Sepsis and cytomegalovirus: foes or conspirators?

Medical Microbiology and Immunology

Volumn 204, Issue 3, 2015, Pages 431-437

  Mansfield, Sara ^a   Grießl, Marion ^b   Gutknecht, Michael ^b   Cook, Charles H ^b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cytomegalovirus; Reactivation; Sepsis

Indexed keywords

ACICLOVIR; GANCICLOVIR; PLACEBO; ANTIVIRUS AGENT;

BACTERIAL INFECTION; CRITICALLY ILL PATIENT; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DRUG MEGADOSE; EPIGENETICS; HUMAN; IMMUNE RESPONSE; INCIDENCE; INFLAMMATION; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPSIS; VIRUS LOAD; VIRUS REACTIVATION; ANIMAL; CYTOMEGALOVIRUS INFECTIONS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MOUSE; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

ANIMALS; ANTIVIRAL AGENTS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; SEPSIS; VIRUS ACTIVATION;

EID: 84929958655     PISSN: 03008584     EISSN: 14321831     Source Type: Journal    
DOI: 10.1007/s00430-015-0407-0     Document Type: Review

References (60)

1. Smith MG (1954) Propagation of salivary gland virus of the mouse in tissue cultures. Proc Soc Exp Biol Med 86(3):435–440
2. Smith MG (1956) Propagation in tissue cultures of a cytopathogenic virus from human salivary gland virus (SGV) disease. Proc Soc Exp Biol Med 92(2):424–430
3. Guidry CA, Mansfield SA, Sawyer RG, Cook CH (2014) Resistant pathogens, fungi, and viruses. Surg Clin North Am 94(6):1195–1218. doi:10.1016/j.suc.2014.08.010
4. Cook CH, Trgovcich J (2011) Cytomegalovirus reactivation in critically ill immunocompetent hosts: a decade of progress and remaining challenges. Antivir Res 90(3):151–159. doi:10.1016/j.antiviral.2011.03.179
5. Bordes J, Maslin J, Prunet B, d’Aranda E, Lacroix G, Goutorbe P, Dantzer E, Meaudre E (2011) Cytomegalovirus infection in severe burn patients monitoring by real-time polymerase chain reaction: a prospective study. Burns 37(3):434–439. doi:10.1016/j.burns.2010.11.006
6. Heininger A, Haeberle H, Fischer I, Beck R, Riessen R, Rohde F, Meisner C, Jahn G, Koenigsrainer A, Unertl K, Hamprecht K (2011) Cytomegalovirus reactivation and associated outcome of critically ill patients with severe sepsis. Crit Care 15(2):R77. doi:10.1186/cc10069
7. Heininger A, Jahn G, Engel C, Notheisen T, Unertl K, Hamprecht K (2001) Human cytomegalovirus infections in nonimmunosuppressed critically ill patients. Crit Care Med 29(3):541–547
8. Chilet M, Aguilar G, Benet I, Belda J, Tormo N, Carbonell JA, Clari MA, Costa E, Navarro D (2010) Virological and immunological features of active cytomegalovirus infection in nonimmunosuppressed patients in a surgical and trauma intensive care unit. J Med Virol 82(8):1384–1391. doi:10.1002/jmv.21825
9. Ziemann M, Sedemund-Adib B, Reiland P, Schmucker P, Hennig H (2008) Increased mortality in long-term intensive care patients with active cytomegalovirus infection. Crit Care Med 36(12):3145–3150
10. Limaye AP, Kirby KA, Rubenfeld GD, Leisenring WM, Bulger EM, Neff MJ, Gibran NS, Huang M-L, Santo Hayes TK, Corey L, Boeckh M (2008) Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 300(4):413–422. doi:10.1001/jama.300.4.413
11. von Muller L, Klemm A, Weiss M, Schneider M, Suger-Wiedeck H, Durmus N, Hampl W, Mertens T (2006) Active cytomegalovirus infection in patients with septic shock. Emerg Infect Dis 12(10):1517–1522
12. Kutza AS, Muhl E, Hackstein H, Kirchner H, Bein G (1998) High incidence of active cytomegalovirus infection among septic patients. Clin Infect Dis 26(5):1076–1082
13. Papazian L, Fraisse A, Garbe L, Zandotti C, Thomas P, Saux P, Pierrin G, Gouin F (1996) Cytomegalovirus. An unexpected cause of ventilator-associated pneumonia. Anesthesiology 84(2):280–287
14. Domart Y, Trouillet JL, Fagon JY, Chastre J, Brun-Vezinet F, Gibert C (1990) Incidence and morbidity of cytomegaloviral infection in patients with mediastinitis following cardiac surgery [see comments]. Chest 97(1):18–22
15. Walton AH, Muenzer JT, Rasche D, Boomer JS, Sato B, Brownstein BH, Pachot A, Brooks TL, Deych E, Shannon WD, Green JM, Storch GA, Hotchkiss RS (2014) Reactivation of multiple viruses in patients with sepsis. PLoS ONE 9(6):e98819. doi:10.1371/journal.pone.0098819
16. Coisel Y, Bousbia S, Forel J-M, Hraiech S, Lascola B, Roch A, Zandotti C, Million M, Jaber S, Raoult D, Papazian L (2012) Cytomegalovirus and herpes simplex virus effect on the prognosis of mechanically ventilated patients suspected to have ventilator-associated pneumonia. PLoS ONE 7(12):e51340. doi:10.1371/journal.pone.0051340
17. Smith CA, Conroy LT, Pollock M, Ruddy J, Binning A, McCruden EA (2010) Detection of herpes viruses in respiratory secretions of patients undergoing artificial ventilation. J Med Virol 82(8):1406–1409. doi:10.1002/jmv.21794
18. Jaber S, Chanques G, Borry J, Souche B, Verdier R, Perrigault P-F, Eledjam J-J (2005) Cytomegalovirus infection in critically ill patients: associated factors and consequences. Chest 127(1):233–241
19. Friedrichs I, Bingold T, Keppler OT, Pullmann B, Reinheimer C, Berger A (2013) Detection of herpesvirus EBV DNA in the lower respiratory tract of ICU patients: a marker of infection of the lower respiratory tract? Med Microbiol Immunol 202(6):431–436. doi:10.1007/s00430-013-0306-1
20. Chiche L, Forel JM, Roch A, Guervilly C, Pauly V, Allardet-Servent J, Gainnier M, Zandotti C, Papazian L (2009) Active cytomegalovirus infection is common in mechanically ventilated medical intensive care unit patients. Crit Care Med 37(6):1850–1857
21. Cook CH, Martin LC, Yenchar JK, Lahm MC, McGuinness B, Davies EA, Ferguson RM (2003) Occult herpes family viral infections are endemic in critically ill surgical patients. Crit Care Med 31(7):1923–1929
22. Cook CH, Yenchar JK, Kraner TO, Davies EA, Ferguson RM (1998) Occult herpes family viruses may increase mortality in critically ill surgical patients. Am J Surg 176(4):357–360
23. Desachy A, Ranger-Rogez S, Francois B, Venot C, Traccard I, Gastinne H, Denis F, Vignon P (2001) Reactivation of human herpesvirus type 6 in multiple organ failure syndrome. Clin Infect Dis 32(2):197–203
24. Razonable RR, Fanning C, Brown RA, Espy MJ, Rivero A, Wilson J, Kremers W, Smith TF, Paya CV (2002) Selective reactivation of human herpesvirus 6 variant a occurs in critically ill immunocompetent hosts.[see comment]. J Infect Dis 185(1):110–113
25. Stephan F, Meharzi D, Ricci S, Fajac A, Clergue F, Bernaudin JF (1996) Evaluation by polymerase chain reaction of cytomegalovirus reactivation in intensive care patients under mechanical ventilation. Intensiv Care Med 22(11):1244–1249
26. Vogel T, Vadonis R, Kuehn J, Eing BR, Senninger N, Haier J (2008) Viral reactivation is not related to septic complications after major surgical resections. APMIS 116(4):292–301
27. Ishioka H, Sanui M, Tsutsumi Y, Yanase F, Shiotsuka J (2014) Low prevalence of active cytomegalovirus infection in a cardiovascular intensive care unit. J Intensiv Care 2(1):12. doi:10.1186/2052-0492-2-12
28. Docke WD, Prosch S, Fietze E, Kimel V, Zuckermann H, Klug C, Syrbe U, Kruger DH, von Baehr R, Volk HD (1994) Cytomegalovirus reactivation and tumour necrosis factor. Lancet 343(8892):268–269
29. Stein J, Volk HD, Liebenthal C, Kruger DH, Prosch S (1993) Tumour necrosis factor alpha stimulates the activity of the human cytomegalovirus major immediate early enhancer/promoter in immature monocytic cells. J Gen Virol 74(11):2333–2338
30. Prosch S, Staak K, Stein J, Liebenthal C, Stamminger T, Volk HD, Kruger DH (1995) Stimulation of the human cytomegalovirus IE enhancer/promoter in HL-60 Cells by TNF alpha is mediated via induction of NF-kappaB. Virology 208(1):197–206
31. Cook C, Zhang X, McGuinness B, Lahm M, Sedmak D, Ferguson R (2002) Intra-abdominal bacterial infection reactivates latent pulmonary cytomegalovirus in immunocompetent mice. J Infect Dis 185:1395–1400
32. Cook CH, Trgovcich J, Zimmerman PD, Zhang Y, Sedmak DD (2006) Lipopolysaccharide, tumor necrosis factor alpha, or interleukin-1{beta} triggers reactivation of latent cytomegalovirus in immunocompetent mice. J Virol 80(18):9151–9158
33. Seckert CK, Griessl M, Buttner JK, Freitag K, Lemmermann N, Hummel M, Liu XF, Abecassis M, Angulo A, Messerle M, Cook CH, Reddehase M (2013) Immune Surveillance of Cytomegalovirus Latency and Reactivation in Murine Models: Link to Memory Inflation. In: Reddehase MJ (ed) Cytomegaloviruses, vol 1., Caister Academic PressNorfolk, UK, pp 374–416
34. Cook CH, Zhang Y, Sedmak DD, Martin LC, Jewell S, Ferguson RM (2006) Pulmonary cytomegalovirus reactivation causes pathology in immunocompetent mice. Crit Care Med 34(3):842–849
35. Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, Diamond MS, Miller VL, Virgin HW (2007) Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447(7142):326–329
36. Smith PD, Shimamura M, Musgrove LC, Dennis EA, Bimczok D, Novak L, Ballestas M, Fenton A, Dandekar S, Britt WJ, Smythies LE (2014) Cytomegalovirus enhances macrophage TLR expression and MyD88-mediated signal transduction to potentiate inducible inflammatory responses. J Immunol 193:5604–5612. doi:10.4049/jimmunol.1302608
37. Tanaka K, Sawamura S, Satoh T, Kobayashi K, Noda S (2007) Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J Immunol 178(8):5209–5216
38. Seckert CK, Griessl M, Buttner JK, Scheller S, Simon CO, Kropp KA, Renzaho A, Kuhnapfel B, Grzimek NK, Reddehase MJ (2012) Viral latency drives ‘memory inflation’: a unifying hypothesis linking two hallmarks of cytomegalovirus infection. Med Microbiol Immunol. doi:10.1007/s00430-012-0273-y
39. Kurz SK, Reddehase MJ (1999) Patchwork pattern of transcriptional reactivation in the lungs indicates sequential checkpoints in the transition from murine cytomegalovirus latency to recurrence. J Virol 73(10):8612–8622
40. De Vlieger G, Meersseman W, Lagrou K, Wouters P, Wilmer A, Peetermans W, Van den Berghe G, Van Wijngaerden E (2012) Cytomegalovirus serostatus and outcome in nonimmunocompromised critically ill patients. Crit Care Med 40(1):36–42
41. Simanek AM, Dowd JB, Pawelec G, Melzer D, Dutta A, Aiello AE (2011) Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS ONE 6(2):e16103. doi:10.1371/journal.pone.0016103
42. Strandberg TE, Pitkala KH, Tilvis RS (2009) Cytomegalovirus antibody level and mortality among community-dwelling older adults with stable cardiovascular disease. JAMA 301(4):380–382
43. Wang GC, Kao WHL, Murakami P, Xue Q-L, Chiou RB, Detrick B, McDyer JF, Semba RD, Casolaro V, Walston JD, Fried LP (2010) Cytomegalovirus infection and the risk of mortality and frailty in older women: a prospective observational cohort study. Am J Epidemiol 171(10):1144–1152. doi:10.1093/aje/kwq062
44. Miggins M, Hasan A, Hohmann S, Southwick F, Casella G, Schain D, Liu H, Bihorac A, Moldawer L, Efron P, Ang D (2011) The potential influence of common viral infections diagnosed during hospitalization among critically ill patients in the United States. PLoS ONE 6(4):e18890
45. + T cells dominate the memory compartments of exposed subjects. J Exp Med 202(5):673–685. doi:10.1084/jem.20050882
46. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, Finnerty CC, Lopez CM, Honari S, Moore EE, Minei JP, Cuschieri J, Bankey PE, Johnson JL, Sperry J, Nathens AB, Billiar TR, West MA, Jeschke MG, Klein MB, Gamelli RL, Gibran NS, Brownstein BH, Miller-Graziano C, Calvano SE, Mason PH, Cobb JP, Rahme LG, Lowry SF, Maier RV, Moldawer LL, Herndon DN, Davis RW, Xiao W, Tompkins RG (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA. doi:10.1073/pnas.1222878110
47. Welsh RM, Selin LK (2002) No one is naive: the significance of heterologous T-cell immunity. Nat Rev Immunol 2(6):417–426
48. Barton ES, White DW, Virgin HW (2009) Herpesvirus latency and symbiotic protection from bacterial infection. Viral Immunol 22(1):3–4. doi:10.1089/vim.2008.0100
49. Kalil AC, Florescu DF (2009) Prevalence and mortality associated with cytomegalovirus infections in non-immunosuppressed ICU patients. Crit Care Med 37(8):2350–2358
50. Wohl DA, Zeng D, Stewart P, Glomb N, Alcorn T, Jones S, Handy J, Fiscus S, Weinberg A, Gowda D, van der Horst C (2005) Cytomegalovirus viremia, mortality, and end-organ disease among patients with AIDS receiving potent antiretroviral therapies. JAIDS J Acquir Immune Defic Syndr 38(5):538–544
51. Hotchkiss RS, Coopersmith CM, McDunn JE, Ferguson TA (2009) The sepsis seesaw: tilting toward immunosuppression. Nat Med 15(5):496–497
52. Campbell J, Trgovcich J, Kincaid M, Zimmerman PD, Klenerman P, Sims S, Cook CH (2012) Transient CD8-memory contraction: a potential contributor to latent cytomegalovirus reactivation. J Leukoc Biol 92(5):933–937. doi:10.1189/jlb.1211635
53. von Muller L, Mertens T (2008) Human cytomegalovirus infection and antiviral immunity in septic patients without canonical immunosuppression. Med Microbiol Immunol 197(2):75–82
54. Seckert CK, Renzaho A, Tervo H-M, Krause C, Deegen P, Kuhnapfel B, Reddehase MJ, Grzimek NKA (2009) Liver sinusoidal endothelial cells are a site of murine cytomegalovirus latency and reactivation. J Virol 83(17):8869–8884. doi:10.1128/jvi.00870-09
55. Balthesen M, Messerle M, Reddehase MJ (1993) Lungs are a major organ site of cytomegalovirus latency and recurrence. J Virol 67(9):5360–5366
56. Toorkey CB, Carrigan DR (1989) Immunohistochemical detection of an immediate early antigen of human cytomegalovirus in normal tissues. J Infect Dis 160(5):741–751
57. Cook CH (2007) Cytomegalovirus reactivation in “immunocompetent” patients: a call for scientific prophylaxis. J Infect Dis 196(9):1273–1275
58. Kalil AC, Levitsky J, Lyden E, Stoner J, Freifeld AG (2005) Meta-analysis: the efficacy of strategies to prevent organ disease by cytomegalovirus in solid organ transplant recipients. Ann Intern Med 143(12):870–880
59. Forster MR, Trgovcich J, Zimmerman P, Chang A, Miller C, Klenerman P, Cook CH (2010) Antiviral prevention of sepsis induced cytomegalovirus reactivation in immunocompetent mice. Antivir Res 85(3):496–503. doi:10.1016/j.antiviral.2009.12.004
60. Traen S, Bochanen N, Ieven M, Schepens T, Bruynseels P, Verbrugghe W, Jorens PG (2014) Is acyclovir effective among critically ill patients with herpes simplex in the respiratory tract? J Clin Virol 60(3):215–221. doi:10.1016/j.jcv.2014.04.010