From mad cows to sensible blood transfusion: The risk of prion transmission by labile blood components in the United Kingdom and in France

Transfusion

Volumn 49, Issue 4, 2009, Pages 797-812

  Lefrère, Jean Jacques ^b   Hewitt, Patricia ^a  

^a NHS BLOOD AND TRANSPLANT   (United Kingdom)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

BLOOD COMPONENT; BLOOD DONOR; BLOOD TRANSFUSION; BOVINE SPONGIFORM ENCEPHALOPATHY; CREUTZFELDT JAKOB DISEASE; DISEASE TRANSMISSION; FRANCE; HEREDITY; HUMAN; LEUKAPHERESIS; LEUKOCYTE; NONHUMAN; PLASMA; PREVALENCE; RECIPIENT; REVIEW; RISK; SCREENING TEST; UNITED KINGDOM;

ANIMALS; BLOOD COMPONENT TRANSFUSION; BLOOD TRANSFUSION; CATTLE; ENCEPHALOPATHY, BOVINE SPONGIFORM; FRANCE; GREAT BRITAIN; HUMANS; PRION DISEASES; PRIONS; PROTEIN STABILITY; RISK FACTORS; TEMPERATURE;

EID: 62949173759     PISSN: 00411132     EISSN: 15372995     Source Type: Journal    
DOI: 10.1111/j.1537-2995.2008.02044.x     Document Type: Review

References (101)

1. Wells GA, Scott AC, Johnson CT, Gunning RF, Hancock RD, Jeffrey M, Dawson M, Bradley R. A novel progressive spongiform encephalopathy in cattle. Vet Rec 1987 121 : 419 20.
2. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982 216 : 136 44.
3. Diener TO, McKinkley MP, Prusiner SB. Viroids and prions. Proc Natl Acad Sci U S A 1982 79 : 5220 4.
4. Baskakov IV. The reconstitution of mammalian prion infectivity de novo. FEBS 2007 274 : 576 87.
5. Oesch B, Westaway D, Walchli M, McKinley MP, Kent SB, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE, Prusiner SB, Weissman C. A cellular gene encodes scrapie PrP 27-30 protein. Cell 1985 40 : 735 46.
6. Prusiner SB. Prions. Proc Natl Acad Sci U S A 1998 95 : 13363 83.
7. Holman RC, Khan AS, Belay ED, Schonberger ED. Creutzfeldt-Jakob disease in the United States, 1979-1994: using national mortality data to assess the possible occurrence of variant cases. Emerg Infect Dis 1996 2 : 333 7.
8. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, McCardle L, Chree A, Hope J, Birkett C, Cousens S, Fraser H, Bostock CJ. Transmissions to mice indicate that "new variants" CJD is caused by the BSE agent. Nature 1997 389 : 498 501.
9. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, Poser S, Pocchiari M, Hofman A, Smith PG. A new variant of CJD in the UK. Lancet 1996 347 : 921 5.
10. Will RG, Zeidler M, Stewart GE, Macleod MA, Ironside JW, Cousens SN, Mackenzie J, Estibeiro K, Green AJ, Knight RS. Diagnosis of new variant of Creutzfeldt-Jakob disease. Ann Neurol 2000 47 : 575 82.
11. Wadsworth JD, Joiner S, Hill AF, Campbell TA, Desbruslais M, Luthert PJ, Collinge J. Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 2001 358 : 171 80.
12. Wadsworth JD, Asante EA, Desbrulais M, Linehan JM, Joiner S, Gowland I, Welch J, Stone L, Lloyd SE, Hill AF, Brandner S, Collinge J. Human prion protein with valine 129 prevents expression of variant CJD phenotype. Science 2004 306 : 1793 6.
13. Bishop MT, Hart P, Aitchison L, Baybutt HN, Plinston C, Thomson V, Tuzi NL, Head MW, Ironside JW, Will RG, Manson JC. Predicting susceptibility and incubation time of human-to-human transmission of vCJD. Lancet Neurol 2006 5 : 393 8.
14. Ghani AC, Ferguson NM, Donnelly CA, Anderson RM. Factors determining the pattern of the variant Creutzfeldt-Jakob disease (vCJD) epidemic in the UK. Proc Biol Sci 2003 270 : 689 98.
15. Ironside JW, Bishop MT, Connolly K, Hegazy D, Lowrie S, Le Grice M, Ritchie DL, McCardle LM, Hilton DA. Variant Creutzfeldt-Jakob disease: prion protein genotype analysis of positive appendix tissue samples from a retrospective prevalence study. BMJ 2006 332 : 1186 8.
16. Ward HJ, Everington D, Cousens SN, Smith-Bathgate B, Leitch M, Cooper S, Heath C Knight RS, Smith PG, Will RG. Risk factors for variant Creutzfeldt-Jakob disease: a case-control study. Ann Neurol 2006 59 : 111 20.
17. Brandel JP, Salomon D, Alpérovitch A. Epidémiologie de la variante de la maladie de Creutzfeldt-Jakob en France. Transfus Clin Biol 2006 13 : 304 6.
18. Chadeau-Hyam M, Tard A, Bird S, Le Guennec S, Bemrah N, Volatier JL, Alpérovitch A. Estimation of the exposure of the French population to the BSE agent: comparison of the 1980-95 consumption of beef products containing mechanically recovered meat in France and the UK, by birth cohort and gender. Stat Methods Med Res 2003 12 : 247 60.
19. Alperovitch A, Will RG. Predicting the size of the vCJD epidemic in France. CR Biol 2002 325 : 33 6.
20. Cooper JD, Bird SM. UK bovine carcass meat consumed as burgers, sausages and other meat products: by birth cohort and gender. J Cancer Epidemiol Prev 2002 7 : 49 52.
21. Chadeau-Hyam M, Alperovitch A. Risk of variant Creutzfeldt-Jakob disease in France. Int J Epidemiol 2005 34 : 46 52.
22. Hilton D, Ghani A, Conyers L, Edwards P, McCardle L, Ritchie D, Penney M, Hegazy D, Ironside JW. Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J Pathal 2004 203 : 733 9.
23. Valleron AJ, Boelle PY, Will R, Cesbron JY. Estimation of epidemic size and incubation time based on age characteristics of vCJD in the United Kingdom. Science 2001 294 : 1726 8.
24. Ricketts MN, Cashman NR, Stratton EE, El-Saadany S. Is Creutzfeldt-Jakob disease transmitted in blood? Emerg Infect Dis 1997 3 : 155 63.
25. Kondo K, Kuriowa Y. A case control study of Creutzfeldt-Jakob disease: association with physical injuries. Ann Neurol 1982 11 : 377 81.
26. Davanipour Z, Alter M, Sobel E, Asher DM, Gajdusek DC. A case-control study of Creutzfeldt-Jakob disease: dietary risk factors. Am J Epidemiol 1985 122 : 443 51.
27. Head MW, Ritchie D, Smith N, McLoughlin V, Nailon W, Samad S, Masson S, Bishop M, McCardle L, Ironside JW. Peripheral tissue involvement in sporadic, iatrogenic, and variant Creutzfeldt-Jakob disease: an immunohistochemical, quantitative, and biochemical study. Am J Pathol 2004 164 : 143 53.
28. Dodd R, Sullivan M. Creutzfeld-Jakob disease and transfusion safety: tilting at icebergs? Transfusion 1998 38 : 221 3.
29. Evatt B, Austin H, Barnhart E, Schonberger L, Sharer L, Jones R, DeArmond S. Surveillance for Creutzfeldt-Jakob disease among persons with hemophilia. Transfusion 1998 38 : 817 20.
30. Hoey J, Giuluvi A, Todkill AM. New variant Creutzfeldt-Jakob disease and the blood supply: is it time to face music? Can Med Assoc J 1998 159 : 669 70.
31. Turner ML, Ironside JW. New-variant Creutzfeldt-Jakob disease: the risk of transmission by blood transfusion. Blood Rev 1998 12 : 255 68.
32. Aguzzi A, Heppner FL, Heikenwalder M, Pronz M, Seeger H, Glatzel M. Immune system and peripheral nerves in propagation of prions to CNS. Br Med Bull 2003 66 : 141 59.
33. Bruce ME, McConnell I, Will RG, Ironside JW. Detection of variant Creutzfeldt-Jakob disease (vCJD) infectivity in extraneural tissues. Lancet 2001 358 : 208 9.
34. Brown P. Can Creutzfeldt-Jakob disease be transmitted by transfusion? Curr Opin Hematol 1995 2 : 472 7.
35. Cervenakova L, Yakovleva O, McKenzie C, Kolchinsky S, McShane L, Drohan WN, Brown P. Similar levels of infectivity in the blood of mice infected with human-derived vCJD and GSS strains of transmissible spongiform encephalopathy. Transfusion 2003 43 : 1687 94.
36. Brown P, Rohwer RG, Dunstan BC, MacAuley C, Gajdusek DC, Drohan WN. The distribution of infectivity in blood components and plasma derivatives in experimental models of transmissible spongiform encephalopathy. Transfusion 1998 38 : 810 8166.
37. Houston F, Foster JD, Chong A, Hunter N, Bostock CJ. Transmission of BSE by blood transfusion in sheep. Lancet 2000 356 : 999 1000.
38. Hunter N, Foster J, Chong A, McCutcheon S, Parnham D, Eaton S, MacKenzie C, Houston F. Transmission of prion diseases by blood transfusion. J Gen Virol 2002 83 : 2897 905.
39. Saa P, Castilla J, Soto C. Presymptomatic detection of prions in blood. Science 2006 313 : 92 4.
40. Cousens SN, Zeidler M, Esmonde TF, DeSilva R, Wilesmith JW, Smith PG, Will RG. Sporadic Creutzfeldt-Jakob disease in the United Kingdom: analysis of epidemiological surveillance data for 1970-1996. Br Med J 1997 315 : 389 95.
41. Hewitt P. vCJD and transfusion in the United Kingdom. Transfus Clin Biol 2006 13 : 312 6.
42. Hewitt PE, Llewelyn CA, Mackenzie J, Will RG. Creutzfeldt-Jakob disease and blood transfusion: results of the UK Transfusion Medicine Epidemiological Review study. Vox Sang 2006 91 : 221 30.
43. Heye N, Hensen S, Muller N. Creutzfeldt-Jakob disease and blood transfusion. Lancet 1994 343 : 298 9.
44. Wilson K, Code C, Ricketts MN. Risk of acquiring Creutzfeldt-Jakob disease from blood transfusions: systematic review of case-control studies. BMJ 2000 321 : 17 9.
45. Esmonde TFG, Will RG, Slattery JM, Knight R, Harries-Jones R, DeSilva R, Matthews WB. Creutzfeldt-Jakob disease and blood transfusion. Lancet 1993 341 : 205 7.
46. VanDuijn CM, Delasnerie-Laupretre N, Masullo C, Zerr I, Silva R de, Wientjes DPWM, Brandel J-P, Weber T, Bonavita V, Zeidler M, Alpérovitch A, Poser S, Granieri E, Hofman A, Will RG,. Case-control study of risk factors of Creutzfeldt-Jakob disease in Europe during 1993-1995. Lancet 1998 : 353 : 1081 5.
47. Collins S, Law MG, Fletcher A, Boyd A, Kaldor J, Masters CL. Surgical treatment and risk of sporadic Creutzfeldt-Jakob disease: a case-control study. Lancet 1999 353 : 693 7.
48. Llewelyn CA, Hewitt PA, Knight RSG, Amar K, Cousens S, Mackenzie J, Will RG. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 2004 363 : 417 21.
49. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 2004 364 : 527 9.
50. Health Protection Agency. New case of transfusion-associated variant-CJD. CDR Wkly 2006 16 : 2 3.
51. Wroe SJ, Pal S, Siddique D, Hyare H, Macfarlane R, Joiner S, Linehan JM, Brandner S, Wadsworth JD, Hewitt P, Collinge J. Clinical presentation and pre-mortem diagnosis of blood transfusion-associated variant CJD. Lancet 2006 368 : 2061 7.
52. Editorial team. Fourth case of transfusion-associated vCJD infection in the United Kingdom. Euro Surveill 2007 12 : E070118.4.
53. Brown P, Preece M, Brandel JP, Sato T, McShane L, Zerr I, Fletcher A, Will RG, Pocchiari M, Cashman NR, d'Aignaux JH, Cervenakova L, Fradkin J, Schonberger LB, Collins SJ. Iatrogenic Creutzfeldt-Jakob disease at the millennium. Neurology 2000 55 : 1075 81.
54. Johnston R. Prion diseases. Lancet Neurol 2005 4 : 635 42.
55. Wilson K, Ricketts MN. A third episode of transfusion-derived vCJD. Lancet 2006 368 : 2037 9.
56. Prowse CV, Bailey A. Validation of prion removal by leucocyte-depleting filters: a cautionary tale. Vox Sang 2000 79 : 248.
57. Gregori L, McCombie N, Palmer D, Birch P, Sowemimo-Coker SO, Giulivi A, Rohwer RG. Effectiveness of leucoreduction for removal of infectivity of transmissible spongiform encephalopathies from blood. Lancet 2004 364 : 529 31.
58. Ludlam CA, Turner ML. Managing the risk of transmission of variant Creutzfeldt-Jakob disease by blood products. Br J Haemat 2005 132 : 13 24.
59. Prowse C. Controlling the blood-borne spread of human prion disease. ISBT Sci Ser 2006 1 : 21 4.
60. Circulaire N° DGS/SD5C/DHOS/2005/435 du 23 septembre 2005 relative aux recommandations pour le traitement des dispositifs médicaux utilisés chez les sujets ayant reçu des produits sanguins labiles (PSL) provenant de donneurs rétrospectivement atteints de variant de la maladie de Creutzfeldt-Jakob (vMCJ). Bull Officiel Santé 2005 n° 10.
61. Wilson K, Ricketts MN. Transfusion transmission of vCJD: a crisis avoided. Lancet 2004 364 : 477 9.
62. Murphy EL, Connor D, McEvoy P, Hirschler N, Busch MP, Roberts P, Nguyen KA, Reich P. Estimating blood donor loss due to the variant CJD travel deferral. Transfusion 2004 44 : 645 50.
63. Farrugia A, Ironside JW, Giangrande P. Variant Creutzfeldt-Jakob disease transmission by plasma products: assessing and communicating risk in an era of scientific uncertainty. Vox Sang 2005 89 : 186 92.
64. Wilson K, Ricketts MN. The success of precaution? Managing the risk of transfusion transmission of variant Creutzfeldt-Jakob disease. Transfusion 2004 44 : 1475 8.
65. Wilson K, Wilson M, Hebert PC, Graham I. The application of the precautionary principle to the blood system: the Canadian blood system's vCJD donor deferral policy. Transfus Med Rev 2003 17 : 89 94.
66. O'Brien S, Chiavetta JA, Goldman M, Fan W, Nair RC, Sher GD, Vamvakas EC. Predictive ability of sequential surveys in determining donor loss from increasingly stringent variant Creutzfeldt-Jakob disease defferal policies. Transfusion 46 : 461 8.
67. Martin M, Legras JF, Pouchol E, Trouvin J.H. Evaluation du risque transfusionnel vis-à-vis de la variante de la maladie de Creutzfeldt-Jakob en France. Transfus Clin Biol 2006 13 : 298 303.
68. Houston F, McCutcheon S, Goldmann W, Chong A, Foster J, Siso S, Gonzalez L, Jeffrey M, Hunter N. Prion diseases are efficiently transmitted by blood transfusion in sheep. Blood 2008 July 22. [Epub ahead of print SA, Bennett PG. VCJD and blood transfusion: risk assessment in the United Kingdom. Transfus Clin Biol 2006 13 : 307 11.
69. Siso S, Gonzalez L, Houston F, Hunter N, Martin S, Jeffrey M. The neuropathologic phenotype of experimental ovine BSE is maintained after blood transfusion. Blood 2006 108 : 745 8.
70. Brown P, Cervenakova L, McShane LM, Barber P, Rubenstein R, Drohan WN. Further studies of blood infectivity in an experimental model of transmissible spongiform encephalopathy, with an explanation of why blood components do not transmit Creutzfeldt-Jakob disease in humans. Transfusion 1999 39 : 1169 78.
71. Brown P. Blood infectivity, processing and screening tests in transmissible spongiform encephalopathy. Vox Sang 2005 89 : 63 70.
72. Holada K, Vostal JG, Theisen PW, MacSulay C, Gregori L, Rowher RG. Scrapie infectivity in hamster blood is not associated with platelets. J Virol 2002 76 : 4649 50.
73. Prowse C. Prion removal with filters. ISBT Sci Ser 2006 1 : 193 7.
74. Sowemimo-Coker S, Kascsak R, Kim A, Andrade F, Pesci S, Kascsak R, Meeker C, Carp R, Brown P. Removal of exogenous (spiked) and endogenous prion infectivity from red cells with a new prototype of leukoreduction filter. Transfusion 2005 45 : 1839 44.
75. Sowemimo-Coker SO, Pesci S, Andrade F, Kim A, Kascsak RB, Kascsak RJ, Meeker C, Carp R. Pall leukotrap affinity prion-reduction filter removes exogenous infectious prions and endogenous infectivity from red cell concentrates. Vox Sang 2006 90 : 265 75.
76. Cervia JS, Sowemimo-Coker SO, Ortolano GA, Wilkins K, Schaffer J, Wortham ST. An overview of prion biology and the role of blood filtration in reducing the risk of transfusion-transmitted variant Creutzfeldt-Jakob disease. Transfus Med Rev 2006 20 : 190 206.
77. Gregori L, Lambert BC, Gurgel PV, Gheorghiu L, Edwardson P, Lathrop JT, Macauley C, Carbonell RG, Burton SJ, Hammond D, Rohwer RG. Reduction of transmissible spongiform encephalopathy infectivity from human red blood cells with prion protein affinity ligands. Transfusion 2006 46 : 1152 61.
78. Gregori L, Gurgel P, Lathrop JT, Edwardson P, Lambert BC, Carbonell RG, Burton SJ, Hammond DJ, Rohwer RG. Reduction in infectivity of endogenous transmissible spongiform encephalopathies present in blood by adsorption to selective affinity resins. Lancet 2006 368 : 2226 30.
79. Turner ML. Prion reduction filters. Lancet 2006 368 : 2190 1.
80. Silviera JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, Caughey B. The most infectious prion particles. Nature 2005 437 : 257 61.
81. Dodd R. Bovine spongiform encephalopathy, variant CJD, and blood transfusion: beefer madness? Transfusion 2004 44 : 628 30.
82. Zerr I, Bodemer M, Gefeller O, Otto M, Poser S, Wiltfang J, Windl O, Kretzschmar HA, Weber T. Detection of the 14-3-3 protein in the cerebrospinal fluid supports the diagnosis of Creutzfeldt-Jakob disease. Ann Neurol 1998 43 : 32 40.
83. Otto M, Wiltfang J, Schulz E, Zerr I, Otto A, Pfahlberg A, Gefeller O, Uhr M, Giese A, Weber T, Kretzschmar HA, Poser S. Diagnosis of Creutzfeldt-Jakob disease by measurement of S100 protein in serum; prospective case control study. BMJ 1998 316 : 577 82.
84. Miele G, Manson J, Clinton M. A novel erythroid-specific marker of transmissible spongiform encephalopathies. Nature 2001 7 : 361 4.
85. Barnard G, Helmick B, Maden S, Gilbourne C, Patel R. The measurement of prion protein in bovine brain tissue differential extraction and Delfia as a diagnostic test for BSE. Luminescence 2000 15 : 1 6.
86. Safar JG, Scott M, Monahan J, Deering C, Didorenko S, Vergara J, Ball H, Legname G, Leclerc E, Solforosi L, Serban H, Groth D, Burton DR, Prusiner SB, Williamson RA. Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nat Biotechnol 2002 20 : 1147 50.
87. Bellon A, Seyfort-Brandt W, Lang H, Baron H, Vey M. Improved conformation dependent immunoassay: suitability for human prion detection with enhanced sensitivity. J Gen Virol 2003 84 : 1921 5.
88. Schmerr MJ, Jenny AL, Bolgin MS, Miller JM, Hami AN, Cutlipp RC, Goodwin CR. Use of capillary electrophoresis and fluorescent labelled peptide to detect the abnormal prion protein in the blood of animals that are infected with a transmissible spongiform encephalopathy. J Chromatogr 1999 853 : 207 14.
89. Safar JG, Geschwind MD, Deering C, Didorenko S, Sattavat M, Sanchez H, Serban A, Vey M, Baron H, Giles K, Miller BL, Dearmond SJ, Prusiner SB. Diagnosis of human prion disease. Proc Natl Acad Sci U S A 2005 102 : 3501 6.
90. Brown P, Cervenakova L. The modern landscape of transfusion-related iatrogenic Creutzfeldt-Jakob disease and blood screening tests. Curr Opin Hematol 2004 11 : 351 6.
91. MacGregor IR. Screening assays for transmissible spongiform encephalopathies. Vox Sang 2004 87 : 3 6.
92. Minor PD. Technical aspects of the development and validation of tests for variant Creutzfeldt-Jakob disease in blood transfusion. Vox Sang 2004 86 : 164 70.
93. Cooper JK, Ladhani K, Minor D. Reference materials for the evaluation of pre-mortem variant Creutzfeldt-Jakob disease diagnostic assays. Vox Sang 2007 92 : 302 10.
94. Fagge T, Barclay GR, MacGregor I, Head M, Ironside J, Turner M. Variation in concentration of prion protein in the peripheral blood of patients with variant and sporadic Creutzfeldt-Jakob disease detected by dissociation enhanced lanthanide fluoroimmunoassay and flow cytometry. Transfusion 2005 45 : 504 13.
95. Turner ML. Transfusion safety with regards to prions: ethical, legal and societal considerations. Transfus Clin Biol 2007 13 : 317 9.
96. Lefrère JJ. The BOTIA project ("Blood and Organ Transmissible Infectious Agents"): a European collection of blood samples and an observatory of agents transmitted by blood transfusion or organ transplantation. Transfus Clin Biol 2005 12 : 93 4.
97. Valleron AJ, Boelle PY, Chatignoux E, Cesbron JY. Can a second wave of new variant of the CJD be discarded in absence of observation of clinical non Met-Met cases? Rev Epidemiol Sante Publique 2006 54 : 111 5.
98. Dietz K, Raddatz G, Wallis J, Müller N, Zerr I, Duerr HP, Lefèvre H, Seifried E, Löwer J. Blood transfusion and spread of variant Creutzfeldt-Jakob disease. Emerg Infect Dis 2007 13 : 89 96.
99. Hartemann P et le Comité européen SCENHIR. Actualités sur le risque iatrogène d'infection par agent à transmission non conventionnelle lors de la transfusion sanguine et d'un acte invasif. Hygiènes 2006 14 : 417 22.
100. Eglin RP, Murphy WG. Beyond leukodepletion: removing infectious prions by filtration. Transfusion 2005 45 : 1836 8.
101. Mabbott N, Turner M. Prions and the blood and immune systems. Haematologica 2005 90 : 542 8.