Felix Yao DOCTOR OF PHILOSOPHY
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1 Investigation on the Risk of Viral Infection in Musculoskeletal Grafts Felix Yao The collection of these publications is presented for the degree of DOCTOR OF PHILOSOPHY of The University of Western Australia School of Surgery The University of Western Australia 2009 The work presented in this thesis was performed in The University of Western Australia, School of Surgery, Centre for Orthopaedic Research Queen Elizabeth II Medical Centre, Nedlands, Perth, Western Australia.
2 TABLE OF CONTENTS Declaration...i Thesis Summary...ii List of Figures...v List of Tables...vi Abbreviations...viii Chapter 1: The risk of HIV, HBV, HCV and HTLV infection among musculoskeletal tissue donors in Australia (American Journal of Transplantation, : )...1 Chapter 2: Comparison of the risk of viral infection between the living and nonliving musculoskeletal tissue donors in Australia (Transplant International, :936-41)...9 Chapter 3: Trends in prevalence of viral infections in Australian musculoskeletal tissue donors and projections of incidence and residual risk, (Transplantation, (5): )...20 Chapter 4: Prevalence and incidence of viral infections among musculoskeletal tissue donors and first-time blood donors (Annals of Internal Medicine, (10): )...43 Chapter 5: General Discussion Discussion Future Direction...53 References...57
3 DECLARATION The work detailed in this thesis was performed by the candidate unless otherwise specified. This thesis is submitted for the degree of Doctorate of Philosophy at the University of Western Australia and has not been submitted for any other qualifications at other institutions. CANDIDATE Felix Yao Signature SUPERVISORS Winthrop Professor Ming Hao Zheng Signature Winthrop Professor David Wood Signature i
4 THESIS SUMMARY Around 50,000 hip and knee replacements are performed every year in Australia and this number has been increasing by around 13% annually since 1998 (Transplantation Society 2006). The incidence and number of revision surgery has increased by a similar proportion. Autogenous bone or allograft is still the gold standard grafting material and is currently used in a variety of reconstructive surgical procedures. The use of any allograft material carries with it the risk of transfer of disease from donor to recipient. These tissues can transmit the same viral and bacterial infections as blood, and the products of a single donation may be transplanted to several recipients. In contrast to blood, musculoskeletal tissues may come from surgical and cadaveric donation. Overall, the prevention of infection relies on the maintenance of rigid protocols for procurement, donor and allograft testing, secondary sterilisation, and the adherence to internal safety standards within the tissue banks. This thesis aims to determine the risk of viral infection among musculoskeletal tissue donors in Australia. We retrieved and analysed data retrospectively from three large tissue banks in Australia (Perth, Queensland, Victoria). This includes 12,415 musculoskeletal tissue donors, 10,937 of which are surgical donors and 1,478 of which are deceased donors, for the period of This data was analysed to determine the prevalence and incidence of viral infections such as human immunodeficiency virus (HIV), hepatitis B virus (HBV), hepatitis C virus (HCV) and human T-lymphotropic virus (HTLV) in musculoskeletal allografts. The results indicate that the risk of viral infection from musculoskeletal tissue transplantation in Australia is low. The probability of a donor being viremic but serologically negative at the time of donation is calculated to be 1 in 128,000 for HIV, 1 in 188,000 for HBV, 1 in 55,000 for HCV ii
5 and 1 in 118,000 for HTLV. These figures are further reduced with nucleic acid amplification testing (NAT); however NAT is more complex, time consuming, and expensive than most serological testing. Currently, in Australia, the majority of musculoskeletal tissue donations are from living surgical donors, predominantly consisting of retrieved femoral head postprimary hip arthroplasty. However, to fulfil the increasing demand for tissues, there is a trend to begin the use of materials obtained post-mortem from organ donation patients and from cadaveric sources. This thesis compared the risk of viral infection from living and nonliving musculoskeletal tissue donors in Australia. Results indicate that current mandatory retesting of surgical donors six (6) months postdonation reduces the risk of viral infection by approximately 95% by eliminating almost all infected donors in the window period. The results also suggest that the use of NAT as an additional screening tool for nonliving donors would reduce the residual risk to levels comparable to that in living donors. The risk of major blood-borne infections from musculoskeletal tissue donation in Australia is very low due to sensitive screening methods and effective donor recruitment and selection. Analysis of infection trends in tissue donors is an essential part of monitoring the effectiveness of donor deferral strategies, testing algorithms, and the safety of tissue supply. This thesis focussed on the trends in prevalence of HIV, HBV, HCV and HTLV infections in Australian musculoskeletal donations and evaluated the changes in incidence and residual risk in 12,415 musculoskeletal donations for the period 1993 to The results indicate that the overall prevalence of screened transfusion-transmitted viral infections did not vary significantly for iii
6 musculoskeletal donors over the study period, despite falling in the general population and first-time blood donors. In tissue donors, HIV incidence significantly decreased over time, and HBV decreased significantly during ; however, there was an apparent increase in the estimated incidence of HCV in compared with earlier years. Furthermore the residual risk estimate of HIV in the period has declined 5-fold compared to estimates in the period This is perhaps due to greater awareness of high risk behaviours among donors, improvement in donor recruitment and an overall decrease in infection levels in the general population. Musculoskeletal tissue is second only to blood as the most frequent transplanted human tissue. Viral infection is a potential complication of tissue transplantation. In this thesis the rates of HIV, HBV, HCV and HTV infection in musculoskeletal donors in Australia were identified and then compared with results in published data from Canada, Scotland and the United States. The study also compared that result with first-time blood donors because they have satisfied similar donor selection criteria (Galea et al. 2006). The results indicate that prevalence and incidence estimates for viral infection in Australian tissue donors are higher than those in blood donors. This was also reported in studies from other countries. Accordingly, it is crucial that viral prevalence and incidence be monitored to evaluate the safety of tissue supply and to improve donor selection processes. iv
7 LIST OF FIGURES PAGE CHAPTER 3: Figure 1: Prevalence trends of transfusion-transmissible viral infections per 100,000 persons among musculoskeletal tissue donors and first-time blood donors by period of time. 27 v
8 LIST OF TABLES PAGE CHAPTER 1: Table 1: Prevalence of viral infection among musculoskeletal tissue donors in comparison to first-time blood donors for the period Table 2: Estimated incidence of viral infection among musculoskeletal tissue donors in Australia. 7 Table 3: Estimated probability of undetected viral infections in musculoskeletal tissue donors in Australia. 7 CHAPTER 2: Table 1: Prevalence of viral markers among living musculoskeletal donors, according to age and gender ( ). 16 Table 2: Prevalence of viral markers among nonliving musculoskeletal donors, according to age and gender ( ). 16 Table 3: Estimated incidence and probability 17 vi
9 PAGE CHAPTER 4: Table 1: Characteristics of Musculoskeletal Tissue Donors and First- Time Blood Donors 45 Table 2: Comparison of Prevalence and Incidence of HIV, Hepatitis B Virus, Hepatitis C Virus and Human T-Cell Lymphomatropic Virus among Musculoskeletal Tissue Donors and First-Time Blood Donors 45 vii
10 ABBREVIATIONS HIV HBV HCV HTLV anti-hiv anti-hcv anti-htlv HBsAg NAT PBTB ARCBS QBB DTBV CI WP IQR EIA NCHECR Human immunodeficiency virus Hepatitis B virus Hepatitis B virus Human T- lymphotrophic virus Antibody to HIV Antibody to HCV Antibody to HTLV Hepatitis B surface antigen Nucleic acid amplification testing Perth Bone and Tissue Bank Australian Red Cross Blood Services Queensland Bone Bank Donor Tissue Bank of Victoria Confidence interval Window period Inter-quartile range Enzyme immunoassay National Centre in HIV Epidemiology and Clinical Research viii
11 CHAPTER ONE THE RISK OF HIV, HBV, HCV AND HTLV INFECTION AMONG MUSCULOSKELETAL DONORS IN AUSTRALIA Journal: American Journal of Transplantation Date of Publication: 28 th August 2007 Volume and Pages: 7:
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19 CHAPTER TWO COMPARISON OF THE RISK OF VIRAL INFECTION BETWEEN THE LIVING AND NONLIVING MUSCULOSKELETAL DONORS IN AUSTRALIA Journal: Transplant International Date of Publication: 7 th May 2008 Volume and Pages: 21:
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30 CHAPTER THREE TRENDS IN PREVALENCE OF VIRAL INFECTIONS IN AUSTRALIAN MUSCULOSKELETAL TISSUE DONORS AND PROJECTIONS OF INCIDENCE AND RESIDUAL RISK, Journal: Transplantation Date of Publication: 23 rd May 2008 Volume and Pages: 86 (5) :
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53 CHAPTER FOUR PREVALENCE AND INCIDENCE OF VIRAL INFECTONS AMONG MUSCULOSKELETAL TISSUE DONORS AND FIRST-TIME BLOOD DONORS. Journal: Annals of Internal Medicine Date of Publication: 20 th May 2008 Volume and Pages: 148 (10) :
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59 CHAPTER FIVE GENERAL DISCUSSION 49
60 5.1 DISCUSSION Over 6,000 musculoskeletal grafts are implanted annually in Australia for use in trauma surgery, joint replacement arthroplasty, tendon reconstructive surgery, and in other treatment modalities. In order to safeguard patient safety from tissue implantation there is an ongoing need to minimise the possibility of disease transmission from donated bone grafts. However, there is no national data on the risk of infection associated with musculoskeletal allograft transplantation in Australia. In the past few years, tissue banks have made significant progress regarding the provision of safe and efficacious grafts, however there is little knowledge by medical clinicians and the general public of the risk of disease transmission from this source. Orthopaedic patients receiving transfusions may worry about the safety of the blood they receive, but be blissfully unaware of the possible risks associated with the allograft bone in their femur or hip. The risk of disease transmission from donor to recipient is always present. Therefore the supply of safe allograft material is central to the success of an allograft reconstruction program. Since 1993, all musculoskeletal tissue banks in Australia have been regulated by the Therapeutic Goods Administration (TGA), which issues a framework for donor tissue screening, retrieval, processing, distribution, and reporting of adverse events (Australian Therapeutic Goods Administration 2000). However, there is no evidence-based data on the risk of viral and bacterial infection associated with musculoskeletal tissue transplantation in Australia. As such there are immediate limitations to the assessment of current screening and processing methods, and little support by way of information medical practitioners can provide to their patients and the general population. 50
61 Currently, there are no national estimates of the risk of viral infection from musculoskeletal tissue transplantation in Australia. Using data from three large tissue banks in Australia (Perth, Queensland and Victoria), this project evaluated the risk of human immunodeficiency virus (HIV), hepatitis B virus (HBV), hepatitis C virus (HCV) and human T-lymphotrophic virus (HTLV). By applying the Incidence/Window Period model to incidence estimates for musculoskeletal donors, the probability of a donor being viremic but serologically negative at the time of donation was calculated to be 1 in 128,000 for HIV, 1 in 188,000 for HBV, 1 in 55,000 for HCV and 1 in 118,000 for HTLV. These figures indicate that the risk of viral infection from musculoskeletal tissue transplantation in Australia is low. With the addition of nucleic acid amplification testing (NAT), the probability of donor viremia would be reduced to 1 in 315,000 in HIV, 1 in 385,000 for HBV and 1 in 500,000 for HCV. NAT reduced the risk of viral infection, but is very complex, time consuming and expensive. Screening with NAT of musculoskeletal tissue donors for HIV and HCV has been implemented in the United States and other developed nations. In Australia, however, the majority of musculoskeletal tissue donations are from living surgical donors. This thesis investigates the prevalence and estimated incidence of HIV, HBV, HCV and HTLV in living donors and nonliving donors in Australia, to ascertain whether there is a greater risk of viral infection associated with tissues obtained from nonliving donors and whether NAT screening tests should be implemented. Results indicate that current mandatory retesting of surgical donors six (6) months post donation reduces the risk of viral infection approximately 95% by eliminating almost all donors in the window period. NAT screening of donations from non-living donors would similarly reduce the 51
62 window period, and consequently the residual risk by approximately 50 percent for HBV, 60 percent for HIV, and 90 percent for HCV. NAT screening for non-living musculoskeletal tissue donations will reduce the risk of viral transmission to rates similar to that among living donors undergoing 6-month serological retesting. Monitoring trends in infectious disease rates is important in determining the safety of the tissue supply including the effectiveness of donor deferral criteria, serological testing, and other screening measures. This project evaluated the changes in the prevalence, incidence and residual risk of major transfusion-transmitted viral infections between 1993 and 2004 using data collected from three major musculoskeletal tissue banks in Australia. The results showed that prevalence for all viral markers were higher in musculoskeletal tissue donors than in first-time blood donors. For musculoskeletal tissue, donor trend analysis showed that prevalence rates of HIV, HBV, HCV and HTLV remained relatively stable. However, there was a significant decrease in the estimated incidence of HIV for tissue donors during the study period (p<010001). Our results suggest that the current risk of transmission of HBV is 1 in 274,000, and HCV is 1 in 45,000. The residual estimate for HIV in the period 2002 through 2004 is 1 in 417,000, a decline of more than five-fold when compared to the 1 in 80,000 estimated in the period 1993 through In Australia, the current risk of a musculoskeletal tissue graft recipient becoming infected with a retrovirus or a hepatitis virus is extremely low. These findings affirm the effectiveness of current stringent donor selection criteria and screening methods in reducing the residual risk of transfusiontransmitted viral infections. 52
63 The comparison of viral prevalence and incidence among tissue donors provides an indication of the relative safety of the tissue supply in different countries. The common perception among clinicians that the risk associated with the transmission of viral infection from a musculoskeletal tissue donor is equivalent to that of a first-time blood donor is inaccurate. Our findings show that while prevalence rates in tissue donors are low, they are comparably higher than blood donor rates (p<0.05), a pattern also reported by Canada, Scotland and the United States. However, it must be admitted that the results of this study are highly dependent on the assumptions inherent in the mathematical risk model and the accuracy and completeness of the original data collection. Comparisons of data between countries are also affected by differences in donor selection policies, the evolution and differences in screening tests, and differences in the donor profile. 5.2 FUTURE DIRECTION Despite demonstrating its ability to interdict HCV sero-negative organ and tissue donors, a French study suggested that the cost-effectiveness of such testing may not compare favourably with that of other health preventative measures, such as the application of more stringent donor exclusion criteria, or better reporting methods (Challine et al. 2004). This is certainly the experience with HIV and HCV NAT donor screening in the US where its cost effectiveness has been assessed as poor in the order of 4.7 and 11.2 million US$ per quality-adjusted life year (QALY) saved. This is substantially higher than the upper limit of $50,000 per QALY normally applied to assess healthcare interventions. Further studies are needed to evaluate the efficacy of nucleic acid amplification testing (NAT) in Australia, as an additional screening tool. NAT is more complex, time consuming, and expensive than most serological testing 53
64 which may discourage implementation. Some of the cost may be offset by the discontinuation of less effective serological tests. Similarly cost effectiveness maybe achieved by spreading the cost over the total number of products sourced from one donor. Cytomegalovirus (CMV) infections usually cause minimal, often asymptomatic disease in individuals with normal, healthy immune systems. However, in immunocompromised patients, CMV infections represent a significant risk for serious, or even fatal, morbidity. Furthermore, post-transplantation, systemic CMV disease appears to be a negative prognostic factor for long-term graft survival. One key parameter for preventing transfusion-transmitted CMV is to determine the frequency of primary CMV infection among sero-negative bone donors. Only a few studies have been published concerning this in blood donors, and there is no literature regarding the risk of primary CMV infection in bone donors. A study by the Perth Bone and Tissue Bank (PBTB) in 2005 showed an overall rejection rate of 32% for musculoskeletal tissue donors, a figure in the upper range of the 17-36% rejection rate reported by other banks (Ivory & Thomas, 1993; Lord et al. 1988; Tomford et al.1990). Allografts may be contaminated with exogenous microorganisms during the retrieval or processing of tissue. Future studies should evaluate the risk of bacterial infection in musculoskeletal tissue donors and factors which may contribute to the increased bacterial bio-burden from recovered tissue including the recovery environment, the length of time from death to tissue harvesting, the cause of death, and the number of staff involved during tissue harvesting. 54
65 Screening for markers of infectious disease, although important, is an incomplete solution to the problem of ensuring safety of musculoskeletal allografts. Pre-donation screening of donors for risk factors of transmissible diseases should still be considered of primary importance in reventing transmission of disease. A review of the musculoskeletal donor selection criteria for both living and nonliving donors should be conducted in order to reduce the risk of infection in musculoskeletal allograft transplantation. The demand for musculoskeletal tissue is growing in Australia. It has been estimated that in 10 years 50% of all orthopaedic procedures will involve tissue grafts (Hackett 2001). In Australia, 88% of musculoskeletal allografts are retrieved from surgical donors with the majority sourced from femoral heads obtained post primary total hip replacement (Transplantation Society 2006). Future studies should evaluate the supply and demand of musculoskeletal allografts in Australia, including overall availability, size and composition of the national pool of cadaveric donors, and ways to increase the rate of donation. The increasing demand in musculoskeletal allograft underpins attempts to increase the supply from available donors. Data-driven analysis of the pool of potential donors is essential to evaluate the performance of tissue procurement organizations. More donors are needed to fill the growing need for tissue donation and refusal to donate remains a significant obstacle to tissue donation rates (Maloney & Altmaier. 2003). A better understanding of Australian tissue donor beliefs and motivations is needed to develop targeted interventions to improve the process, thus potentially increasing the number of families who consent to tissue donation. Recruiters must know how 55
66 motivation variables and correlation patterns differ with donor experience and gender, and then be able to develop targeted recruitment and retention strategies (Glynn et al.2006; Hupfer et al. 2005; Suarez et al. 2004). The combination of retrospective analysis of data concerning rates of musculoskeletal tissue donation and identification of factors which affect it, will lead to improved education of medical professionals and hospital staff, and greater awareness among potential donors and the general population. 56
67 REFERENCES Amin J, Gidding H, Gilbert G, Bachouse J, Kaldor JM, Dore GJ. Hepatitis C prevalence a nationwide serosurvey. Commun Dis Intell 2004; 28: Australian Therapeutic Goods Administration Code of Good Manufacturing Practice Human Blood and Tissues. Australian Therapeutic Goods Administration, Wooden ACT Australia (2000). Busch MP, Glynn SA, Stramer SL, et al. A new strategy for estimating risks of transfusion-transmitted viral infections based on rates of detection of recently infected donors. Transfusion 2005; 45(2): Busch MP, Lee LL, Satten GA, et al. Time course of detection of viral and serologic markers preceding human immunodeficiency virus type 1 seroconversion: implications for screening of blood and tissue donors. Transfusion1995; 35(2): Challine D, Pellegrin B, Bouvier-Alias M. HIV and hepatitis C virus RNA in seronegative organ and tissue donors. Lancet 2004; 364: Coste J, Reesink HW, Engelfriet CP et al. Implementation of donor screening for infectious agents transmitted by blood by nucleic acid technology: Update to Vox Sang 2005; 88: Dodd RY, Notari EP, Stramer SL. Current prevalence and incidence of infectious disease markers and estimated window-period risk in the American Red Cross blood donor population. Transfusion 2002; 42: Fleiss JL. Statistical methods for rates and proportions. 2nd edition. New York: Wiley: 1981: Galea G, Dow BC. Comparison of prevalence rates of microbiological markers between bone / tissue donations and new blood donors in Scotland. Vox Sang 2006; 91: Glynn SA, Schreiber GB, Murphy EL, Kessler D, Higgins M, Wright DJ, Mathew S, Tu Y, King M, Smith JW. Factors influencing the decision to donate: racial and ethnic comparisons. Transfusion 2006; 46: Glynn SA, Kleinman SH, Wright DJ, Busch MP. International application of the incidence rate / window period model. Transfusion 2002; 42: Hackett K. Tissue Donation, Tissue Bank Report, Halifax, Hupfer ME, Taylor DW, Letwin JA. Understanding Canadian student motivations and beliefs about giving blood. Transfusion 2005; 45: Ivory JP, Thomas IJ. Audit of a bone bank. J Bone Joint Surg 1993 ; 75B:
68 Jackson BR, Busch MP, Stramer SL, Aubuchon JP. The cost-effectiveness of NAT for HIV, HCV, and HBV in whole blood donations. Transfusion 2003; 43: Kleinman SH, Busch MP. Assessing the impact of HBV NAT on window period reduction and residual risk. J Clin Virol 36 Supplement 2006; 1: S Kleinman S, Stramer S, Mimms L et al. Comparison of Preliminary observed yield of HCV and HIV minipool (MP) nucleic acid testing (NAT) with predictions from the Incidence/Window Period (INC/WP) Model. Transfusion 2000; 40: S6-S30. Kleinman S, Busch MP, Korelitz JJ, Schreiber GB. The incidence / window period model and its use to assess the risk of transfusion-transmitted human immunodeficiency virus and hepatitis C virus infection. Transfusion Medical Review 1997; 11: Lord CF, Gebhart MC, Tomford WW, Mankin HJ. Infection in bone allografts: incidence, nature, and treatment. J Bone Joint Surg 1988; 70A: Maloney R, Altmaier EM. Caring for bereaved families: self-efficacy in the donation request process. J Clin Psychol Med Settings 2003; 10: Manns A, Wilks RJ, Murphy EL, et al. A prospective study of transmission by transfusion of HTLV-1 and risk factors associated with seroconversion. Int. J Cancer 1992; 51(6): National Centre in HIV Epidemiology and Clinical Research (NCHECR). HIV/AIDS, viral hepatitis, and sexually transmissible infections in Australia annual surveillance report. Australian Institute of Health and Welfare, ACT Australia Available from: O Sullivan BG, Gidding HF, Law M, Kaldor JM, Gilbert GL, Dore GJ. Estimates of chronic hepatitis B virus infection in Australia, Aust NZ J Public Health 2004; 28: Peterson LR, Sattern GA, Dodd R et al. Duration of time from onset of human immunodeficiency virus type 1 infectiousness to development of detectable antibody. The HIV Seroconversion Study Group. Transfusion 1994; 34: Pillonel J, Saura C, Courouce AM. Prevalence of HIV HTLV, and Hepatitis B and C viruses in blood donors in France, Transfus Clin Biol 1998; 5: Schreiber GB, Busch MP, Kleinman SH, Korelitz JJ. The risk of transfusiontransmitted viral infections. The Retrovirus Epidemiology Donor Study. N Eng J Med 1996; 334: Seed CR, Kiely P, Keller AJ. Residual risk of transfusion transmitted human immunodeficiency virus, hepatitis B virus, hepatitis C virus, and human T lymphotrophic virus. Intern Med J 2005; 35:
69 Seed CR, Cheng A, Ismay SL. Assessing the accuracy of three viral risk models in predicting the outcome of implementing HIV and HCV NAT donor screening in Australia and the implications for future HBV NAT. Transfusion 2002; 42: Suarez IMB, Fenandez-Montoya A, Fernandez AR, Lopez-Berrio A, Cillero-Penuela M. How regular blood donors explain their behaviour. Transfusion 2004; 44: Tomford WW, Thongphasuk J, Mankin HJ, Ferraro MJ. Frozen musculoskeletal allografts: a study of the clinical incidence and causes of infection with their use. J Bone Joint Surg 1990; 72A: Transplantation Society of Australia and New Zealand. Bank Activities ( ). (accessed August 2006) Tugwell B, Patel P, Williams I. Transmission of hepatitis C virus to several organ and tissue recipients from an antibody-negative donor. Ann Intern Med 2005; 143: Yao F, Seed C, Farrugia A, et al. The risk of HIV, HBV, HCV and HTLV infection among musculoskeletal tissue donors in Australia. American Journal of Transplantation 2007; 7: Zahariadis G, Plitt SS, O Brien S, Yi QL, Fan W, Preiksaitis JK. Prevalence and estimated incidence of blood-borne viral pathogen infection in organ and tissue donation from Northern Alberta. American Journal of Transplantation 2006; 7: Zou S, Dodd RY, Stramer SL, Strong DM. Probability of viremia with HBV, HCV, HIV, and HTLV among tissue donors in the United States. N Eng J Med 2004; 351: Zou S, Notari IVEP, Stramer SL, Wahab F, Musavi F, Dodd RY. Patterns of age- and sex-specific prevalence of major blood-borne infections in the United States blood donors, : American Red Cross blood donor study. Transfusion 2004; 44:
The cost-effectiveness of NAT for HIV, HCV, and HBV in whole-blood donations Jackson B R, Busch M P, Stramer S L, AuBuchon J P
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