Interpretation of pathogen load in relationship to infectivity and pathogen reduction efficacy

Transfusion

Volumn 59, Issue 3, 2019, Pages 1132-1146

  McCullough, Jeffrey ^a   Alter, Harvey J ^b   Ness, Paul M ^c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

BABESIA; BLOOD TRANSFUSION; CHIKUNGUNYA VIRUS; CYTOMEGALOVIRUS; DENGUE VIRUS; ERYTHROCYTE PRESERVATION; GENETIC VARIATION; HEPATITIS A VIRUS; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HEPATITIS E VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; INFECTION RISK; NONHUMAN; NUCLEIC ACID AMPLIFICATION; PARASITE LOAD; PARASITE VIRULENCE; PARVOVIRIDAE; PLASMODIUM MALARIAE; QUANTITATIVE ANALYSIS; REVIEW; RISK REDUCTION; SEROCONVERSION; TRYPANOSOMA CRUZI; VIRUS INACTIVATION; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS VIRULENCE; WEST NILE VIRUS; ZIKA VIRUS; BLOOD SAFETY; BLOOD STORAGE; PROCEDURES; THROMBOCYTE TRANSFUSION; VIRUS INFECTION;

BLOOD PRESERVATION; BLOOD SAFETY; HUMANS; PLATELET TRANSFUSION; VIRUS DISEASES;

EID: 85059281051     PISSN: 00411132     EISSN: 15372995     Source Type: Journal    
DOI: 10.1111/trf.15103     Document Type: Review

References (103)

1. Saldanha J, Lelie N, Heath A, et al. WHO Collaborative Study Group. Establishment of the first international standard for nucleic acid amplification technology (NAT) assays for HCV RNA. Vox Sang 1999;76:149-58.
2. Grabarczyk P, Koppelman M, Boland F, et al. Inclusion of human immunodeficiency virus type 2 (HIV-2) in a multiplex transcription-mediated amplification assay does not affect detection of HIV-1 and hepatitis B and C virus genotypes: a multicenter performance evaluation study. Transfusion 2015;55:2246-55.
3. Grabarczyk P, van Drimmelen H, Kopacz A, et al. Head-to-head comparison of two transcription-mediated amplification assay versions for detection of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 in blood donors. Transfusion 2013;53:2512-24.
4. Kleinman SH, Lelie N, Busch MP. Infectivity of human immunodeficiency virus-1, hepatitis C virus, and hepatitis B virus and risk of transmission by transfusion. Transfusion 2009;49:2454-89.
5. Allain JP, Mihaljevic I, Gonzalez-Fraile MI, et al. Infectivity of blood products from donors with occult hepatitis B virus infection. Transfusion 2013;53:1405-15.
6. Busch MP. HIV, HBV and HCV: new developments related to transfusion safety. Vox Sang 2000;78(Suppl 2):253-6.
7. Epstein JS, Vostal JG. FDA approach to evaluation of pathogen reduction technology. Transfusion 2003;43:1347-50.
8. Committee for Proprietary Medicinal Products. Note for guidance on virus validation studies: the design, contribution and interpretation of studies validating the inactivation and removal of viruses. The European Agency for the Evaluation of Medicinal Products, Human Medicines Evaluation Unit: London; 1996.
9. Goodrich RP, Custer B, Keil S, et al. Defining “adequate” pathogen reduction performance for transfused blood components. Transfusion 2010;50:1827-37.
10. Fratantoni JC, Prodouz KN, Horowitz MS. Viral inactivation of blood products. Transfusion 1990;30:480-1.
11. Zanetti AR, Bodini U, Clerici M, et al. Transfusion of red blood cells from an HIV-RNA-positive/anti-HIV-negative donor without HIV infection in the recipient. Transfusion 2007;47:1328-9.
12. Aprahamian H, Bish DR, Bish EK. Residual risk and waste in donated blood with pooled nucleic acid testing. Stat Med 2016;35:5283-301.
13. Hart H, McOmish F, Hart WG, et al. A comparison of polymerase chain reaction and an infectivity assay for human immunodeficiency virus type 1 titration during virus inactivation of blood components. Transfusion 1993;33:838-41.
14. Satake M, Taira R, Yugi H, et al. Infectivity of blood components with low hepatitis B virus DNA levels identified in a lookback program. Transfusion 2007;47:1197-205.
15. Busch MP, Kleinman SH, Tobler LH, et al. Virus and antibody dynamics in acute West Nile virus infection. J Infect Dis 2008;198:984-93.
16. Ferreira MC, Nel TJ. Differential transmission of human immunodeficiency virus (HIV) via blood components from an HIV-infected donor. Transfusion 2006;46:156-7.
17. Hewitt PE, Ijaz S, Brailsford SR, et al. Hepatitis E virus in blood components: a prevalence and transmission study in southeast England. Lancet 2014;384:1766-73.
18. Donegan E, Lenes BA, Tomasulo PA, et al. Transmission of HIV-1 by component type and duration of shelf storage before transfusion. Transfusion 1990;30:851-2.
19. Busch MP, Operskalski EA, Mosley JW, et al. Factors influencing human immunodeficiency virus type 1 transmission by blood transfusion. J Infect Dis 1996;174:26-33.
20. Weusten J, Vermeulen M, van Drimmelen H, et al. Refinement of a viral transmission risk model for blood donations in seroconversion window phase screened by nucleic acid testing in different pool sizes and repeat test algorithms. Transfusion 2011;51:203-15.
21. Cohen MS, Gay CL, Busch MP, et al. The detection of acute HIV infection. J Infect Dis 2010;202(Suppl 2):S270-7.
22. Candotti D, Grabarczyk P, Ghiazza P, et al. Characterization of occult hepatitis B virus from blood donors carrying genotype A2 or genotype D strains. J Hepatol 2008;49:537-47.
23. Yoshikawa A, Gotanda Y, Minegishi K, et al. Lengths of hepatitis B viremia and antigenemia in blood donors: preliminary evidence of occult (hepatitis B surface antigen-negative) infection in the acute stage. Transfusion 2007;47:1162-71.
24. Zhu T, Corey L, Hwangbo Y, et al. Persistence of extraordinarily low levels of genetically homogeneous human immunodeficiency virus type 1 in exposed seronegative individuals. J Virol 2003;77:6108-16.
25. Fiebig EW, Wright DJ, Rawal BD, et al. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 2003;17:1871-9.
26. Weusten JJ, van Drimmelen HA, Lelie PN. Mathematic modeling of the risk of HBV, HCV, and HIV transmission by window-phase donations not detected by NAT. Transfusion 2002;42:537-48.
27. El Ekiaby M, Moftah F, Goubran H, et al. Viremia levels in hepatitis C infection among Egyptian blood donors and implications for transmission risk with different screening scenarios. Transfusion 2015;55:1186-94.
28. Vermeulen M, Coleman C, Mitchel J, et al. Comparison of human immunodeficiency virus assays in window phase and elite controller samples: viral load distribution and implications for transmission risk. Transfusion 2013;53(10 Pt 2):2384-98.
29. Salles NA, Levi JE, Barreto CC, et al. Human immunodeficiency virus transfusion transmission despite nucleic acid testing. Transfusion 2013;53:2593-5.
30. Keil SD, Kiser P, Sullivan JJ, et al. Inactivation of Plasmodium spp. in plasma and platelet concentrates using riboflavin and ultraviolet light. Transfusion 2013;53:2278-86.
31. 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;45:254-64.
32. Biswas R, Tabor E, Hsia CC, et al. Comparative sensitivity of HBV NATs and HBsAg assays for detection of acute HBV infection. Transfusion 2003;43:788-98.
33. Stolz M, Tinguely C, Fontana S, et al. Hepatitis B virus DNA viral load determination in hepatitis B surface antigen-negative Swiss blood donors. Transfusion 2014;54:2961-7.
34. Kleinman SH, Strong DM, Tegtmeier GG, et al. Hepatitis B virus (HBV) DNA screening of blood donations in minipools with the COBAS AmpliScreen HBV test. Transfusion 2005;45:1247-57.
35. Stramer SL, Krysztof DE, Brodsky JP, et al. Sensitivity comparison of two Food and Drug Administration-licensed, triplex nucleic acid test automated assays for hepatitis B virus DNA detection and associated projections of United States yield. Transfusion 2011;51:2012-22.
36. Gonzalez R, Torres P, Castro E, et al. Efficacy of hepatitis B virus (HBV) DNA screening and characterization of acute and occult HBV infections among blood donors from Madrid, Spain. Transfusion 2010;50:221-30.
37. Ren FR, Wang JX, Huang Y, et al. Hepatitis B virus nucleic acid testing in Chinese blood donors with normal and elevated alanine aminotransferase. Transfusion 2011;51:2588-95.
38. Bouchardeau F, Girault A, Razer A, et al. Sensitivity of hepatitis B virus DNA transcription-mediated amplification testing in hepatitis B surface antigen-positive blood donations. Transfusion 2006;46:2047-52.
39. Kuhns MC, Kleinman SH, McNamara AL, et al. Lack of correlation between HBsAg and HBV DNA levels in blood donors who test positive for HBsAg and anti-HBc: implications for future HBV screening policy. Transfusion 2004;44:1332-9.
40. Kleinman SH, Kuhns MC, Todd DS, et al. Frequency of HBV DNA detection in US blood donors testing positive for the presence of anti-HBc: implications for transfusion transmission and donor screening. Transfusion 2003;43:696-704.
41. Yotsuyanagi H, Yasuda K, Moriya K, et al. Frequent presence of HBV in the sera of HBsAg-negative, anti-HBc-positive blood donors. Transfusion 2001;41:1093-9.
42. Bremer CM, Saniewski M, Wend UC, et al. Transient occult hepatitis B virus infection in a blood donor with high viremia. Transfusion 2009;49:1621-9.
43. Weusten J, van Drimmelen H, Vermeulen M, et al. A mathematical model for estimating residual transmission risk of occult hepatitis B virus infection with different blood safety scenarios. Transfusion 2017;57:841-9.
44. Matsumoto C, Tadokoro K, Fujimura K, et al. Analysis of HBV infection after blood transfusion in Japan through investigation of a comprehensive donor specimen repository. Transfusion 2001;41:878-84.
45. Hsia CC, Purcell RH, Farshid M, et al. Quantification of hepatitis B virus genomes and infectivity in human serum samples. Transfusion 2006;46:1829-35.
46. Tabuchi A, Tanaka J, Katayama K, et al. Titration of hepatitis B virus infectivity in the sera of pre-acute and late acute phases of HBV infection: transmission experiments to chimeric mice with human liver repopulated hepatocytes. J Med Virol 2008;80:2064-8.
47. Wang JT, Lee CZ, Chen PJ, et al. Transfusion-transmitted HBV infection in an endemic area: the necessity of more sensitive screening for HBV carriers. Transfusion 2002;42:1592-7.
48. Prince AM, Lee DH, Brotman B. Infectivity of blood from PCR-positive, HBsAg-negative, anti-HBs-positive cases of resolved hepatitis B infection. Transfusion 2001;41:329-32.
49. Glynn SA, Wright DJ, Kleinman SH, et al. Dynamics of viremia in early hepatitis C virus infection. Transfusion 2005;45:994-1002.
50. Nubling CM, Unger G, Chudy M, et al. Sensitivity of HCV core antigen and HCV RNA detection in the early infection phase. Transfusion 2002;42:1037-45.
51. Busch MP, Tobler LH, Gerlich WH, et al. Very low level viremia in HCV infectious unit missed by NAT. Transfusion 2003;43:1173-4.
52. Operskalski EA, Mosley JW, Tobler LH, et al. HCV viral load in anti-HCV-reactive donors and infectivity for their recipients. Transfusion 2003;43:1433-41.
53. Coste J, Levayer T, Izopet J, et al. Acute HCV infection detected in a blood donor by NAT. Transfusion 2003;43:116-8.
54. Allain JP, Owusu-Ofori AK, Assennato SM, et al. Effect of Plasmodium inactivation in whole blood on the incidence of blood transfusion-transmitted malaria in endemic regions: the African Investigation of the Mirasol System (AIMS) randomised controlled trial. Lancet 2016;387:1753-61.
55. Aubry M, Richard V, Green J, et al. Inactivation of Zika virus in plasma with amotosalen and ultraviolet A illumination. Transfusion 2016;56:33-40.
56. Mead PS, Duggal NK, Hook SA, et al. Zika virus shedding in semen of symptomatic infected men. N Engl J Med 2018;378:1377-85.
57. Feldmann H. Virus in semen and the risk of sexual transmission. N Engl J Med 2018;378:1440-1.
58. Keil SD, Saakadze N, Bowen R, et al. Riboflavin and ultraviolet light for pathogen reduction of murine cytomegalovirus in blood products. Transfusion 2015;55:858-63.
59. Roback JD, Drew WL, Laycock ME, et al. CMV DNA is rarely detected in healthy blood donors using validated PCR assays. Transfusion 2003;43:314-21.
60. Greenlee DJ, Fan H, Lawless K, et al. Quantitation of CMV by real-time PCR in transfusable RBC units. Transfusion 2002;42:403-8.
61. Roback JD, Caliendo AM, Newman JL, et al. Comparison of cytomegalovirus polymerase chain reaction and serology for screening umbilical cord blood components. Transfusion 2005;45:1722-8.
62. Ziemann M, Juhl D, Brockmann C, et al. Infectivity of blood products containing cytomegalovirus DNA: results of a lookback study in nonimmunocompromised patients. Transfusion 2017;57:1691-8.
63. Ziemann M, Juhl D, Gorg S, et al. The impact of donor cytomegalovirus DNA on transfusion strategies for at-risk patients. Transfusion 2013;53:2183-9.
64. Ziemann M, Krueger S, Maier AB, et al. High prevalence of cytomegalovirus DNA in plasma samples of blood donors in connection with seroconversion. Transfusion 2007;47:1972-83.
65. Rios M, Daniel S, Dayton AI, et al. In vitro evaluation of the protective role of human antibodies to West Nile virus (WNV) produced during natural WNV infection. J Infect Dis 2008;198:1300-8.
66. Lai L, Lee TH, Tobler L, et al. Relative distribution of West Nile virus RNA in blood compartments: implications for blood donor nucleic acid amplification technology screening. Transfusion 2012;52:447-54.
67. Lanciotti RS, Kerst AJ, Nasci RS, et al. Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol 2000;38:4066-71.
68. Harritshoj LH, Holm DK, Saekmose SG, et al. Low transfusion transmission of hepatitis E among 25,637 single-donation, nucleic acid-tested blood donors. Transfusion 2016;56:2225-32.
69. Sauleda S, Ong E, Bes M, et al. Seroprevalence of hepatitis E virus (HEV) and detection of HEV RNA with a transcription-mediated amplification assay in blood donors from Catalonia (Spain). Transfusion 2015;55:972-9.
70. Fearon MA, O'Brien SF, Delage G, et al. Hepatitis E in Canadian blood donors. Transfusion 2017;57:1420-5.
71. McCullough J. Transfusion medicine. 4th ed. West Sussex: Wiley-Blackwell; 2016.
72. Gowland P, Fontana S, Niederhauser C, et al. Molecular and serologic tracing of a transfusion-transmitted hepatitis A virus. Transfusion 2004;44:1555-61.
73. Normann A, Jung C, Vallbracht A, et al. Time course of hepatitis A viremia and viral load in the blood of human hepatitis A patients. J Med Virol 2004;72:10-6.
74. Juhl D, Özdemir M, Dreier J, et al. Look-back study on recipients of parvovirus B19 (B19V) DNA-positive blood components. Vox Sang 2015;109:305-11.
75. Juhl D, Görg S, Hennig H. Persistence of parvovirus B19 (B19V) DNA and humoral immune response in B19V-infected blood donors. Vox Sang 2014;107:226-32.
76. Slavov SN, Otaguiri KK, Covas DT, et al. Prevalence and viral load of human parvovirus B19 (B19V) among blood donors in South-East Brazil. Indian J Hematol Blood Transfus 2016;32:323-5.
77. Juhl D, Steppat D, Görg S, et al. Parvovirus B19 infections and blood counts in blood donors. Transfus Med Hemother 2014;41:52-9.
78. Lindblom A, Isa A, Norbeck O, et al. Slow clearance of human parvovirus B19 viremia following acute infection. Clin Infect Dis 2005;41:1201-3.
79. de Haan TR, Beersma MF, Claas EC, et al. Parvovirus B19 infection in pregnancy studied by maternal viral load and immune responses. Fetal Diagn Ther 2007;22:55-62.
80. Nagaharu K, Sugimoto Y, Hoshi Y, et al. Persistent symptomatic parvovirus B19 infection with severe thrombocytopenia transmitted by red blood cell transfusion containing low parvovirus B19 DNA levels. Transfusion 2017;57:1414-8.
81. Stone M, Bakkour S, Lee T, et al. Zika RNA persistence in blood and body fluids and clinical outcomes in infected donors. Transfusion 2017;4A:57.
82. Slavov SN, Hespanhol MR, Rodrigues ES, et al. Zika virus RNA detection in asymptomatic blood donors during an outbreak in the northeast region of Sao Paulo State, Brazil, 2016. Transfusion 2017;57:2897-901.
83. Musso D, Rouault E, Teissier A, et al. Molecular detection of Zika virus in blood and RNA load determination during the French Polynesian outbreak. J Med Virol 2017;89:1505-10.
84. Best K, Guedj J, Madelain V, et al. Zika plasma viral dynamics in nonhuman primates provides insights into early infection and antiviral strategies. Proc Natl Acad Sci U S A 2017;114:8847-52.
85. Faddy HM, Fryk JJ, Watterson D, et al. Riboflavin and ultraviolet light: impact on dengue virus infectivity. Vox Sang 2016;111:235-41.
86. Mohammed H, Linnen JM, Munoz-Jordan JL, et al. Dengue virus in blood donations, Puerto Rico, 2005. Transfusion 2008;48:1348-54.
87. Stramer SL, Linnen JM, Carrick JM, et al. Dengue viremia in blood donors identified by RNA and detection of dengue transfusion transmission during the 2007 dengue outbreak in Puerto Rico. Transfusion 2012;52:1657-66.
88. Chusri S, Siripaitoon P, Silpapojakul K, et al. Kinetics of chikungunya infections during an outbreak in Southern Thailand, 2008–2009. Am J Trop Med Hyg 2014;90:410-7.
89. Vanlandingham DL, Keil SD, Horne KM, et al. Photochemical inactivation of chikungunya virus in plasma and platelets using the Mirasol pathogen reduction technology system. Transfusion 2013;53:284-90.
90. Labadie K, Larcher T, Joubert C, et al. Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J Clin Invest 2010;120:894-906.
91. Simmons G, Bres V, Lu K, et al. High incidence of chikungunya virus and frequency of viremic blood donations during epidemic, Puerto Rico, USA, 2014. Emerg Infect Dis 2016;22:1221-8.
92. McKenzie FE, Jeffery GM, Collins WE. Plasmodium vivax blood-stage dynamics. J Parasitol 2002;88:521-35.
93. Owusu-Ofori A, Gadzo D, Bates I. Transfusion-transmitted malaria: donor prevalence of parasitaemia and a survey of healthcare workers knowledge and practices in a district hospital in Ghana. Malar J 2016;15:234.
94. El Chaar M, Atwal S, Freimanis GL, et al. Inactivation of Plasmodium falciparum in whole blood by riboflavin plus irradiation. Transfusion 2013;53:3174-83.
95. Leiby DA, Chung AP, Gill JE, et al. Demonstrable parasitemia among Connecticut blood donors with antibodies to Babesia microti. Transfusion 2005;45:1804-10.
96. Moritz ED, Tonnetti L, Hewins ME, et al. Description of 15 DNA-positive and antibody-negative “window-period” blood donations identified during prospective screening for Babesia microti. Transfusion 2017;57:1781-6.
97. Bloch EM, Lee TH, Krause PJ, et al. Development of a real-time polymerase chain reaction assay for sensitive detection and quantitation of Babesia microti infection. Transfusion 2013;53:2299-306.
98. Tonnetti L, Proctor MC, Reddy HL, et al. Evaluation of the Mirasol pathogen [corrected] reduction technology system against Babesia microti in apheresis platelets and plasma. Transfusion 2010;50:1019-27.
99. Kirchhoff LV. American trypanosomiasis (Chagas' disease)--a tropical disease now in the United States. N Engl J Med 1993;329:639-44.
100. Andrade LO, Andrews NW. The Trypanosoma cruzi-host-cell interplay: location, invasion, retention. Nat Rev Microbiol 2005;3:819-23.
101. Sanchez Negrette O, Mora MC, Basombrio MA. High prevalence of congenital Trypanosoma cruzi infection and family clustering in Salta, Argentina. Pediatrics 2005;115:e668-72.
102. Cardo LJ, Salata J, Mendez J, et al. Pathogen inactivation of Trypanosoma cruzi in plasma and platelet concentrates using riboflavin and ultraviolet light. Transfus Apher Sci 2007;37:131-7.
103. Kirchoff LV, Paredes P, Lomeli-Guerrero A, et al. Transfusion-associated Chagas disease (American trypanosomiasis) in Mexico: implications for transfusion medicine in the United States. Transfusion 2006;46:298.