The Perioperative Lung Transplant Virome: Torque Teno Viruses Are Elevated in Donor Lungs and Show Divergent Dynamics in Primary Graft Dysfunction

American Journal of Transplantation

Volumn 17, Issue 5, 2017, Pages 1313-1324

  Abbas, A A ^a   Diamond, J M ^a   Chehoud, C ^a   Chang, B ^a   Kotzin, J J ^a   Young, J C ^a   Imai, I ^a   Haas, A R ^a   Cantu, E ^a   Lederer, D J ^b   Meyer, K C ^c   Milewski, R K ^a   Olthoff, K M ^a   Shaked, A ^a   Christie, J D ^a   Bushman, F D ^a   Collman, R G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

immunosuppression immune modulation; lung (allograft) function dysfunction; lung failure injury; lung transplantation pulmonology; microbiomics; molecular biology; translational research science

Indexed keywords

VIRUS DNA;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; BRAIN DEATH; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE SEQUENCE; GRAFT RECIPIENT; HOST CELL; HUMAN; IMMUNOREACTIVITY; LUNG LAVAGE; LUNG PERFUSION; LUNG TRANSPLANTATION; MALE; METAGENOMICS; MIDDLE AGED; ORGAN DONOR; PERIOPERATIVE PERIOD; POLYMERASE CHAIN REACTION; PRIMARY GRAFT DYSFUNCTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TISSUE INJURY; TORQUE TENO VIRUS 1; VIRUS REPLICATION; CASE CONTROL STUDY; CLINICAL TRIAL; DONOR; FOLLOW UP; GENETICS; GRAFT REJECTION; GRAFT SURVIVAL; MULTICENTER STUDY; PATHOLOGY; PROGNOSIS; PROSPECTIVE STUDY; RESPIRATORY SYSTEM; RISK FACTOR; VIROLOGY; VIRUS GENOME;

ADULT; AGED; CASE-CONTROL STUDIES; DNA, VIRAL; FEMALE; FOLLOW-UP STUDIES; GENOME, VIRAL; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; LUNG TRANSPLANTATION; MALE; METAGENOMICS; MIDDLE AGED; PERIOPERATIVE CARE; PRIMARY GRAFT DYSFUNCTION; PROGNOSIS; PROSPECTIVE STUDIES; RESPIRATORY SYSTEM; RISK FACTORS; TISSUE DONORS; TORQUE TENO VIRUS;

EID: 84995921776     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.14076     Document Type: Article

References (74)

1. Yusen RD, Edwards LB, Kucheryavaya AY, et al. The Registry of the International Society for Heart and Lung Transplantation: Thirty-Second Official Adult Lung and Heart-Lung Transplantation Report—2015; Focus Theme: Early Graft Failure. J Heart Lung Transplant 2015; 34: 1264–1277.
2. Watson CJE, Dark JH. Organ transplantation: Historical perspective and current practice. Br J Anaesth 2012; 108(Suppl 1): i29–i42.
3. Lee JC, Christie JD. Primary graft dysfunction. Clin Chest Med 2011; 32: 279–293.
4. Ius F, Sommer W, Tudorache I, et al. Early donor-specific antibodies in lung transplantation: Risk factors and impact on survival. J Heart Lung Transplant 2014; 33: 1255–1263.
5. Daud SA, Yusen RD, Meyers BF, et al. Impact of immediate primary lung allograft dysfunction on bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2007; 175: 507–513.
6. Eppinger MJ, Deeb GM, Bolling SF, Ward PA. Mediators of ischemia-reperfusion injury of rat lung. Am J Pathol 1997; 150: 1773–1784.
7. Eppinger MJ, Jones ML, Deeb GM, Bolling SF, Ward PA. Pattern of injury and the role of neutrophils in reperfusion injury of rat lung. J Surg Res 1995; 58: 713–718.
8. Fiser SM, Tribble CG, Long SM, Kaza AK. Pulmonary macrophages are involved in reperfusion injury after lung transplantation. Ann Thorac Surg 2001; 71: 1134–1138.
9. Naidu BV, Krishnadasan B, Farivar AS, et al. Early activation of the alveolar macrophage is critical to the development of lung ischemia-reperfusion injury. J Thoracic Cardiovasc Surg 2003; 126: 200–207.
10. Yang Z, Sharma AK, Linden J, Kron IL, Laubach VE. CD4 + T lymphocytes mediate acute pulmonary ischemia–reperfusion injury. J Thoracic Cardiovasc Surg 2009; 137: 695–702.
11. Sharma AK, LaPar DJ, Zhao Y, et al. Natural killer T cell–derived IL-17 mediates lung ischemia-reperfusion injury. Am J Respir Crit Care Med 2011; 183: 1539–1549.
12. Johnston LK, Rims CR, Gill SE, McGuire JK, Manicone AM. Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol 2012; 47: 417–426.
13. Diamond JM, Wigfield CH. Role of innate immunity in primary graft dysfunction after lung transplantation. Curr Opin Organ Transplant 2013; 18: 518–523.
14. Cantu E, Shah RJ, Lin W, et al. Oxidant stress regulatory genetic variation in recipients and donors contributes to risk of primary graft dysfunction after lung transplantation. J Thoracic Cardiovasc Surg 2015; 149: 596–602.
15. Cantu E, Lederer DJ, Meyer K, et al. Gene set enrichment analysis identifies key innate immune pathways in primary graft dysfunction after lung transplantation. Am J Transplant 2013; 13: 1898–1904.
16. Naka Y, Marsh HC, Scesney SM, Oz MC, Pinsky DJ. Complement activation as a cause for primary graft failure in an isogeneic rat model of hypothermic lung preservation and transplantation. Transplantation 1997; 64: 1248–1255.
17. Shah RJ, Emtiazjoo AM, Diamond JM, et al. Plasma complement levels are associated with primary graft dysfunction and mortality after lung transplantation. Am J Respir Crit Care Med 2014; 189: 1564–1567.
18. Khalifah AP, Hachem RR, Chakinala MM, et al. Respiratory viral infections are a distinct risk for bronchiolitis obliterans syndrome and death. Am J Respir Crit Care Med 2004; 170: 181–187.
19. Botha P, Archer L, Anderson RL, et al. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation 2008; 85: 771–774.
20. Weigt SS, Elashoff RM, Huang C, et al. Aspergillus colonization of the lung allograft is a risk factor for bronchiolitis obliterans syndrome. Am J Transplant 2009; 9: 1903–1911.
21. Gottlieb J, Schulz TF, Welte T, et al. Community-acquired respiratory viral infections in lung transplant recipients: A single season cohort study. Transplantation 2009; 87: 1530–1537.
22. Borewicz K, Pragman AA, Kim HB, Hertz M, Wendt C, Isaacson RE. Longitudinal analysis of the lung microbiome in lung transplantation. FEMS Microbiol Lett 2013; 339: 57–65.
23. Nakajima T, Palchevsky V, Perkins DL, Belperio JA, Finn PW. Lung transplantation: Infection, inflammation, and the microbiome. Semin Immunopathol 2011; 33: 135–156.
24. Verleden SE, Ruttens D, Vandermeulen E, et al. Restrictive chronic lung allograft dysfunction: Where are we now? The Journal of heart and lung transplantation 2015; 34: 625–630.
25. Charlson ES, Diamond JM, Bittinger K, et al. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med 2012; 186: 536–545.
26. Young JC, Chehoud C, Bittinger K, et al. Viral metagenomics reveal blooms of anelloviruses in the respiratory tract of lung transplant recipients. Am J Transplant 2015; 15: 200–209.
27. Sharma P, Diene SM, Thibeaut S, et al. Phenotypic and genotypic properties of Microbacterium yannicii, a recently described multidrug resistant bacterium isolated from a lung transplanted patient with cystic fibrosis in France. BMC Microbiol 2013; 13: 97.
28. Dickson RP, Erb-Downward JR, Freeman CM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct Pseudomonas species with distinct clinical associations. PLoS ONE 2014; 9: e97214.
29. Willner DL, Hugenholtz P, Yerkovich ST, et al. Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2013; 187: 640–647.
30. Spandole S, Cimponeriu D, Berca LM, Mihăescu G. Human anelloviruses: An update of molecular, epidemiological and clinical aspects. Arch Virol 2015; 160: 893–908.
31. Ninomiya M, Takahashi M, Nishizawa T, Shimosegawa T, Okamoto H. Development of PCR assays with nested primers specific for differential detection of three human anelloviruses and early acquisition of dual or triple infection during infancy. J Clin Microbiol 2008; 46: 507–514.
32. McElvania TeKippe E, Wylie KM, Deych E, Sodergren E, Weinstock G, Storch GA. Increased prevalence of anellovirus in pediatric patients with fever. PLoS ONE 2012; 7: e50937.
33. Chen T, Väisänen E, Mattila PS, Hedman K, Söderlund-Venermo M. Antigenic diversity and seroprevalences of Torque teno viruses in children and adults by ORF2-based immunoassays. J Gen Virol 2013; 94(Pt 2): 409–417.
34. Thom K, Petrik J. Progression towards AIDS leads to increased torque teno virus and torque teno minivirus titers in tissues of HIV infected individuals. J Med Virol 2007; 79: 1–7.
35. Madsen CD, Eugen-Olsen J, Kirk O, et al. TTV viral load as a marker for immune reconstitution after initiation of HAART in HIV-infected patients. HIV Clin Trials 2002; 3: 287–295.
36. Devalle S, Rua F, Morgado MG, Niel C. Variations in the frequencies of torque teno virus subpopulations during HAART treatment in HIV-1-coinfected patients. Arch Virol 2009; 154: 1285–1291.
37. De Vlaminck I, Khush KK, Strehl C, et al. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell 2013; 155: 1178–1187.
38. Görzer I, Haloschan M, Jaksch P, Klepetko W, Puchhammer-Stöckl E. Plasma DNA levels of Torque teno virus and immunosuppression after lung transplantation. J Heart Lung Transplant 2014; 33: 320–323.
39. Görzer I, Jaksch P, Kundi M, Seitz T, Klepetko W, Puchhammer-Stöckl E. Pre-transplant plasma Torque Teno virus load and increase dynamics after lung transplantation. PLoS ONE 2015; 10: e0122975.
40. Hino S, Miyata H. Torque teno virus (TTV): Current status. Rev Med Virol 2007; 17: 45–57.
41. Charlson ES, Bittinger K, Haas AR, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011; 184: 957–963.
42. Beck JM, Schloss PD, Venkataraman A, et al. Multicenter comparison of lung and oral microbiomes of HIV-infected and HIV-uninfected individuals. Am J Respir Crit Care Med 2015; 192: 1335–1344.
43. Wang D, Urisman A, Liu Y-T, et al. Viral discovery and sequence recovery using DNA microarrays. PLoS Biol 2003; 1: E2.
44. Ihaka R, Gentleman R. R: A language for data analysis and graphics. J Comput Graph Stat 1996; 5: 299–314.
45. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995; 57: 289–300.
46. Dollive S, Peterfreund GL, Sherrill-Mix S, et al. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol 2012; 13: 1–13.
47. Salter SJ, Cox MJ, Turek EM, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014; 12: 1–12.
48. Kotloff RM, Thabut G. Lung transplantation. Am J Respir Crit Care Med 2011; 184: 159–171.
49. Smits SL, Schapendonk CM, van Beek J, et al. New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg Infect Dis 2014; 20: 1218–1222.
50. Phan TG, da Costa AC, Zhang W, et al. A new gyrovirus in human feces. Virus Genes 2015; 51: 132–135.
51. Phan TG, Mori D, Deng X, et al. Small circular single stranded DNA viral genomes in unexplained cases of human encephalitis, diarrhea, and in untreated sewage. Virology 2015; 482: 98–104.
52. Phan TG, Luchsinger V, Avendano LF, Deng X, Delwart E. Cyclovirus in nasopharyngeal aspirates of Chilean children with respiratory infections. J Gen Virol 2014; 95(Pt_4): 922–927.
53. Saadi H, Pagnier I, Colson P, et al. First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis 2013; 57: 34.
54. Kutikhin AG, Yuzhalin AE, Brusina EB. Mimiviridae, marseilleviridae, and virophages as emerging human pathogens causing healthcare-associated infections. GMS Hyg Infect Control 2014; 9: Doc16.
55. Kutsogiannis DJ, Pagliarello G, Doig C, Ross H, Shemie SD. Medical management to optimize donor organ potential: Review of the literature. Can J Anaesth 2006; 53: 820–830.
56. Faropoulos K, Apostolakis E. Brain death and its influence on the lungs of the donor: How is it prevented? Transpl Proc 2009; 41: 4114–4119.
57. Maggi F, Fornai C, Zaccaro L, et al. TT virus (TTV) loads associated with different peripheral blood cell types and evidence for TTV replication in activated mononuclear cells. J Med Virol 2001; 64: 190–194.
58. Mariscal LF, López-Alcorocho JM, Rodríguez-Iñigo E, et al. TT virus replicates in stimulated but not in nonstimulated peripheral blood mononuclear cells. Virology 2002; 301: 121–129.
59. Zhong S, Yeo W, Tang M, et al. Frequent detection of the replicative form of TT virus DNA in peripheral blood mononuclear cells and bone marrow cells in cancer patients. J Med Virol 2002; 66: 428–434.
60. Takahashi M, Asabe S, Gotanda Y, Kishimoto J, Tsuda F, Okamoto H. TT virus is distributed in various leukocyte subpopulations at distinct levels, with the highest viral load in granulocytes. Biochem Biophys Res Commun 2002; 290: 242–248.
61. Focosi D, Macera L, Boggi U, Nelli LC, Maggi F. Short-term kinetics of torque teno virus viraemia after induction immunosuppression confirm T lymphocytes as the main replication-competent cells. J Gen Virol 2015; 96(Pt 1): 115–117.
62. Maggi F, Pifferi M, Fornai C, et al. TT virus in the nasal secretions of children with acute respiratory diseases: Relations to viremia and disease severity. J Virol 2003; 77: 2418–2425.
63. Walton AH, Muenzer JT, Rasche D, et al. Reactivation of multiple viruses in patients with sepsis. PLoS ONE 2014; 9: e98819.
64. Focosi D, Maggi F, Albani M, et al. Torquetenovirus viremia kinetics after autologous stem cell transplantation are predictable and may serve as a surrogate marker of functional immune reconstitution. J Clin Virol 2010; 47: 189–192.
65. Pifferi M, Maggi F, Di Cristofano C, et al. Torquetenovirus infection and ciliary dysmotility in children with recurrent pneumonia. Pediatr Infect Dis J 2008; 27: 413–418.
66. Okamoto H, Nishizawa T, Takahashi M, Asabe S, Tsuda F, Yoshikawa A. Heterogeneous distribution of TT virus of distinct genotypes in multiple tissues from infected humans. Virology 2001; 288: 358–368.
67. Haloschan M, Bettesch R, Görzer I, Weseslindtner L, Kundi M, Puchhammer-Stöckl E. TTV DNA plasma load and its association with age, gender, and HCMV IgG serostatus in healthy adults. Age (Dordr) 2014; 36: 9716.
68. Christensen JK, Eugen-Olsen J, SŁrensen M, et al. Prevalence and prognostic significance of infection with TT virus in patients infected with human immunodeficiency virus. J Infect Dis 2000; 181: 1796–1799.
69. Moen EM, Sagedal S, Bjøro K, Degré M, Opstad PK, Grinde B. Effect of immune modulation on TT virus (TTV) and TTV-like-mini-virus (TLMV) viremia. J Med Virol 2003; 70: 177–182.
70. Mancuso R, Saresella M, Hernis A, et al. Torque teno virus (TTV) in multiple sclerosis patients with different patterns of disease. J Med Virol 2013; 85: 2176–2183.
71. Wylie KM, Mihindukulasuriya KA, Sodergren E, Weinstock GM, Storch GA. Sequence analysis of the human virome in febrile and afebrile children. PLoS ONE 2012; 7: e27735.
72. Holtz LR, Cao S, Zhao G, et al. Geographic variation in the eukaryotic virome of human diarrhea. Virology 2014; 468–470: 556–564.
73. Handley SA, Thackray LB, Zhao G, et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 2012; 151: 253–266.
74. Willner D, Haynes MR, Furlan M, et al. Case studies of the spatial heterogeneity of DNA viruses in the cystic fibrosis lung. Am J Respir Cell Mol Biol 2012; 46: 127–131.