Community Respiratory Virus Infections in Immunocompromised Patients: Hematopoietic Stem Cell and Solid Organ Transplant Recipients, and Individuals with Human Immunodeficiency Virus Infection

Yae-Jean Kim; Michael Boeckh; Janet A. Englund

doi:10.1055/s-2007-976494

Seminars in Respiratory and Critical Care Medicine, Inhaltsverzeichnis

Semin Respir Crit Care Med 2007; 28(2): 222-242
DOI: 10.1055/s-2007-976494

Community Respiratory Virus Infections in Immunocompromised Patients: Hematopoietic Stem Cell and Solid Organ Transplant Recipients, and Individuals with Human Immunodeficiency Virus Infection

Yae-Jean Kim¹ ^, ² , Michael Boeckh¹ , Janet A. Englund¹ ^, ³

¹Division of Infectious Diseases, Fred Hutchinson Cancer Research Center, Seattle, Washington
²Department of Pediatrics, Samsung Medical Center, SungKyunKwan University School of Medicine, Seoul, Korea
³Division of Infectious Diseases, Children’s Hospital and Regional Medical Center, Seattle, Washington

Abstract

ABSTRACT

Infection is the leading cause of morbidity and mortality in immunocompromised patients such as hematopoietic/solid organ transplant recipients and individuals with human immunodeficiency virus. Community respiratory virus infections are increasingly recognized as a significant threat to these patients. This article reviews current information in the clinical field of community respiratory viruses, including several newly discovered respiratory viruses.

Respiratory syncytial virus, influenza viruses, parainfluenza viruses, and adenoviruses cause the most serious disease in immunocompromised hosts, but other respiratory viruses are becoming increasingly appreciated as a cause of both upper and lower respiratory tract disease. The clinical impact of these new viruses, including human metapneumovirus, non-SARS human coronaviruses, and human bocavirus, is not yet clear. Modern molecular technology has made the discovery of new viruses possible; the use of these new technologies in direct patient care is not yet standard but is becoming increasingly utilized. Clinicians should appreciate the potential for the development of antiviral resistance to influenza antivirals in immunocompromised patients.

KEYWORDS

Respiratory virus - immunocompromised - transplant - respiratory syncytial virus - influenza - metapneumovirus - coronavirus - parainfluenza virus - rhinovirus - adenovirus

Volltext

Referenzen

REFERENCES

1 Kuypers J, Wright N, Ferrenberg J et al.. Comparison of real-time PCR assays with fluorescent-antibody assays for diagnosis of respiratory virus infections in children. J Clin Microbiol. 2006; 44 2382-2388
2 Freymuth F, Vabret A, Cuvillon-Nimal D et al.. Comparison of multiplex PCR assays and conventional techniques for the diagnostic of respiratory virus infections in children admitted to hospital with an acute respiratory illness. J Med Virol. 2006; 78 1498-1504
3 Englund J A, Sullivan C J, Jordan M C, Dehner L P, Vercellotti G M, Balfour Jr H H. Respiratory syncytial virus infection in immunocompromised adults. Ann Intern Med. 1988; 109 203-208
4 Crooks B N, Taylor C E, Turner A J et al.. Respiratory viral infections in primary immune deficiencies: significance and relevance to clinical outcome in a single BMT unit. Bone Marrow Transplant. 2000; 26 1097-1102
5 Ljungman P, Ward K N, Crooks B N et al.. Respiratory virus infections after stem cell transplantation: a prospective study from the Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant. 2001; 28 479-484
6 Small T N, Casson A, Malak S F et al.. Respiratory syncytial virus infection following hematopoietic stem cell transplantation. Bone Marrow Transplant. 2002; 29 321-327
7 Chemaly R F, Ghosh S, Bodey G P et al.. Respiratory viral infections in adults with hematologic malignancies and human stem cell transplantation recipients: a retrospective study at a major cancer center. Medicine (Baltimore). 2006; 85 278-287
8 Whimbey E, Champlin R E, Englund J A et al.. Combination therapy with aerosolized ribavirin and intravenous immunoglobulin for respiratory syncytial virus disease in adult bone marrow transplant recipients. Bone Marrow Transplant. 1995; 16 393-399
9 Nichols W G, Gooley T, Boeckh M. Community-acquired respiratory syncytial virus and parainfluenza virus infections after hematopoietic stem cell transplantation: the Fred Hutchinson Cancer Research Center experience. Biol Blood Marrow Transplant. 2001; 7(Suppl) 11S-15S
10 Whimbey E, Bodey G P. Viral pneumonia in the immunocompromised adult with neoplastic disease: the role of common community respiratory viruses. Semin Respir Infect. 1992; 7 122-131
11 Whimbey E, Champlin R E, Couch R B et al.. Community respiratory virus infections among hospitalized adult bone marrow transplant recipients. Clin Infect Dis. 1996; 22 778-782
12 Englund J A. Diagnosis and epidemiology of community-acquired respiratory virus infections in the immunocompromised host. Biol Blood Marrow Transplant. 2001; 7(Suppl) 2S-4S
13 Erard V, Chien J W, Kim H W et al.. Airflow decline after myeloablative allogeneic hematopoietic cell transplantation: the role of community respiratory viruses. J Infect Dis. 2006; 193 1619-1625
14 Wendt C H. Community respiratory viruses: organ transplant recipients. Am J Med. 1997; 102(3A) 31-36 discussion 42-43
15 Sinnott IV J R, Cullison J P, Sweeney M S, Hammond M, Holt D A. Respiratory syncytial virus pneumonia in a cardiac transplant recipient. J Infect Dis. 1988; 158 650-651
16 Peigue-Lafeuille H, Gazuy N, Mignot P, Deteix P, Beytout D, Baguet J C. Severe respiratory syncytial virus pneumonia in an adult renal transplant recipient: successful treatment with ribavirin. Scand J Infect Dis. 1990; 22 87-89
17 Pohl C, Green M, Wald E R, Ledesma-Medina J. Respiratory syncytial virus infections in pediatric liver transplant recipients. J Infect Dis. 1992; 165 166-169
18 Blanchard S S, Gerrek M, Siegel C, Czinn S J. Significant morbidity associated with RSV infection in immunosuppressed children following liver transplantation: case report and discussion regarding need of routine prophylaxis. Pediatr Transplant. 2006; 10 826-829
19 Wendt C H, Fox J M, Hertz M I. Paramyxovirus infection in lung transplant recipients. J Heart Lung Transplant. 1995; 14 479-485
20 Kumar D, Erdman D, Keshavjee S et al.. Clinical impact of community-acquired respiratory viruses on bronchiolitis obliterans after lung transplant. Am J Transplant. 2005; 5 2031-2036
21 Harrington R D, Hooton T M, Hackman R C et al.. An outbreak of respiratory syncytial virus in a bone marrow transplant center. J Infect Dis. 1992; 165 987-993
22 Hertz M I, Englund J A, Snover D, Bitterman P B, McGlave P B. Respiratory syncytial virus-induced acute lung injury in adult patients with bone marrow transplants: a clinical approach and review of the literature. Medicine (Baltimore). 1989; 68 269-281
23 Fouillard L, Mouthon L, Laporte J P et al.. Severe respiratory syncytial virus pneumonia after autologous bone marrow transplantation: a report of three cases and review. Bone Marrow Transplant. 1992; 9 97-100
24 Abdallah A, Rowland K E, Schepetiuk S K, To L B, Bardy P. An outbreak of respiratory syncytial virus infection in a bone marrow transplant unit: effect on engraftment and outcome of pneumonia without specific antiviral treatment. Bone Marrow Transplant. 2003; 32 195-203
25 Raad I, Abbas J, Whimbey E. Infection control of nosocomial respiratory viral disease in the immunocompromised host. Am J Med. 1997; 102(3A) 48-52 discussion 3-4
26 Tablan O C, Anderson L J, Besser R, Bridges C, Hajjeh R. Guidelines for preventing health-care-associated pneumonia, 2003: recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee. MMWR Recomm Rep. 2004; 53(RR-3) 1-36
27 Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. The IMpact-RSV Study Group. Pediatrics. 1998; 102(3 Pt 1) 531-537
27a Wu H, Pfarr D S, Johnson S et al.. Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J Mol Biol. , 2007 Feb 20 [Epub ahead of print]
28 Dall'Acqua W F, Kiener P A, Wu H. Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J Biol Chem. 2006; 281 23514-23524
29 Mejias A, Chavez-Bueno S, Rios A M et al.. Comparative effects of two neutralizing anti-respiratory syncytial virus (RSV) monoclonal antibodies in the RSV murine model: time versus potency. Antimicrob Agents Chemother. 2005; 49 4700-4707
30 Ghosh S, Champlin R E, Englund J et al.. Respiratory syncytial virus upper respiratory tract illnesses in adult blood and marrow transplant recipients: combination therapy with aerosolized ribavirin and intravenous immunoglobulin. Bone Marrow Transplant. 2000; 25 751-755
31 Cortez K, Murphy B R, Almeida K N et al.. Immune-globulin prophylaxis of respiratory syncytial virus infection in patients undergoing stem-cell transplantation. J Infect Dis. 2002; 186 834-838
32 Boeckh M, Berrey M M, Bowden R A, Crawford S W, Balsley J, Corey L. Phase 1 evaluation of the respiratory syncytial virus-specific monoclonal antibody palivizumab in recipients of hematopoietic stem cell transplants. J Infect Dis. 2001; 184 350-354
33 Peck A J, Corey L, Boeckh M. Pretransplantation respiratory syncytial virus infection: impact of a strategy to delay transplantation. Clin Infect Dis. 2004; 39 673-680
34 Bowden R A. Respiratory virus infections after marrow transplant: the Fred Hutchinson Cancer Research Center experience. Am J Med. 1997; 102(3A) 27-30 discussion 42-43
35 Whimbey E, Englund J A, Couch R B. Community respiratory virus infections in immunocompromised patients with cancer. Am J Med. 1997; 102(3A) 10-18 discussion 25-26
36 Boeckh M, Englund J, Carpenter M et al.. Randomized controlled multicenter trial of aerosolized ribavirin for respiratory syncytial virus upper respiratory tract infection in hematopoietic cell transplant recipients. Clin Infect Dis. 2007; 44 245-249
37 Gruber W C, Wilson S Z, Throop B J, Wyde P R. Immunoglobulin administration and ribavirin therapy: efficacy in respiratory syncytial virus infection of the cotton rat. Pediatr Res. 1987; 21 270-274
38 Hemming V G, Rodriguez W, Kim H W et al.. Intravenous immunoglobulin treatment of respiratory syncytial virus infections in infants and young children. Antimicrob Agents Chemother. 1987; 31 1882-1886
39 De Vincenzo J P, Leombruno D, Soiffer R J, Siber G R. Immunotherapy of respiratory syncytial virus pneumonia following bone marrow transplantation. Bone Marrow Transplant. 1996; 17 1051-1056
40 Rodriguez W J, Gruber W C, Welliver R C et al.. Respiratory syncytial virus (RSV) immune globulin intravenous therapy for RSV lower respiratory tract infection in infants and young children at high risk for severe RSV infections: Respiratory Syncytial Virus Immune Globulin Study Group. Pediatrics. 1997; 99 454-461
41 Lewinsohn D M, Bowden R A, Mattson D, Crawford S W. Phase I study of intravenous ribavirin treatment of respiratory syncytial virus pneumonia after marrow transplantation. Antimicrob Agents Chemother. 1996; 40 2555-2557
42 Englund J A, Piedra P A, Whimbey E. Prevention and treatment of respiratory syncytial virus and parainfluenza viruses in immunocompromised patients. Am J Med. 1997; 102(3A) 61-70 discussion 5-6
43 Sparrelid E, Ljungman P, Ekelof-Andstrom E et al.. Ribavirin therapy in bone marrow transplant recipients with viral respiratory tract infections. Bone Marrow Transplant. 1997; 19 905-908
44 Glanville A R, Scott A I, Morton J M et al.. Intravenous ribavirin is a safe and cost-effective treatment for respiratory syncytial virus infection after lung transplantation. J Heart Lung Transplant. 2005; 24 2114-2119
45 Anaissie E J, Mahfouz T H, Aslan T et al.. The natural history of respiratory syncytial virus infection in cancer and transplant patients: implications for management. Blood. 2004; 103 1611-1617
46 Peck A, Englund J, Kuypers J et al.. Asymptomatic respiratory virus infection among hematopoietic cell recipients. 43rd Annual Meeting of Infectious Diseases Society of America, San Francisco, CA, USA 2005 Poster no. 710
47 Elting L S, Whimbey E, Lo W, Couch R, Andreeff M, Bodey G P. Epidemiology of influenza A virus infection in patients with acute or chronic leukemia. Support Care Cancer. 1995; 3 198-202
48 Yousuf H M, Englund J, Couch R et al.. Influenza among hospitalized adults with leukemia. Clin Infect Dis. 1997; 24 1095-1099
49 Englund J A. Antiviral therapy of influenza. Semin Pediatr Infect Dis. 2002; 13 120-128
50 Hassan I A, Chopra R, Swindell R, Mutton K J. Respiratory viral infections after bone marrow/peripheral stem-cell transplantation: the Christie Hospital experience. Bone Marrow Transplant. 2003; 32 73-77
51 Raboni S M, Nogueira M B, Tsuchiya L R et al.. Respiratory tract viral infections in bone marrow transplant patients. Transplantation. 2003; 76 142-146
52 Milstone A P, Brumble L M, Barnes J et al.. A single-season prospective study of respiratory viral infections in lung transplant recipients. Eur Respir J. 2006; 28 131-137
53 Nichols W G, Guthrie K A, Corey L, Boeckh M. Influenza infections after hematopoietic stem cell transplantation: risk factors, mortality, and the effect of antiviral therapy. Clin Infect Dis. 2004; 39 1300-1306
54 Ison M G, Hayden F G. Viral infections in immunocompromised patients: what's new with respiratory viruses?. Curr Opin Infect Dis. 2002; 15 355-367
55 Smith N M, Bresee J S, Shay D K, Uyeki T M, Cox N J, Strikas R A. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2006; 55(RR-10) 1-42
56 Apalsch A M, Green M, Ledesma-Medina J, Nour B, Wald E R. Parainfluenza and influenza virus infections in pediatric organ transplant recipients. Clin Infect Dis. 1995; 20 394-399
57 Mauch T J, Bratton S, Myers T, Krane E, Gentry S R, Kashtan C E. Influenza B virus infection in pediatric solid organ transplant recipients. Pediatrics. 1994; 94(2 Pt 1) 225-229
58 Briggs J D, Timbury M C, Paton A M, Bell P R. Viral infection and renal transplant rejection. BMJ. 1972; 4 520-522
59 Gabriel R, Selwyn S, Brown D et al.. Virus infections and acute renal transplant rejection. Nephron. 1976; 16 282-286
60 Hohlfeld J, Niedermeyer J, Hamm H, Schafers H J, Wagner T O, Fabel H. Seasonal onset of bronchiolitis obliterans syndrome in lung transplant recipients. J Heart Lung Transplant. 1996; 15 888-894
61 Vilchez R, McCurry K, Dauber J et al.. Influenza and parainfluenza respiratory viral infection requiring admission in adult lung transplant recipients. Transplantation. 2002; 73 1075-1078
62 Vilchez R A, McCurry K, Dauber J et al.. Influenza virus infection in adult solid organ transplant recipients. Am J Transplant. 2002; 2 287-291
63 Duchini A, Goss J A, Karpen S, Pockros P J. Vaccinations for adult solid-organ transplant recipients: current recommendations and protocols. Clin Microbiol Rev. 2003; 16 357-364
64 Sullivan K M, Dykewicz C A, Longworth D L et al.. Preventing opportunistic infections after hematopoietic stem cell transplantation: the Centers for Disease Control and Prevention, Infectious Diseases Society of America, and American Society for Blood and Marrow Transplantation Practice Guidelines and beyond. Hematology (Am Soc Hematol Educ Program). 2001; 392-421
65 Machado C M, Cardoso M R, da Rocha I F, Boas L S, Dulley F L, Pannuti C S. The benefit of influenza vaccination after bone marrow transplantation. Bone Marrow Transplant. 2005; 36 897-900
66 Engelhard D, Nagler A, Hardan I et al.. Antibody response to a two-dose regimen of influenza vaccine in allogeneic T cell-depleted and autologous BMT recipients. Bone Marrow Transplant. 1993; 11 1-5
67 Somani J, Larson R A. Reimmunization after allogeneic bone marrow transplantation. Am J Med. 1995; 98 389-398
68 Ljungman P, Cordonnier C, de Bock R et al.. Immunisations after bone marrow transplantation: results of a European survey and recommendations from the infectious diseases working party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant. 1995; 15 455-460
69 Avetisyan G, Ragnavolgyi E, Toth G T, Hassan M, Ljungman P. Cell-mediated immune responses to influenza vaccination in healthy volunteers and allogeneic stem cell transplant recipients. Bone Marrow Transplant. 2005; 36 411-415
70 Haining W N, Evans J W, Seth N P et al.. Measuring T cell immunity to influenza vaccination in children after haematopoietic stem cell transplantation. Br J Haematol. 2004; 127 322-325
71 Mazzone P J, Mossad S B, Mawhorter S D, Mehta A C, Mauer J R. Cell-mediated immune response to influenza vaccination in lung transplant recipients. J Heart Lung Transplant. 2004; 23 1175-1181
72 Pauksen K, Linde A, Hammarstrom V et al.. Granulocyte-macrophage colony-stimulating factor as immunomodulating factor together with influenza vaccination in stem cell transplant patients. Clin Infect Dis. 2000; 30 342-348
73 Ramanathan R K, Potter D M, Belani C P et al.. Randomized trial of influenza vaccine with granulocyte-macrophage colony-stimulating factor or placebo in cancer patients. J Clin Oncol. 2002; 20 4313-4318
74 Bright R A, Shay D K, Shu B, Cox N J, Klimov A I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA. 2006; 295 891-894
75 Hayden F G. Antiviral resistance in influenza viruses: implications for management and pandemic response. N Engl J Med. 2006; 354 785-788
76 Jefferson T, Demicheli V, Rivetti D, Jones M, Di Pietrantonj C, Rivetti A. Antivirals for influenza in healthy adults: systematic review. Lancet. 2006; 367 303-313
77 Vu D, Nichols W G, Barley C, Englund J A, Corey L, Boeckh M. Oseltamivir Prophylaxis in Hematopoietic Cell Transplantation Recipients: A Case-Control Study 44th Annual Meeting of Infectious Diseases Society of America Toronto, Ontario, Canada 2006 Poster no. 816
78 Hayden F G, Osterhaus A D, Treanor J J et al.. Efficacy and safety of the neuraminidase inhibitor zanamivir in the treatment of Influenzavirus infections. GG167 Influenza Study Group. N Engl J Med. 1997; 337 874-880
79 Hayden F G, Treanor J J, Fritz R S et al.. Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza: randomized controlled trials for prevention and treatment. JAMA. 1999; 282 1240-1246
80 Treanor J J, Hayden F G, Vrooman P S et al.. Efficacy and safety of the oral neuraminidase inhibitor oseltamivir in treating acute influenza: a randomized controlled trial. US Oral Neuraminidase Study Group. JAMA. 2000; 283 1016-1024
81 Whitley R J, Hayden F G, Reisinger K S et al.. Oral oseltamivir treatment of influenza in children. Pediatr Infect Dis J. 2001; 20 127-133
81a Nichols W G, Guthrie K A, Corey L, Boeckh M. Influenza infections after hematopoietic stem cell transplantation: risk factors, mortality, and the effect of antiviral therapy. Clin Infect Dis. 2004; 39 1300-1306
82 Kiso M, Mitamura K, Sakai-Tagawa Y et al.. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet. 2004; 364 759-765
83 Ison M G, Gubareva L V, Atmar R L, Treanor J, Hayden F G. Recovery of drug-resistant influenza virus from immunocompromised patients: a case series. J Infect Dis. 2006; 193 760-764
84 Monto A S, McKimm-Breschkin J L, Macken C et al.. Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob Agents Chemother. 2006; 50 2395-2402
85 Ison M G, Gnann Jr J W, Nagy-Agren S et al.. Safety and efficacy of nebulized zanamivir in hospitalized patients with serious influenza. Antivir Ther. 2003; 8 183-190
86 Hayden F G. Combination antiviral therapy for respiratory virus infections. Antiviral Res. 1996; 29 45-48
87 Chanock R M, Parrott R H, Johnson K M, Kapikian A Z, Bell J A. Myxoviruses: parainfluenza. Am Rev Respir Dis. 1963; 88(Suppl) 152-166
88 Wendt C H, Weisdorf D J, Jordan M C, Balfour Jr H H, Hertz M I. Parainfluenza virus respiratory infection after bone marrow transplantation. N Engl J Med. 1992; 326 921-926
89 Ljungman P. Respiratory virus infections in bone marrow transplant recipients: the European perspective. Am J Med. 1997; 102(3A) 44-47
90 Lewis V A, Champlin R, Englund J et al.. Respiratory disease due to parainfluenza virus in adult bone marrow transplant recipients. Clin Infect Dis. 1996; 23 1033-1037
91 Whimbey E, Vartivarian S E, Champlin R E, Elting L S, Luna M, Bodey G P. Parainfluenza virus infection in adult bone marrow transplant recipients. Eur J Clin Microbiol Infect Dis. 1993; 12 699-701
92 Nichols W G, Corey L, Gooley T, Davis C, Boeckh M. Parainfluenza virus infections after hematopoietic stem cell transplantation: risk factors, response to antiviral therapy, and effect on transplant outcome. Blood. 2001; 98 573-578
93 Dignan F, Alvares C, Riley U et al.. Parainfluenza type 3 infection post stem cell transplant: high prevalence but low mortality. J Hosp Infect. 2006; 63 452-458
94 Nichols W G, Erdman D D, Han A, Zukerman C, Corey L, Boeckh M. Prolonged outbreak of human parainfluenza virus 3 infection in a stem cell transplant outpatient department: insights from molecular epidemiologic analysis. Biol Blood Marrow Transplant. 2004; 10 58-64
95 Vilchez R A, McCurry K, Dauber J et al.. The epidemiology of parainfluenza virus infection in lung transplant recipients. Clin Infect Dis. 2001; 33 2004-2008
96 Ottolini M G, Hemming V G, Piazza F M, Johnson S A, Darnell M E, Prince G A. Topical immunoglobulin is an effective therapy for parainfluenza type 3 in a cotton rat model. J Infect Dis. 1995; 172 243-245
97 Karron R A, Belshe R B, Wright P F et al.. A live human parainfluenza type 3 virus vaccine is attenuated and immunogenic in young infants. Pediatr Infect Dis J. 2003; 22 394-405
98 Belshe R B, Newman F K, Tsai T F et al.. Phase 2 evaluation of parainfluenza type 3 cold passage mutant 45 live attenuated vaccine in healthy children 6-18 months old. J Infect Dis. 2004; 189 462-470
99 Ottolini M G, Porter D D, Blanco J C, Prince G A. A cotton rat model of human parainfluenza 3 laryngotracheitis: virus growth, pathology, and therapy. J Infect Dis. 2002; 186 1713-1717
100 Frank Jr J A, Warren R W, Tucker J A, Zeller J, Wilfert C M. Disseminated parainfluenza infection in a child with severe combined immunodeficiency. Am J Dis Child. 1983; 137 1172-1174
101 Wright J J, O'Driscoll G. Treatment of parainfluenza virus 3 pneumonia in a cardiac transplant recipient with intravenous ribavirin and methylprednisolone. J Heart Lung Transplant. 2005; 24 343-346
102 Carballal G, Videla C, Misirlian A, Requeijo P V, Aguilar Mdel C. Adenovirus type 7 associated with severe and fatal acute lower respiratory infections in Argentine children. BMC Pediatr. 2002; 2 6
103 Hong J Y, Lee H J, Piedra P A et al.. Lower respiratory tract infections due to adenovirus in hospitalized Korean children: epidemiology, clinical features, and prognosis. Clin Infect Dis. 2001; 32 1423-1429
104 Barker J H, Luby J P, Sean Dalley A, Bartek W M, Burns D K, Erdman D D. Fatal type 3 adenoviral pneumonia in immunocompetent adult identical twins. Clin Infect Dis. 2003; 37 e142-e146
105 Chuang Y Y, Chiu C H, Wong K S et al.. Severe adenovirus infection in children. J Microbiol Immunol Infect. 2003; 36 37-40
106 Ison M G. Adenovirus infections in transplant recipients. Clin Infect Dis. 2006; 43 331-339
107 Suparno C, Milligan D W, Moss P A, Mautner V. Adenovirus infections in stem cell transplant recipients: recent developments in understanding of pathogenesis, diagnosis and management. Leuk Lymphoma. 2004; 45 873-885
108 Hoffman J A, Shah A J, Ross L A, Kapoor N. Adenoviral infections and a prospective trial of cidofovir in pediatric hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2001; 7 388-394
109 Bruno B, Gooley T, Hackman R C, Davis C, Corey L, Boeckh M. Adenovirus infection in hematopoietic stem cell transplantation: effect of ganciclovir and impact on survival. Biol Blood Marrow Transplant. 2003; 9 341-352
110 Baldwin A, Kingman H, Darville M et al.. Outcome and clinical course of 100 patients with adenovirus infection following bone marrow transplantation. Bone Marrow Transplant. 2000; 26 1333-1338
111 de Mezerville M H, Tellier R, Richardson S, Hebert D, Doyle J, Allen U. Adenoviral infections in pediatric transplant recipients: a hospital-based study. Pediatr Infect Dis J. 2006; 25 815-818
112 Lion T, Baumgartinger R, Watzinger F et al.. Molecular monitoring of adenovirus in peripheral blood after allogeneic bone marrow transplantation permits early diagnosis of disseminated disease. Blood. 2003; 102 1114-1120
113 Leruez-Ville M, Minard V, Lacaille F et al.. Real-time blood plasma polymerase chain reaction for management of disseminated adenovirus infection. Clin Infect Dis. 2004; 38 45-52
114 Chakrabarti S, Mautner V, Osman H et al.. Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immunosuppression, and immune recovery. Blood. 2002; 100 1619-1627
115 Schilham M W, Claas E C, van Zaane W et al.. High levels of adenovirus DNA in serum correlate with fatal outcome of adenovirus infection in children after allogeneic stem-cell transplantation. Clin Infect Dis. 2002; 35 526-532
116 Humar A, Kumar D, Mazzulli T et al.. A surveillance study of adenovirus infection in adult solid organ transplant recipients. Am J Transplant. 2005; 5 2555-2559
117 Michaels M G, Green M, Wald E R, Starzl T E. Adenovirus infection in pediatric liver transplant recipients. J Infect Dis. 1992; 165 170-174
118 McGrath D, Falagas M E, Freeman R et al.. Adenovirus infection in adult orthotopic liver transplant recipients: incidence and clinical significance. J Infect Dis. 1998; 177 459-462
119 Seidemann K, Heim A, Pfister E D et al.. Monitoring of adenovirus infection in pediatric transplant recipients by quantitative PCR: report of six cases and review of the literature. Am J Transplant. 2004; 4 2102-2108
120 Kaufman S S, Magid M S, Tschernia A, LeLeiko N S, Fishbein T M. Discrimination between acute rejection and adenoviral enteritis in intestinal transplant recipients. Transplant Proc. 2002; 34 943-945
121 Pinchoff R J, Kaufman S S, Magid M S et al.. Adenovirus infection in pediatric small bowel transplantation recipients. Transplantation. 2003; 76 183-189
122 Ohori N P, Michaels M G, Jaffe R, Williams P, Yousem S A. Adenovirus pneumonia in lung transplant recipients. Hum Pathol. 1995; 26 1073-1079
123 Bridges N D, Spray T L, Collins M H, Bowles N E, Towbin J A. Adenovirus infection in the lung results in graft failure after lung transplantation. J Thorac Cardiovasc Surg. 1998; 116 617-623
124 Shirali G S, Ni J, Chinnock R E et al.. Association of viral genome with graft loss in children after cardiac transplantation. N Engl J Med. 2001; 344 1498-1503
125 Morfin F, Dupuis-Girod S, Mundweiler S et al.. In vitro susceptibility of adenovirus to antiviral drugs is species-dependent. Antivir Ther. 2005; 10 225-229
126 Yusuf U, Hale G A, Carr J et al.. Cidofovir for the treatment of adenoviral infection in pediatric hematopoietic stem cell transplant patients. Transplantation. 2006; 81 1398-1404
127 Wallot M A, Dohna-Schwake C, Auth M et al.. Disseminated adenovirus infection with respiratory failure in pediatric liver transplant recipients: impact of intravenous cidofovir and inhaled nitric oxide. Pediatr Transplant. 2006; 10 121-127
128 Legrand F, Berrebi D, Houhou N et al.. Early diagnosis of adenovirus infection and treatment with cidofovir after bone marrow transplantation in children. Bone Marrow Transplant. 2001; 27 621-626
129 Nagafuji K, Aoki K, Henzan H et al.. Cidofovir for treating adenoviral hemorrhagic cystitis in hematopoietic stem cell transplant recipients. Bone Marrow Transplant. 2004; 34 909-914
130 Hartline C B, Gustin K M, Wan W B et al.. Ether lipid-ester prodrugs of acyclic nucleoside phosphonates: activity against adenovirus replication in vitro. J Infect Dis. 2005; 191 396-399
131 Lankester A C, Heemskerk B, Claas E C et al.. Effect of ribavirin on the plasma viral DNA load in patients with disseminating adenovirus infection. Clin Infect Dis. 2004; 38 1521-1525
132 Feuchtinger T, Matthes-Martin S, Richard C et al.. Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br J Haematol. 2006; 134 64-76
133 van den Hoogen B G, de Jong J C, Groen J et al.. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med. 2001; 7 719-724
134 Falsey A R, Erdman D, Anderson L J, Walsh E E. Human metapneumovirus infections in young and elderly adults. J Infect Dis. 2003; 187 785-790
135 Williams J V, Crowe Jr J E, Enriquez R et al.. Human metapneumovirus infection plays an etiologic role in acute asthma exacerbations requiring hospitalization in adults. J Infect Dis. 2005; 192 1149-1153
136 Williams J V, Harris P A, Tollefson S J et al.. Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med. 2004; 350 443-450
137 Williams J V, Wang C K, Yang C F et al.. The role of human metapneumovirus in upper respiratory tract infections in children: a 20-year experience. J Infect Dis. 2006; 193 387-395
138 Martino R, Porras R P, Rabella N et al.. Prospective study of the incidence, clinical features, and outcome of symptomatic upper and lower respiratory tract infections by respiratory viruses in adult recipients of hematopoietic stem cell transplants for hematologic malignancies. Biol Blood Marrow Transplant. 2005; 11 781-796
139 Sumino K C, Agapov E, Pierce R A et al.. Detection of severe human metapneumovirus infection by real-time polymerase chain reaction and histopathological assessment. J Infect Dis. 2005; 192 1052-1060
140 Englund J, Boeckh M, Kuypers J et al.. Fatal human metapneumovirus infection in stem cell transplant recipients. Ann Intern Med. 2006; 144 344-349
141 Williams J V, Martino R, Rabella N et al.. A prospective study comparing human metapneumovirus with other respiratory viruses in adults with hematologic malignancies and respiratory tract infections. J Infect Dis. 2005; 192 1061-1065
142 Debiaggi M, Canducci F, Sampaolo M et al.. Persistent symptomless human metapneumovirus infection in hematopoietic stem cell transplant recipients. J Infect Dis. 2006; 194 474-478
143 Dare R, Sanghavi S, Bullotta A et al.. Detection of human metapneumovirus (hMPV) infection in immunosuppressed lung transplant recipients and children evaluated for pertussis. J Clin Microbiol. 2007; 45 548-552
144 Larcher C, Geltner C, Fischer H, Nachbaur D, Muller L C, Huemer H P. Human metapneumovirus infection in lung transplant recipients: clinical presentation and epidemiology. J Heart Lung Transplant. 2005; 24 1891-1901
145 Wyde P R, Chetty S N, Jewell A M, Boivin G, Piedra P A. Comparison of the inhibition of human metapneumovirus and respiratory syncytial virus by ribavirin and immune serum globulin in vitro. Antiviral Res. 2003; 60 51-59
146 Englund J A, Boeckh M, Kuypers J et al.. Brief communication: fatal human metapneumovirus infection in stem-cell transplant recipients. Ann Intern Med. 2006; 144 344-349
147 Tang R S, Mahmood K, Macphail M et al.. A host-range restricted parainfluenza virus type 3 (PIV3) expressing the human metapneumovirus (hMPV) fusion protein elicits protective immunity in African green monkeys. Vaccine. 2005; 23 1657-1667
148 Cseke G, Wright D W, Tollefson S J, Johnson J E, Crowe Jr J E, Williams J V. Human metapneumovirus fusion protein vaccines that are immunogenic and protective in cotton rats. J Virol. 2007; 81 698-707
149 Johnston S L. Natural and experimental rhinovirus infections of the lower respiratory tract. Am J Respir Crit Care Med. 1995; 152(4 Pt 2) S46-S52
150 Gern J E, Galagan D M, Jarjour N N, Dick E C, Busse W W. Detection of rhinovirus RNA in lower airway cells during experimentally induced infection. Am J Respir Crit Care Med. 1997; 155 1159-1161
151 Ghosh S, Champlin R, Couch R et al.. Rhinovirus infections in myelosuppressed adult blood and marrow transplant recipients. Clin Infect Dis. 1999; 29 528-532
152 Ison M G, Hayden F G, Kaiser L, Corey L, Boeckh M. Rhinovirus infections in hematopoietic stem cell transplant recipients with pneumonia. Clin Infect Dis. 2003; 36 1139-1143
153 Malcolm E, Arruda E, Hayden F G, Kaiser L. Clinical features of patients with acute respiratory illness and rhinovirus in their bronchoalveolar lavages. J Clin Virol. 2001; 21 9-16
154 Kaiser L, Aubert J D, Pache J C et al.. Chronic rhinoviral infection in lung transplant recipients. Am J Respir Crit Care Med. 2006; 174 1392-1399
155 Patick A K. Rhinovirus chemotherapy. Antiviral Res. 2006; 71 391-396
156 Gerna G, Campanini G, Rovida F et al.. Genetic variability of human coronavirus OC43-, 229E-, and NL63-like strains and their association with lower respiratory tract infections of hospitalized infants and immunocompromised patients. J Med Virol. 2006; 78 938-949
157 Garbino J, Crespo S, Aubert J D et al.. A prospective hospital-based study of the clinical impact of non-severe acute respiratory syndrome (Non-SARS)-related human coronavirus infection. Clin Infect Dis. 2006; 43 1009-1015
158 Chakrabarti S, Collingham K E, Stevens R H, Pillay D, Fegan C D, Milligan D W. Isolation of viruses from stools in stem cell transplant recipients: a prospective surveillance study. Bone Marrow Transplant. 2000; 25 277-282
159 Gonzalez Y, Martino R, Badell I et al.. Pulmonary enterovirus infections in stem cell transplant recipients. Bone Marrow Transplant. 1999; 23 511-513
160 Tan P L, Verneris M R, Charnas L R, Reck S J, van Burik J A, Blazar B R. Outcome of CNS and pulmonary enteroviral infections after hematopoietic cell transplantation. Pediatr Blood Cancer. 2005; 45 74-75
161 Winkelstein J A, Marino M C, Lederman H M et al.. X-linked agammaglobulinemia: report on a United States registry of 201 patients. Medicine (Baltimore). 2006; 85 193-202
162 Donoso Mantke O, Meyer R, Prosch S et al.. High prevalence of cardiotropic viruses in myocardial tissue from explanted hearts of heart transplant recipients and heart donors: a 3-year retrospective study from a German patients’ pool. J Heart Lung Transplant. 2005; 24 1632-1638
163 Allander T, Tammi M T, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci USA. 2005; 102 12891-12896
164 Manning A, Russell V, Eastick K et al.. Epidemiological profile and clinical associations of human bocavirus and other human parvoviruses. J Infect Dis. 2006; 194 1283-1290
165 Kesebir D, Vazquez M, Weibel C et al.. Human bocavirus infection in young children in the United States: molecular epidemiological profile and clinical characteristics of a newly emerging respiratory virus. J Infect Dis. 2006; 194 1276-1282
166 Chung J Y, Han T H, Kim C K, Kim S W. Bocavirus infection in hospitalized children, South Korea. Emerg Infect Dis. 2006; 12 1254-1256
167 Foulongne V, Olejnik Y, Perez V, Elaerts S, Rodiere M, Segondy M. Human bocavirus in French children. Emerg Infect Dis. 2006; 12 1251-1253
168 Bastien N, Brandt K, Dust K, Ward D, Li Y. Human Bocavirus infection, Canada. Emerg Infect Dis. 2006; 12 848-850
169 Sloots T P, McErlean P, Speicher D J, Arden K E, Nissen M D, Mackay I M. Evidence of human coronavirus HKU1 and human bocavirus in Australian children. J Clin Virol. 2006; 35 99-102
170 Kumar D, Humar A. Pandemic influenza and its implications for transplantation. Am J Transplant. 2006; 6 1512-1517
171 Guidelines for preventing opportunistic infections among hematopoietic stem cell transplant recipients. MMWR Recomm Rep. 2000; 49(RR-10) 1-128
172 King Jr J C. Community respiratory viruses in individuals with human immunodeficiency virus infection. Am J Med. 1997; 102(3A) 19-24 discussion 5-6
173 Madhi S A, Schoub B, Simmank K, Blackburn N, Klugman K P. Increased burden of respiratory viral associated severe lower respiratory tract infections in children infected with human immunodeficiency virus type-1. J Pediatr. 2000; 137 78-84
174 Madhi S A, Venter M, Madhi A, Petersen M K, Klugman K P. Differing manifestations of respiratory syncytial virus-associated severe lower respiratory tract infections in human immunodeficiency virus type 1-infected and uninfected children. Pediatr Infect Dis J. 2001; 20 164-170
175 Madhi S A, Kuwanda L, Cutland C, Klugman K P. Five-year cohort study of hospitalization for respiratory syncytial virus associated lower respiratory tract infection in African children. J Clin Virol. 2006; 36 215-221
176 Neuzil K M, Coffey C S, Mitchel Jr E F, Griffin M R. Cardiopulmonary hospitalizations during influenza season in adults and adolescents with advanced HIV infection. J Acquir Immune Defic Syndr. 2003; 34 304-307
177 Madhi S A, Ramasamy N, Bessellar T G, Saloojee H, Klugman K P. Lower respiratory tract infections associated with influenza A and B viruses in an area with a high prevalence of pediatric human immunodeficiency type 1 infection. Pediatr Infect Dis J. 2002; 21 291-297
178 Malaspina A, Moir S, Orsega S M et al.. Compromised B cell responses to influenza vaccination in HIV-infected individuals. J Infect Dis. 2005; 191 1442-1450
179 Kroon F P, van Dissel J T, de Jong J C, Zwinderman K, van Furth R. Antibody response after influenza vaccination in HIV-infected individuals: a consecutive 3-year study. Vaccine. 2000; 18 3040-3049
180 Atashili J, Kalilani L, Adimora A A. Efficacy and clinical effectiveness of influenza vaccines in HIV-infected individuals: a meta-analysis. BMC Infect Dis. 2006; 6 138
181 Madhi S A, Ramasamy N, Petersen K, Madhi A, Klugman K P. Severe lower respiratory tract infections associated with human parainfluenza viruses 1-3 in children infected and noninfected with HIV type 1. Eur J Clin Microbiol Infect Dis. 2002; 21 499-505
182 Madhi S A, Ludewick H, Abed Y, Klugman K P, Boivin G. Human metapneumovirus-associated lower respiratory tract infections among hospitalized human immunodeficiency virus type 1 (HIV-1)-infected and HIV-1-uninfected African infants. Clin Infect Dis. 2003; 37 1705-1710
183 Mendoza Sanchez M C, Ruiz-Contreras J, Vivanco J L et al.. Respiratory virus infections in children with cancer or HIV infection. J Pediatr Hematol Oncol. 2006; 28 154-159
184 Vilchez R A, Dauber J, Kusne S. Infectious etiology of bronchiolitis obliterans: the respiratory viruses connection-myth or reality?. Am J Transplant. 2003; 3 245-249
185 Vilchez R A, Dauber J, McCurry K, Iacono A, Kusne S. Parainfluenza virus infection in adult lung transplant recipients: an emergent clinical syndrome with implications on allograft function. Am J Transplant. 2003; 3 116-120
186 Lim A K, Parsons S, Ierino F. Adenovirus tubulointerstitial nephritis presenting as a renal allograft space occupying lesion. Am J Transplant. 2005; 5 2062-2066
187 Ljungman P, Ribaud P, Eyrich M et al.. Cidofovir for adenovirus infections after allogeneic hematopoietic stem cell transplantation: a survey by the Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant. 2003; 31 481-486
188 McLaughlin G E, Delis S, Kashimawo L et al.. Adenovirus infection in pediatric liver and intestinal transplant recipients: utility of DNA detection by PCR. Am J Transplant. 2003; 3 224-228
189 Runde V, Ross S, Trenschel R et al.. Adenoviral infection after allogeneic stem cell transplantation (SCT): report on 130 patients from a single SCT unit involved in a prospective multi center surveillance study. Bone Marrow Transplant. 2001; 28 51-57
190 Cane P A, van den Hoogen B G, Chakrabarti S, Fegan C D, Osterhaus A D. Human metapneumovirus in a haematopoietic stem cell transplant recipient with fatal lower respiratory tract disease. Bone Marrow Transplant. 2003; 31 309-310
191 Lau S K, Woo P C, Yip C C et al.. Coronavirus HKU1 and other coronavirus infections in Hong Kong. J Clin Microbiol. 2006; 44 2063-2071
192 Arnold J C, Singh K K, Spector S A, Sawyer M H. Human bocavirus: prevalence and clinical spectrum at a children's hospital. Clin Infect Dis. 2006; 43 283-288
193 Kaplan N M, Dove W, Abu-Zeid A F, Shamoon H E, Abd-Eldayem S A, Hart C A. Human bocavirus infection among children, Jordan. Emerg Infect Dis. 2006; 12 1418-1420

Janet A EnglundM.D.

Children’s Hospital and Regional Medical Center

4800 Sand Point Way NE #W8851, Seattle, WA 98105

eMail: janet.englund@seattlechildrens.org