cornu C. Van Ypersele de Strihou C. Prevalence of hepatitis C antibodies in health-care workers.Lancet. 1994; 344: 339Abstract PubMed Scopus (36) Google Scholar to five (unpublished data) over the last three years. In contrast, the incidence of HCV transmission dropped markedly. The recent demonstration of HCV transmission from a surgeon to five of his patients24.Esteban J.I. GÓMEZ J. Martell M. Cabot B. Quer J. Camps J. GONZÁLEZ A. Otero T. Moya A. Esteban R. Guardia J. Transmission of hepatitits C virus by a cardiac surgeon.N Engl J Med. 1996; 334 (10.1056/NEJM199602293340902): 555-560Crossref PubMed Scopus (360) Google Scholar thus remains unusual. It might be argued that the trend towards a lower prevalence of anti-HCV (+) patients was the factor that reduced the risk of nosocomial transmission, and hence decreased the incidence of seroconversion. This hypothesis does not account for our observations as the prevalence of anti-HCV (+) at the onset of the last 18 month period was 12.7%, similar to that at the onset of the study (13.5%). In the absence of a more convincing explanation, we propose that the suppression of HCV transmission resulted from the improved enforcement of universal precautions. Although adherence to universal precautions was not quantitated in this long-term multicentric study, it is noteworthy that the decrease in HCV transmission coincided with the efforts to fully describe the universal precautions to staff members as well as patients, and improve their actual implementation in the participating units. A special emphasis was laid upon hand washing, the use of gloves and the avoidance of sharing of articles between patients. Our results support the CDC statement that universal precautions should prevent HCV transmission in HD patients12.Moyer L.A. Alter M.J. Hepatitis C virus in the hemodialysis setting: A review with recommendations for control.Semin Dial. 1994; 7: 124-127Crossref Scopus (60) Google Scholar, especially as the infectivity of HCV is much lower than that of HBV. They are also in line with the experience reported in abstract form by the E. Rist Medical Center in Paris, where a 0% incidence has been maintained over several years despite a high HCV prevalence and the absence of isolation25.Chauveau P. Bouchardeau F. Couroucé A.M. Lemarrec N. Naret C. Zins B. Poignet J.L. Incidence of hepatitis C infection in a dialysis centre: A five-years follow-up.Nephrol Dial Transplant. 1994; 7 (abstract): 979Google Scholar. The alternative policy to the strict implementation of universal precautions is the isolation of anti-HCV (+) HD patients in a separate room or on separate monitors. In 1993, these respective policies were adopted by 18 and 37% of HD units from the European Dialysis and Transplant Association Registry26.Valderrábano F. Jones E.H.P. Mallick N.P. Report on management of renal failure in Europe, XXIV, 1993.Nephrol Dial Transplant. 1995; 10: 1-25Crossref PubMed Scopus (226) Google Scholar. These percentages have increased more recently in Spain and Portugal22.Pinto dos Santos J. Loureiro A. Cendoroglo Neto M. Pereira B.J.G. Impact of dialysis room and reuse strategies on the incidence of hepatitis C virus infection in haemodialysis units.Nephrol Dial Transplant. 1996; 11: 2017-2022Crossref Scopus (102) Google Scholar,27.Spanish Multicentric Study Group Traver A. Barril G. Evaluation of isolation measures on HCV+ patients in hemodialysis units. Four years experience.Nephrol Dial Transplant. 1996; 11 (abstract): A217Google Scholar. The effectiveness of isolation in separate rooms remains to be demonstrated. In Portugal, units isolating anti-HCV (+) patients reported a rather high (3.2%) yearly incidence of seroconversion in 1991 to 1993 (prevalence around 25%)22.Pinto dos Santos J. Loureiro A. Cendoroglo Neto M. Pereira B.J.G. Impact of dialysis room and reuse strategies on the incidence of hepatitis C virus infection in haemodialysis units.Nephrol Dial Transplant. 1996; 11: 2017-2022Crossref Scopus (102) Google Scholar. The safety of isolating anti-HCV (+) HD patients also remains unproved. Indeed, as pointed out elsewhere11.Jadoul M. Should hemodialysis patients with hepatitis C virus antibodies be isolated?.Semin Dial. 1995; 8: 1-3Crossref Scopus (21) Google Scholar, isolation entails the risk of less than adequate implementation of universal precautions, with an attendant higher risk of cross-infection by multiple HCV strains and/or other viruses. In this regard preliminary results suggest that the incidence of infection by the recently discovered hepatitis G virus (HGV) also fell to zero in our unit in parallel with that of HCV. Finally, isolation entails a substantial cost, especially in units with HBsAg (+) patients, in which up to four wards (to accommodate the B+C+, B+C-, B-C+, B-C- patients) may be required. The dedication of separate monitors for HCV (+) patients has been advocated as an alternative. Two small single center studies have recently reported a low (but not 0%) incidence of seroconversion for HCV28.Blumberg A. Zehnder C. Burckhardt J.J. Prevention of hepatitis C infection in haemodialysis units. A prospective study.Nephrol Dial Transplant. 1995; 10 (coordinators): 230-233PubMed Google Scholar,29.Fabrizi F. Lunghi G. Guarnori I. Raffaele L. Crepaldi M. Pagano A. Locatelli F. Incidence of seroconversion for hepatitis C virus in chronic haemodialysis patients: A prospective study.Nephrol Dial Transplant. 1994; 9: 1611-1615PubMed Google Scholar with this policy. The risks of cross-infection are not avoided by this policy, and its large scale effectiveness remains to be demonstrated. As the role of the monitors in HCV transmission appears limited, the degree of effectiveness of this policy is likely to depend mainly on the associated improved application of universal precautions, the segregation acting mainly as a reminder of the risk of viral transmission. Nosocomial transmission of HCV has recently been demonstrated both in a hematology ward30.Allander T. Gruber A. Naghavi M. Beyene A. Söderström Njörkholm M. Grillner L. Persson M.A.A. Frequent patient-to-patient transmission of hepatitis C virus in a haematology ward.Lancet. 1995; 345: 603-607PubMed Scopus (207) Google Scholar and in renal transplant recipients31.Munro J. Briggs J.D. Mccruden E.A. Detection of a cluster of hepatitis C infections in a renal transplant unit by analysis of sequence variation of the NS5a gene.J Infect Dis. 1996; 174: 177-180Crossref PubMed Scopus (26) Google Scholar. On the basis of our observations it may be proposed that in these other, less exposed settings, prevention should also rely mainly on an enforced adherence to universal precautions. In conclusion, we report the full prevention of HCV transmission to HD patients by implementing universal precautions, rather than isolation of anti-HCV (+) patients. This study was presented at a Mini Symposium at the XXIXth American Society of Nephrology meeting (New Orleans, 1996). The authors gratefully acknowledge the invaluable help of the nurses of all participating units, and Ortho Diagnostics Systems for the gift of ELISA tests.