Impact of human herpes virus 6 in liver transplantation

World Journal of Hepatology

Volumn 2, Issue 9, 2010, Pages 345-353

  Razonable, Raymund R ^a   Lautenschlager, Irmeli ^a  

^a MAYO CLINIC   (United States)

Author keywords

Antivirals; Human herpes virus 6; Liver transplantation; Opportunistic infections

Indexed keywords

EID: 79959960916     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v2.i9.345     Document Type: Article

References (92)

1. Salahuddin SZ, Ablashi DV, Markham PD, Josephs SF, Sturzenegger S, Kaplan M, Halligan G, Biberfeld P, Wong-Staal F, Kramarsky B. Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science 1986; 234: 596-601
2. Yamanishi K, Okuno T, Shiraki K, Takahashi M, Kondo T, Asano Y, Kurata T. Identification of human herpesvirus-6 as a causal agent for exanthem subitum. Lancet 1988; 1: 1065-1067
3. Zerr DM, Meier AS, Selke SS, Frenkel LM, Huang ML, Wald A, Rhoads MP, Nguy L, Bornemann R, Morrow RA, Corey L. A population-based study of primary human herpesvirus 6 infection. N Engl J Med 2005; 352: 768-776
4. Pruksananonda P, Hall CB, Insel RA, McIntyre K, Pellett PE, Long CE, Schnabel KC, Pincus PH, Stamey FR, Dambaugh TR. Primary human herpesvirus 6 infection in young children. N Engl J Med 1992; 326: 1445-1450
5. Hall CB, Long CE, Schnabel KC, Caserta MT, McIntyre KM, Costanzo MA, Knott A, Dewhurst S, Insel RA, Epstein LG. Human herpesvirus-6 infection in children. A prospective study of complications and reactivation. N Engl J Med 1994; 331: 432-438
6. Ablashi DV, Balachandran N, Josephs SF, Hung CL, Krueger GR, Kramarsky B, Salahuddin SZ, Gallo RC. Genomic polymorphism, growth properties, and immunologic variations in human herpesvirus-6 isolates. Virology 1991; 184: 545-552
7. Schirmer EC, Wyatt LS, Yamanishi K, Rodriguez WJ, Frenkel N. Differentiation between two distinct classes of viruses now classified as human herpesvirus 6. Proc Natl Acad Sci USA 1991; 88: 5922-5926
8. Lindquester GJ, O'Brian JJ, Anton ED, Greenamoyer CA, Pellett PE, Dambaugh TR. Genetic content of a 20.9 kb segment of human herpesvirus 6B strain Z29 spanning the homologs of human herpesvirus 6A genes U40-57 and containing the origin of DNA replication. Arch Virol 1997; 142: 103-123
9. Gompels UA, Nicholas J, Lawrence G, Jones M, Thomson BJ, Martin ME, Efstathiou S, Craxton M, Macaulay HA. The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 1995; 209: 29-51
10. Levy JA, Ferro F, Greenspan D, Lennette ET. Frequent isolation of HHV-6 from saliva and high seroprevalence of the virus in the population. Lancet 1990; 335: 1047-1050
11. Dewhurst S, McIntyre K, Schnabel K, Hall CB. Human herpesvirus 6 (HHV-6) variant B accounts for the majority of symptomatic primary HHV-6 infections in a population of U.S. infants. J Clin Microbiol 1993; 31: 416-418
12. Razonable RR, Fanning C, Brown RA, Espy MJ, Rivero A, Wilson J, Kremers W, Smith TF, Paya CV. Selective reactivation of human herpesvirus 6 variant a occurs in critically ill immunocompetent hosts. J Infect Dis 2002; 185: 110-113
13. Knox KK, Harrington DP, Carrigan DR. Fulminant human herpesvirus six encephalitis in a human immunodeficiency virus-infected infant. J Med Virol 1995; 45: 288-292
14. Takahashi K, Sonoda S, Higashi K, Kondo T, Takahashi H, Takahashi M, Yamanishi K. Predominant CD4 T-lymphocyte tropism of human herpesvirus 6-related virus. J Virol 1989; 63: 3161-3163
15. Santoro F, Kennedy PE, Locatelli G, Malnati MS, Berger EA, Lusso P. CD46 is a cellular receptor for human herpesvirus 6. Cell 1999; 99: 817-827
16. Kondo K, Kondo T, Okuno T, Takahashi M, Yamanishi K. Latent human herpesvirus 6 infection of human monocytes/ macrophages. J Gen Virol 1991; 72 ( Pt 6): 1401-1408
17. He J, McCarthy M, Zhou Y, Chandran B, Wood C. Infection of primary human fetal astrocytes by human herpesvirus 6. J Virol 1996; 70: 1296-1300
18. Caruso A, Rotola A, Comar M, Favilli F, Galvan M, Tosetti M, Campello C, Caselli E, Alessandri G, Grassi M, Garrafa E, Cassai E, Di Luca D. HHV-6 infects human aortic and heart microvascular endothelial cells, increasing their ability to secrete proinflammatory chemokines. J Med Virol 2002; 67: 528-533
19. Chen M, Popescu N, Woodworth C, Berneman Z, Corbellino M, Lusso P, Ablashi DV, DiPaolo JA. Human herpesvirus 6 infects cervical epithelial cells and transactivates human papillomavirus gene expression. J Virol 1994; 68: 1173-1178
20. Luka J, Okano M, Thiele G. Isolation of human herpesvirus-6 from clinical specimens using human fibroblast cultures. J Clin Lab Anal 1990; 4: 483-486
21. Luppi M, Barozzi P, Maiorana A, Marasca R, Torelli G. Human herpesvirus 6 infection in normal human brain tissue. J Infect Dis 1994; 169: 943-944
22. Luppi M, Barozzi P, Marasca R, Torelli G. Integration of human herpesvirus-6 (HHV-6) genome in chromosome 17 in two lymphoma patients. Leukemia 1994; 8 Suppl 1: S41-S45
23. Fox JD, Briggs M, Ward PA, Tedder RS. Human herpesvirus 6 in salivary glands. Lancet 1990; 336: 590-593
24. Roush KS, Domiati-Saad RK, Margraf LR, Krisher K, Scheuermann RH, Rogers BB, Dawson DB. Prevalence and cellular reservoir of latent human herpesvirus 6 in tonsillar lymphoid tissue. Am J Clin Pathol 2001; 116: 648-654
25. Hammerling JA, Lambrecht RS, Kehl KS, Carrigan DR. Prevalence of human herpesvirus 6 in lung tissue from children with pneumonitis. J Clin Pathol 1996; 49: 802-804
26. Gupta M, Diaz-Mitoma F, Feber J, Shaw L, Forget C, Filler G. Tissue HHV6 and 7 determination in pediatric solid organ recipients--a pilot study. Pediatr Transplant 2003; 7: 458-463
27. Ozaki Y, Tajiri H, Tanaka-Taya K, Mushiake S, Kimoto A, Yamanishi K, Okada S. Frequent detection of the human herpesvirus 6-specific genomes in the livers of children with various liver diseases. J Clin Microbiol 2001; 39: 2173-2177
28. Grivel JC, Santoro F, Chen S, Fagá G, Malnati MS, Ito Y, Margolis L, Lusso P. Pathogenic effects of human herpesvirus 6 in human lymphoid tissue ex vivo. J Virol 2003; 77: 8280-8289
29. Lusso P, Malnati MS, Garzino-Demo A, Crowley RW, Long EO, Gallo RC. Infection of natural killer cells by human herpesvirus 6. Nature 1993; 362: 458-462
30. Luppi M, Barozzi P, Morris C, Maiorana A, Garber R, Bonacorsi G, Donelli A, Marasca R, Tabilio A, Torelli G. Human herpesvirus 6 latently infects early bone marrow progenitors in vivo. J Virol 1999; 73: 754-759
31. Leong HN, Tuke PW, Tedder RS, Khanom AB, Eglin RP, Atkinson CE, Ward KN, Griffiths PD, Clark DA. The prevalence of chromosomally integrated human herpesvirus 6 genomes in the blood of UK blood donors. J Med Virol 2007; 79: 45-51
32. Tanaka-Taya K, Sashihara J, Kurahashi H, Amo K, Miyagawa H, Kondo K, Okada S, Yamanishi K. Human herpesvirus 6 (HHV-6) is transmitted from parent to child in an integrated form and characterization of cases with chromosomally integrated HHV-6 DNA. J Med Virol 2004; 73: 465-473
33. Hall CB, Caserta MT, Schnabel K, Shelley LM, Marino AS, Carnahan JA, Yoo C, Lofthus GK, McDermott MP. Chromosomal integration of human herpesvirus 6 is the major mode of congenital human herpesvirus 6 infection. Pediatrics 2008; 122: 513-520
34. Luppi M, Barozzi P, Bosco R, Vallerini D, Potenza L, Forghieri F, Torelli G. Human herpesvirus 6 latency characterized by high viral load: chromosomal integration in many, but not all, cells. J Infect Dis 2006; 194: 1020-1021; author reply 1021-1023
35. Ward KN, Leong HN, Nacheva EP, Howard J, Atkinson CE, Davies NW, Griffiths PD, Clark DA. Human herpesvirus 6 chromosomal integration in immunocompetent patients results in high levels of viral DNA in blood, sera, and hair follicles. J Clin Microbiol 2006; 44: 1571-1574
36. Bandobashi K, Daibata M, Kamioka M, Tanaka Y, Kubonishi I, Taguchi H, Ohtsuki Y, Miyoshi I. Human herpesvirus 6 (HHV-6)-positive Burkitt's lymphoma: establishment of a novel cell line infected with HHV-6. Blood 1997; 90: 1200-1207
37. Daibata M, Taguchi T, Kamioka M, Kubonishi I, Taguchi H, Miyoshi I. Identification of integrated human herpesvirus 6 DNA in early pre-B cell acute lymphoblastic leukemia. Leukemia 1998; 12: 1002-1004
38. Feldstein AE, Razonable RR, Boyce TG, Freese DK, El-Youssef M, Perrault J, Paya CV, Ishitani MB. Prevalence and clinical significance of human herpesviruses 6 and 7 active infection in pediatric liver transplant patients. Pediatr Transplant 2003; 7: 125-129
39. Rossi C, Delforge ML, Jacobs F, Wissing M, Pradier O, Remmelink M, Byl B, Thys JP, Liesnard C. Fatal primary infection due to human herpesvirus 6 variant A in a renal transplant recipient. Transplantation 2001; 71: 288-292
40. Revest M, Camus C, D'Halluin PN, Cha S, Compagnon P, Boudjema K, Colimon R, Thomas R. Fatal human herpes virus 6 primary infection after liver transplantation. Transplantation 2007; 83: 1404-1405
41. Potenza L, Luppi M, Barozzi P, Rossi G, Cocchi S, Codeluppi M, Pecorari M, Masetti M, Di Benedetto F, Gennari W, Portolani M, Gerunda GE, Lazzarotto T, Landini MP, Schulz TF, Torelli G, Guaraldi G. HHV-6A in syncytial giant-cell hepatitis. N Engl J Med 2008; 359: 593-602
42. Dockrell DH, Paya CV. Human herpesvirus-6 and -7 in transplantation. Rev Med Virol 2001; 11: 23-36
43. Mendez JC, Dockrell DH, Espy MJ, Smith TF, Wilson JA, Harmsen WS, Ilstrup D, Paya CV. Human beta-herpesvirus interactions in solid organ transplant recipients. J Infect Dis 2001; 183: 179-184
44. Emery VC. Human herpesviruses 6 and 7 in solid organ transplant recipients. Clin Infect Dis 2001; 32: 1357-1360
45. Razonable RR, Brown RA, Humar A, Covington E, Alecock E, Paya CV. Herpesvirus infections in solid organ transplant patients at high risk of primary cytomegalovirus disease. J Infect Dis 2005; 192: 1331-1339
46. Razonable RR, Zerr DM. HHV-6, HHV-7 and HHV-8 in solid organ transplant recipients. Am J Transplant 2009; 9 Suppl 4: S97-S100
47. Lautenschlager I, Höckerstedt K, Linnavuori K, Taskinen E. Human herpesvirus-6 infection after liver transplantation. Clin Infect Dis 1998; 26: 702-707
48. Singh N, Carrigan DR, Gayowski T, Singh J, Marino IR. Variant B human herpesvirus-6 associated febrile dermatosis with thrombocytopenia and encephalopathy in a liver transplant recipient. Transplantation 1995; 60: 1355-1357
49. Jacobs U, Ferber J, Klehr HU. Severe allograft dysfunction after OKT3-induced human herpes virus-6 reactivation. Transplant Proc 1994; 26: 3121
50. Peleg AY, Husain S, Kwak EJ, Silveira FP, Ndirangu M, Tran J, Shutt KA, Shapiro R, Thai N, Abu-Elmagd K, McCurry KR, Marcos A, Paterson DL. Opportunistic infections in 547 organ transplant recipients receiving alemtuzumab, a humanized monoclonal CD-52 antibody. Clin Infect Dis 2007; 44: 204-212
51. Härmä M, Höckerstedt K, Krogerus L, Lautenschlager I. Pretransplant human herpesvirus 6 infection of patients with acute liver failure is a risk factor for posttransplant human herpesvirus 6 infection of the liver. Transplantation 2006; 81: 367-372
52. Schmidt CA, Wilbron F, Weiss K, Brinkmann V, Oettle H, Lohmann R, Langrehr JM, Neuhaus P, Siegert W. A prospective study of human herpesvirus type 6 detected by polymerase chain reaction after liver transplantation. Transplantation 1996; 61: 662-664
53. Griffiths PD, Ait-Khaled M, Bearcroft CP, Clark DA, Quaglia A, Davies SE, Burroughs AK, Rolles K, Kidd IM, Knight SN, Noibi SM, Cope AV, Phillips AN, Emery VC. Human herpesviruses 6 and 7 as potential pathogens after liver transplant: prospective comparison with the effect of cytomegalovirus. J Med Virol 1999; 59: 496-501
54. Humar A, Kumar D, Caliendo AM, Moussa G, Ashi-Sulaiman A, Levy G, Mazzulli T. Clinical impact of human herpesvirus 6 infection after liver transplantation. Transplantation 2002; 73: 599-604
55. Singh N, Carrigan DR, Gayowski T, Marino IR. Human herpesvirus-6 infection in liver transplant recipients: documentation of pathogenicity. Transplantation 1997; 64: 674-678
56. Montejo M, Ramon Fernandez J, Testillano M, Valdivieso A, Aguirrebengoa K, Varas C, Olaizola A, De Urbina JO. Encephalitis caused by human herpesvirus-6 in a liver transplant recipient. Eur Neurol 2002; 48: 234-235
57. Cervera C, Marcos MA, Linares L, Roig E, Benito N, Pumarola T, Moreno A. A prospective survey of human herpesvirus-6 primary infection in solid organ transplant recipients. Transplantation 2006; 82: 979-982
58. Humar A, Kumar D, Raboud J, Caliendo AM, Moussa G, Levy G, Mazzulli T. Interactions between cytomegalovirus, human herpesvirus-6, and the recurrence of hepatitis C after liver transplantation. Am J Transplant 2002; 2: 461-466
59. Dockrell DH, Mendez JC, Jones M, Harmsen WS, Ilstrup DM, Smith TF, Wiesner RH, Krom RA, Paya CV. Human herpesvirus 6 seronegativity before transplantation predicts the occurrence of fungal infection in liver transplant recipients. Transplantation 1999; 67: 399-403
60. Härmä M, Höckerstedt K, Lyytikäinen O, Lautenschlager I. HHV-6 and HHV-7 antigenemia related to CMV infection after liver transplantation. J Med Virol 2006; 78: 800-805
61. Singh N, Husain S, Carrigan DR, Knox KK, Weck KE, Wagener MM, Gayowski T. Impact of human herpesvirus-6 on the frequency and severity of recurrent hepatitis C virus hepatitis in liver transplant recipients. Clin Transplant 2002; 16: 92-96
62. Rogers J, Rohal S, Carrigan DR, Kusne S, Knox KK, Gayowski T, Wagener MM, Fung JJ, Singh N. Human herpesvirus-6 in liver transplant recipients: role in pathogenesis of fungal infections, neurologic complications, and outcome. Transplantation 2000; 69: 2566-2573
63. Chang FY, Singh N, Gayowski T, Wagener MM, Marino IR. Fever in liver transplant recipients: changing spectrum of etiologic agents. Clin Infect Dis 1998; 26: 59-65
64. Razonable RR, Rivero A, Brown RA, Hart GD, Espy MJ, van Cruijsen H, Wilson J, Groettum C, Kremers W, Smith TF, Paya CV. Detection of simultaneous beta-herpesvirus infections in clinical syndromes due to defined cytomegalovirus infection. Clin Transplant 2003; 17: 114-120
65. Ohashi M, Sugata K, Ihira M, Asano Y, Egawa H, Takada Y, Uemoto S, Yoshikawa T. Human herpesvirus 6 infection in adult living related liver transplant recipients. Liver Transpl 2008; 14: 100-109
66. Lautenschlager I, Linnavuori K, Höckerstedt K. Human herpesvirus-6 antigenemia after liver transplantation. Transplantation 2000; 69: 2561-2566
67. Lautenschlager I, Linnavuori K, Lappalainen M, Suni J, Höckerstedt K. HHV-6 reactivation is often associated with CMV infection in liver transplant patients. Transpl Int 2000; 13 Suppl 1: S351-S353
68. Humar A, Asberg A, Kumar D, Hartmann A, Moussa G, Jardine A, Rollag H, Mouas H, Gahlemann CG, Pescovitz MD. An assessment of herpesvirus co-infections in patients with CMV disease: correlation with clinical and virologic outcomes. Am J Transplant 2009; 9: 374-381
69. Lamoth F, Jayet PY, Aubert JD, Rotman S, Mottet C, Sahli R, Lautenschlager I, Pascual M, Meylan P. Case report: human herpesvirus 6 reactivation associated with colitis in a lung transplant recipient. J Med Virol 2008; 80: 1804-1807
70. Halme L, Arola J, Höckerstedt K, Lautenschlager I. Human herpesvirus 6 infection of the gastroduodenal mucosa. Clin Infect Dis 2008; 46: 434-439
71. Singh N, Paterson DL. Encephalitis caused by human herpesvirus-6 in transplant recipients: relevance of a novel neurotropic virus. Transplantation 2000; 69: 2474-2479
72. Razonable RR, Burak KW, van Cruijsen H, Brown RA, Charlton MR, Smith TF, Espy MJ, Kremers W, Wilson JA, Groettum C, Wiesner R, Paya CV. The pathogenesis of hepatitis C virus is influenced by cytomegalovirus. Clin Infect Dis 2002; 35: 974-981
73. Lautenschlager I, Härmä M, Höckerstedt K, Linnavuori K, Loginov R, Taskinen E. Human herpesvirus-6 infection is associated with adhesion molecule induction and lymphocyte infiltration in liver allografts. J Hepatol 2002; 37: 648-654
74. Jacobs F, Knoop C, Brancart F, Gilot P, Mélot C, Byl B, Delforge ML, Estenne M, Liesnard C. Human herpesvirus-6 infection after lung and heart-lung transplantation: a prospective longitudinal study. Transplantation 2003; 75: 1996-2001
75. Zerr DM, Corey L, Kim HW, Huang ML, Nguy L, Boeckh M. Clinical outcomes of human herpesvirus 6 reactivation after hematopoietic stem cell transplantation. Clin Infect Dis 2005; 40: 932-940
76. Abdel Massih RC, Razonable RR. Human herpesvirus 6 infections after liver transplantation. World J Gastroenterol 2009; 15: 2561-2569
77. Gautheret-Dejean A, Manichanh C, Thien-Ah-Koon F, Fillet AM, Mangeney N, Vidaud M, Dhedin N, Vernant JP, Agut H. Development of a real-time polymerase chain reaction assay for the diagnosis of human herpesvirus-6 infection and application to bone marrow transplant patients. J Virol Methods 2002; 100: 27-35
78. Alvarez-Lafuente R, De las Heras V, Bartolomé M, Picazo JJ, Arroyo R. Relapsing-remitting multiple sclerosis and human herpesvirus 6 active infection. Arch Neurol 2004; 61: 1523-1527
79. Zhen Z, Bradel-Tretheway B, Sumagin S, Bidlack JM, Dewhurst S. The human herpesvirus 6 G protein-coupled receptor homolog U51 positively regulates virus replication and enhances cell-cell fusion in vitro. J Virol 2005; 79: 11914-11924
80. Secchiero P, Carrigan DR, Asano Y, Benedetti L, Crowley RW, Komaroff AL, Gallo RC, Lusso P. Detection of human herpesvirus 6 in plasma of children with primary infection and immunosuppressed patients by polymerase chain reaction. J Infect Dis 1995; 171: 273-280
81. Clark DA, Ait-Khaled M, Wheeler AC, Kidd IM, McLaughlin JE, Johnson MA, Griffiths PD, Emery VC. Quantification of human herpesvirus 6 in immunocompetent persons and post-mortem tissues from AIDS patients by PCR. J Gen Virol 1996; 77 ( Pt 9): 2271-2275
82. Clark DA, Nacheva EP, Leong HN, Brazma D, Li YT, Tsao EH, Buyck HC, Atkinson CE, Lawson HM, Potter MN, Griffiths PD. Transmission of integrated human herpesvirus 6 through stem cell transplantation: implications for laboratory diagnosis. J Infect Dis 2006; 193: 912-916
83. Pradeau K, Bordessoule D, Szelag JC, Rolle F, Ferrat P, Le Meur Y, Turlure P, Denis F, Ranger-Rogez S. A reverse transcription-nested PCR assay for HHV-6 mRNA early transcript detection after transplantation. J Virol Methods 2006; 134: 41-47
84. De Bolle L, Naesens L, De Clercq E. Update on human herpesvirus 6 biology, clinical features, and therapy. Clin Microbiol Rev 2005; 18: 217-245
85. Yoshida M, Yamada M, Tsukazaki T, Chatterjee S, Lakeman FD, Nii S, Whitley RJ. Comparison of antiviral compounds against human herpesvirus 6 and 7. Antiviral Res 1998; 40: 73-84
86. De Clercq E, Naesens L, De Bolle L, Schols D, Zhang Y, Neyts J. Antiviral agents active against human herpesviruses HHV-6, HHV-7 and HHV-8. Rev Med Virol 2001; 11: 381-395
87. De Bolle L, Michel D, Mertens T, Manichanh C, Agut H, De Clercq E, Naesens L. Role of the human herpesvirus 6 u69-encoded kinase in the phosphorylation of ganciclovir. Mol Pharmacol 2002; 62: 714-721
88. Dewhurst S. Human herpesvirus type 6 and human herpesvirus type 7 infections of the central nervous system. Herpes 2004; 11 Suppl 2: 105A-111A
89. Fotheringham J, Akhyani N, Vortmeyer A, Donati D, Williams E, Oh U, Bishop M, Barrett J, Gea-Banacloche J, Jacobson S. Detection of active human herpesvirus-6 infection in the brain: correlation with polymerase chain reaction detection in cerebrospinal fluid. J Infect Dis 2007; 195: 450-454
90. Rapaport D, Engelhard D, Tagger G, Or R, Frenkel N. Antiviral prophylaxis may prevent human herpesvirus-6 reactivation in bone marrow transplant recipients. Transpl Infect Dis 2002; 4: 10-16
91. Tokimasa S, Hara J, Osugi Y, Ohta H, Matsuda Y, Fujisaki H, Sawada A, Kim JY, Sashihara J, Amou K, Miyagawa H, Tanaka-Taya K, Yamanishi K, Okada S. Ganciclovir is effective for prophylaxis and treatment of human herpesvirus-6 in allogeneic stem cell transplantation. Bone Marrow Transplant 2002; 29: 595-598
92. Lautenschlager I, Lappalainen M, Linnavuori K, Suni J, Höckerstedt K. CMV infection is usually associated with concurrent HHV-6 and HHV-7 antigenemia in liver transplant patients. J Clin Virol 2002; 25 Suppl 2: S57-S61