Other Respiratory Viruses as a Cause of Community-Acquired Pneumonia

James M. Walter

doi:10.1055/s-0040-1710537

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2020; 41(04): 579-591
DOI: 10.1055/s-0040-1710537

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Other Respiratory Viruses as a Cause of Community-Acquired Pneumonia

James M. Walter

¹Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Northwestern University Feinberg School of Medicine, Chicago, Illinois

› Author Affiliations

Abstract

Community-acquired pneumonia (CAP) is a major cause of morbidity and mortality worldwide. There is growing appreciation of the burden of noninfluenza viral pathogens in CAP. Due to multiple factors including pneumococcal vaccination programs, declining rates of cigarette smoking, an aging population, and increasingly sensitive diagnostic tests, respiratory viruses are now the most common pathogens detected in CAP, outpacing Streptococcus pneumoniae. Noninfluenza respiratory pathogens are widely accepted as causal pathogens in CAP including in immunocompetent patients. This review provides an overview of five noninfluenza respiratory viral pathogens commonly implicated in CAP pathogenesis: rhinovirus, human metapneumovirus, respiratory syncytial virus, human parainfluenza virus, and human adenoviruses. Nucleic acid amplification testing platforms and their impact on antimicrobial stewardship efforts are also considered.

Keywords

community-acquired pneumonia - viral pneumonia - rhinovirus - human metapneumovirus - respiratory syncytial virus - human adenovirus - nucleic acid amplification

Full Text

References

References
1 Ramirez JA, Wiemken TL, Peyrani P. , et al; University of Louisville Pneumonia Study Group. Adults hospitalized with pneumonia in the United States: incidence, epidemiology, and mortality. Clin Infect Dis 2017; 65 (11) 1806-1812
2 Bartlett JG, Mundy LM. Community-acquired pneumonia. N Engl J Med 1995; 333 (24) 1618-1624
3 Lexau CA, Lynfield R, Danila R. , et al; Active Bacterial Core Surveillance Team. Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine. JAMA 2005; 294 (16) 2043-2051
4 Griffin MR, Zhu Y, Moore MR, Whitney CG, Grijalva CGUS. U.S. hospitalizations for pneumonia after a decade of pneumococcal vaccination. N Engl J Med 2013; 369 (02) 155-163
5 Moore MR, Link-Gelles R, Schaffner W. , et al. Effect of use of 13-valent pneumococcal conjugate vaccine in children on invasive pneumococcal disease in children and adults in the USA: analysis of multisite, population-based surveillance. Lancet Infect Dis 2015; 15 (03) 301-309
6 von Gottberg A, de Gouveia L, Tempia S. , et al; GERMS-SA Investigators. Effects of vaccination on invasive pneumococcal disease in South Africa. N Engl J Med 2014; 371 (20) 1889-1899
7 Nuorti JP, Butler JC, Farley MM. , et al; Active Bacterial Core Surveillance Team. Cigarette smoking and invasive pneumococcal disease. N Engl J Med 2000; 342 (10) 681-689
8 Jain S, Self WH, Wunderink RG. , et al; CDC EPIC Study Team. Community-acquired pneumonia requiring hospitalization among U.S. adults. N Engl J Med 2015; 373 (05) 415-427
9 Gadsby NJ, Russell CD, McHugh MP. , et al. Comprehensive molecular testing for respiratory pathogens in community-acquired pneumonia. Clin Infect Dis 2016; 62 (07) 817-823
10 Pick H, Daniel P, Rodrigo C. , et al. Pneumococcal serotype trends, surveillance and risk factors in UK adult pneumonia, 2013-18. Thorax 2020; 75 (01) 38-49
11 Isturiz RE, Ramirez J, Self WH. , et al. Pneumococcal epidemiology among us adults hospitalized for community-acquired pneumonia. Vaccine 2019; 37 (25) 3352-3361
12 Di Pasquale MF, Sotgiu G, Gramegna A. , et al; GLIMP Investigators. Prevalence and etiology of community-acquired pneumonia in immunocompromised patients. Clin Infect Dis 2019; 68 (09) 1482-1493
13 Peyrani P, Arnold FW, Bordon J. , et al. Incidence and mortality of adults hospitalized with community-acquired pneumonia according to clinical course. Chest 2020; 157 (01) 34-41
14 United States Census Bureau. 2017 National Population Projections Tables: Main Series. Available at: https://www.census.gov/data/tables/2017/demo/popproj/2017-summary-tables.html . Accessed March 1, 2020
15 Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005; 352 (17) 1749-1759
16 Iuliano AD, Roguski KM, Chang HH. , et al; Global Seasonal Influenza-associated Mortality Collaborator Network. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2018; 391 (10127): 1285-1300
17 Falsey AR, Walsh EE. Viral pneumonia in older adults. Clin Infect Dis 2006; 42 (04) 518-524
18 Walter JM, Wunderink RG. Testing for respiratory viruses in adults with severe lower respiratory infection. Chest 2018; 154 (05) 1213-1222
19 Burk M, El-Kersh K, Saad M, Wiemken T, Ramirez J, Cavallazzi R. Viral infection in community-acquired pneumonia: a systematic review and meta-analysis. Eur Respir Rev 2016; 25 (140) 178-188
20 Choi SH, Hong SB, Ko GB. , et al. Viral infection in patients with severe pneumonia requiring intensive care unit admission. Am J Respir Crit Care Med 2012; 186 (04) 325-332
21 Shorr AF, Fisher K, Micek ST, Kollef MH. The burden of viruses in pneumonia associated with acute respiratory failure: an underappreciated issue. Chest 2018; 154 (01) 84-90
22 Tramuto F, Maida CM, Napoli G. , et al. Burden and viral aetiology of influenza-like illness and acute respiratory infection in intensive care units. Microbes Infect 2016; 18 (04) 270-276
23 van Someren Gréve F, Juffermans NP, Bos LDJ. , et al. Respiratory viruses in invasively ventilated critically ill patients-a prospective multicenter observational study. Crit Care Med 2018; 46 (01) 29-36
24 Legoff J, Zucman N, Lemiale V. , et al. Clinical significance of upper airway virus detection in critically ill hematology patients. Am J Respir Crit Care Med 2019; 199 (04) 518-528
25 Greenberg SB. Update on human rhinovirus and coronavirus infections. Semin Respir Crit Care Med 2016; 37 (04) 555-571
26 Turner RB. Rhinovirus: more than just a common cold virus. J Infect Dis 2007; 195 (06) 765-766
27 Musher DM. How contagious are common respiratory tract infections?. N Engl J Med 2003; 348 (13) 1256-1266
28 Reese SM, Thompson M, Price CS, Young HL. Evidence of nosocomial transmission of human rhinovirus in a neonatal intensive care unit. Am J Infect Control 2016; 44 (03) 355-357
29 Waghmare A, Xie H, Kuypers J. , et al. Human rhinovirus infections in hematopoietic cell transplant recipients: risk score for progression to lower respiratory tract infection. Biol Blood Marrow Transplant 2019; 25 (05) 1011-1021
30 Jacobs SE, Lamson DM, Soave R. , et al. Clinical and molecular epidemiology of human rhinovirus infections in patients with hematologic malignancy. J Clin Virol 2015; 71: 51-58
31 Jacobs SE, Soave R, Shore TB. , et al. Human rhinovirus infections of the lower respiratory tract in hematopoietic stem cell transplant recipients. Transpl Infect Dis 2013; 15 (05) 474-486
32 Malcolm E, Arruda E, Hayden FG, Kaiser L. Clinical features of patients with acute respiratory illness and rhinovirus in their bronchoalveolar lavages. J Clin Virol 2001; 21 (01) 9-16
33 Kaiser L, Aubert JD, Pache JC. , et al. Chronic rhinoviral infection in lung transplant recipients. Am J Respir Crit Care Med 2006; 174 (12) 1392-1399
34 Arruda E, Pitkäranta A, Witek Jr TJ, Doyle CA, Hayden FG. Frequency and natural history of rhinovirus infections in adults during autumn. J Clin Microbiol 1997; 35 (11) 2864-2868
35 George SN, Garcha DS, Mackay AJ. , et al. Human rhinovirus infection during naturally occurring COPD exacerbations. Eur Respir J 2014; 44 (01) 87-96
36 Molyneaux PL, Mallia P, Cox MJ. , et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013; 188 (10) 1224-1231
37 Mallia P, Footitt J, Sotero R. , et al. Rhinovirus infection induces degradation of antimicrobial peptides and secondary bacterial infection in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012; 186 (11) 1117-1124
38 Wiemken T, Peyrani P, Bryant K. , et al. Incidence of respiratory viruses in patients with community-acquired pneumonia admitted to the intensive care unit: results from the Severe Influenza Pneumonia Surveillance (SIPS) project. Eur J Clin Microbiol Infect Dis 2013; 32 (05) 705-710
39 Karhu J, Ala-Kokko TI, Vuorinen T, Ohtonen P, Syrjälä H. Lower respiratory tract virus findings in mechanically ventilated patients with severe community-acquired pneumonia. Clin Infect Dis 2014; 59 (01) 62-70
40 Harris II JM, Gwaltney Jr JM. Incubation periods of experimental rhinovirus infection and illness. Clin Infect Dis 1996; 23 (06) 1287-1290
41 Jennings LC, Anderson TP, Beynon KA. , et al. Incidence and characteristics of viral community-acquired pneumonia in adults. Thorax 2008; 63 (01) 42-48
42 Aviragen Therapeutics Inc. Aviragen Therapeutics Announces Top-Line Results from Phase 2b SPIRITUS Trial of Vapendavir. Available at: https://www.globenewswire.com/news-release/2017/02/13/916652/0/en/Aviragen-Therapeutics-Announces-Top-Line-Results-from-Phase-2b-SPIRITUS-Trial-of-Vapendavir.html . Accessed March 1, 2020
43 Senior K. FDA panel rejects common cold treatment. Lancet Infect Dis 2002; 2 (05) 264
44 Ruuskanen O, Waris M, Kainulainen L. Treatment of persistent rhinovirus infection with pegylated interferon α2a and ribavirin in patients with hypogammaglobulinemia. Clin Infect Dis 2014; 58 (12) 1784-1786
45 van den Hoogen BG, de Jong JC, Groen J. , et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med 2001; 7 (06) 719-724
46 Howard LM, Edwards KM, Zhu Y. , et al. Clinical features of human metapneumovirus-associated community-acquired pneumonia hospitalizations. Clin Infect Dis 2020; ciaa088
47 Kahn JS. Epidemiology of human metapneumovirus. Clin Microbiol Rev 2006; 19 (03) 546-557
48 Louie JK, Schnurr DP, Pan CY. , et al. A summer outbreak of human metapneumovirus infection in a long-term-care facility. J Infect Dis 2007; 196 (05) 705-708
49 Boivin G, De Serres G, Hamelin ME. , et al. An outbreak of severe respiratory tract infection due to human metapneumovirus in a long-term care facility. Clin Infect Dis 2007; 44 (09) 1152-1158
50 Kim S, Sung H, Im HJ, Hong SJ, Kim MN. Molecular epidemiological investigation of a nosocomial outbreak of human metapneumovirus infection in a pediatric hemato-oncology patient population. J Clin Microbiol 2009; 47 (04) 1221-1224
51 Englund JA, Boeckh M, Kuypers J. , et al. Brief communication: fatal human metapneumovirus infection in stem-cell transplant recipients. Ann Intern Med 2006; 144 (05) 344-349
52 Godet C, Le Goff J, Beby-Defaux A. , et al. Human metapneumovirus pneumonia in patients with hematological malignancies. J Clin Virol 2014; 61 (04) 593-596
53 Hopkins P, McNeil K, Kermeen F. , et al. Human metapneumovirus in lung transplant recipients and comparison to respiratory syncytial virus. Am J Respir Crit Care Med 2008; 178 (08) 876-881
54 Larcher C, Geltner C, Fischer H, Nachbaur D, Müller LC, Huemer HP. Human metapneumovirus infection in lung transplant recipients: clinical presentation and epidemiology. J Heart Lung Transplant 2005; 24 (11) 1891-1901
55 Shah DP, Shah PK, Azzi JM, El Chaer F, Chemaly RF. Human metapneumovirus infections in hematopoietic cell transplant recipients and hematologic malignancy patients: a systematic review. Cancer Lett 2016; 379 (01) 100-106
56 Seo S, Gooley TA, Kuypers JM. , et al. Human metapneumovirus infections following hematopoietic cell transplantation: factors associated with disease progression. Clin Infect Dis 2016; 63 (02) 178-185
57 Gray GC, Capuano AW, Setterquist SF. , et al. Multi-year study of human metapneumovirus infection at a large US Midwestern Medical Referral Center. J Clin Virol 2006; 37 (04) 269-276
58 Stockton J, Stephenson I, Fleming D, Zambon M. Human metapneumovirus as a cause of community-acquired respiratory illness. Emerg Infect Dis 2002; 8 (09) 897-901
59 Falsey AR, Erdman D, Anderson LJ, Walsh EE. Human metapneumovirus infections in young and elderly adults. J Infect Dis 2003; 187 (05) 785-790
60 Hasvold J, Sjoding M, Pohl K, Cooke C, Hyzy RC. The role of human metapneumovirus in the critically ill adult patient. J Crit Care 2016; 31 (01) 233-237
61 Walsh EE, Peterson DR, Falsey AR. Human metapneumovirus infections in adults: another piece of the puzzle. Arch Intern Med 2008; 168 (22) 2489-2496
62 Liao RS, Appelgate DM, Pelz RK. An outbreak of severe respiratory tract infection due to human metapneumovirus in a long-term care facility for the elderly in Oregon. J Clin Virol 2012; 53 (02) 171-173
63 Te Wierik MJ, Nguyen DT, Beersma MF, Thijsen SF, Heemstra KA. An outbreak of severe respiratory tract infection caused by human metapneumovirus in a residential care facility for elderly in Utrecht, the Netherlands, January to March 2010. Euro Surveill 2012; 17 (13) 17
64 Honda H, Iwahashi J, Kashiwagi T. , et al. Outbreak of human metapneumovirus infection in elderly inpatients in Japan. J Am Geriatr Soc 2006; 54 (01) 177-180
65 Martinello RA, Esper F, Weibel C, Ferguson D, Landry ML, Kahn JS. Human metapneumovirus and exacerbations of chronic obstructive pulmonary disease. J Infect 2006; 53 (04) 248-254
66 Rohde G, Borg I, Arinir U. , et al. Relevance of human metapneumovirus in exacerbations of COPD. Respir Res 2005; 6: 150
67 Vicente D, Montes M, Cilla G, Pérez-Trallero E. Human metapneumovirus and chronic obstructive pulmonary disease. Emerg Infect Dis 2004; 10 (07) 1338-1339
68 Boivin G, Abed Y, Pelletier G. , et al. Virological features and clinical manifestations associated with human metapneumovirus: a new paramyxovirus responsible for acute respiratory-tract infections in all age groups. J Infect Dis 2002; 186 (09) 1330-1334
69 Wong CK, Lai V, Wong YC. Comparison of initial high resolution computed tomography features in viral pneumonia between metapneumovirus infection and severe acute respiratory syndrome. Eur J Radiol 2012; 81 (05) 1083-1087
70 Schuster JE, Cox RG, Hastings AK. , et al. A broadly neutralizing human monoclonal antibody exhibits in vivo efficacy against both human metapneumovirus and respiratory syncytial virus. J Infect Dis 2015; 211 (02) 216-225
71 Corti D, Bianchi S, Vanzetta F. , et al. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature 2013; 501 (7467): 439-443
72 Hamelin ME, Gagnon C, Prince GA. , et al. Prophylactic and therapeutic benefits of a monoclonal antibody against the fusion protein of human metapneumovirus in a mouse model. Antiviral Res 2010; 88 (01) 31-37
73 Renaud C, Xie H, Seo S. , et al. Mortality rates of human metapneumovirus and respiratory syncytial virus lower respiratory tract infections in hematopoietic cell transplantation recipients. Biol Blood Marrow Transplant 2013; 19 (08) 1220-1226
74 Griffiths C, Drews SJ, Marchant DJ. Respiratory syncytial virus: infection, detection, and new options for prevention and treatment. Clin Microbiol Rev 2017; 30 (01) 277-319
75 Nam HH, Ison MG. Respiratory syncytial virus infection in adults. BMJ 2019; 366: l5021
76 Bont L, Checchia PA, Fauroux B. , et al. Defining the epidemiology and burden of severe respiratory syncytial virus infection among infants and children in western countries. Infect Dis Ther 2016; 5 (03) 271-298
77 Drysdale SB, Green CA, Sande CJ. Best practice in the prevention and management of paediatric respiratory syncytial virus infection. Ther Adv Infect Dis 2016; 3 (02) 63-71
78 Bont L. Nosocomial RSV infection control and outbreak management. Paediatr Respir Rev 2009; 10 (Suppl. 01) 16-17
79 Englund JA, Sullivan CJ, Jordan MC, Dehner LP, Vercellotti GM, Balfour Jr HH. Respiratory syncytial virus infection in immunocompromised adults. Ann Intern Med 1988; 109 (03) 203-208
80 Hertz MI, Englund JA, Snover D, Bitterman PB, McGlave PB. 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 (05) 269-281
81 Khanna N, Widmer AF, Decker M. , et al. Respiratory syncytial virus infection in patients with hematological diseases: single-center study and review of the literature. Clin Infect Dis 2008; 46 (03) 402-412
82 Gottlieb J, Zamora MR, Hodges T. , et al. ALN-RSV01 for prevention of bronchiolitis obliterans syndrome after respiratory syncytial virus infection in lung transplant recipients. J Heart Lung Transplant 2016; 35 (02) 213-221
83 Shah JN, Chemaly RF. Management of RSV infections in adult recipients of hematopoietic stem cell transplantation. Blood 2011; 117 (10) 2755-2763
84 Khawaja F, Chemaly RF. Respiratory syncytial virus in hematopoietic cell transplant recipients and patients with hematologic malignancies. Haematologica 2019; 104 (07) 1322-1331
85 Shah DP, Ghantoji SS, Ariza-Heredia EJ. , et al. Immunodeficiency scoring index to predict poor outcomes in hematopoietic cell transplant recipients with RSV infections. Blood 2014; 123 (21) 3263-3268
86 Ieven M, Coenen S, Loens K. , et al; GRACE consortium. Aetiology of lower respiratory tract infection in adults in primary care: a prospective study in 11 European countries. Clin Microbiol Infect 2018; 24 (11) 1158-1163
87 Østby AC, Gubbels S, Baake G, Nielsen LP, Riedel C, Arpi M. Respiratory virology and microbiology in intensive care units: a prospective cohort study. APMIS 2013; 121 (11) 1097-1108
88 Thompson WW, Shay DK, Weintraub E. , et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003; 289 (02) 179-186
89 Colosia AD, Yang J, Hillson E. , et al. The epidemiology of medically attended respiratory syncytial virus in older adults in the United States: a systematic review. PLoS One 2017; 12 (08) e0182321
90 Shi T, Denouel A, Tietjen AK. , et al; RESCEU Investigators. Global disease burden estimates of respiratory syncytial virus-associated acute respiratory infection in older adults in 2015: a systematic review and meta-analysis. J Infect Dis 2019; (e-pub ahead of print)
91 Ackerson B, Tseng HF, Sy LS. , et al. Severe morbidity and mortality associated with respiratory syncytial virus versus influenza infection in hospitalized older adults. Clin Infect Dis 2019; 69 (02) 197-203
92 Ramaswamy M, Groskreutz DJ, Look DC. Recognizing the importance of respiratory syncytial virus in chronic obstructive pulmonary disease. COPD 2009; 6 (01) 64-75
93 Walsh EE, Peterson DR, Falsey AR. Risk factors for severe respiratory syncytial virus infection in elderly persons. J Infect Dis 2004; 189 (02) 233-238
94 Anderson NW, Binnicker MJ, Harris DM. , et al. Morbidity and mortality among patients with respiratory syncytial virus infection: a 2-year retrospective review. Diagn Microbiol Infect Dis 2016; 85 (03) 367-371
95 Dowell SF, Anderson LJ, Gary Jr HE. , et al. Respiratory syncytial virus is an important cause of community-acquired lower respiratory infection among hospitalized adults. J Infect Dis 1996; 174 (03) 456-462
96 O'Shea MK, Ryan MA, Hawksworth AW, Alsip BJ, Gray GC. Symptomatic respiratory syncytial virus infection in previously healthy young adults living in a crowded military environment. Clin Infect Dis 2005; 41 (03) 311-317
97 Wald TG, Miller BA, Shult P, Drinka P, Langer L, Gravenstein S. Can respiratory syncytial virus and influenza A be distinguished clinically in institutionalized older persons?. J Am Geriatr Soc 1995; 43 (02) 170-174
98 Mayer JL, Lehners N, Egerer G, Kauczor HU, Heußel CP. CT-morphological characterization of respiratory syncytial virus (RSV) pneumonia in immune-compromised adults. RoFo Fortschr Geb Rontgenstr Nuklearmed 2014; 186 (07) 686-692
99 Miller Jr WT, Mickus TJ, Barbosa Jr E, Mullin C, Van Deerlin VM, Shiley KT. CT of viral lower respiratory tract infections in adults: comparison among viral organisms and between viral and bacterial infections. AJR Am J Roentgenol 2011; 197 (05) 1088-1095
100 Shah DP, Ghantoji SS, Shah JN. , et al. Impact of aerosolized ribavirin on mortality in 280 allogeneic haematopoietic stem cell transplant recipients with respiratory syncytial virus infections. J Antimicrob Chemother 2013; 68 (08) 1872-1880
101 Chemaly RF, Aitken SL, Wolfe CR, Jain R, Boeckh MJ. Aerosolized ribavirin: the most expensive drug for pneumonia. Transpl Infect Dis 2016; 18 (04) 634-636
102 Beaird OE, Freifeld A, Ison MG. , et al. Current practices for treatment of respiratory syncytial virus and other non-influenza respiratory viruses in high-risk patient populations: a survey of institutions in the Midwestern Respiratory Virus Collaborative. Transpl Infect Dis 2016; 18 (02) 210-215
103 Ralston SL, Lieberthal AS, Meissner HC. , et al; American Academy of Pediatrics. Clinical practice guideline: the diagnosis, management, and prevention of bronchiolitis. Pediatrics 2014; 134 (05) e1474-e1502
104 de Fontbrune FS, Robin M, Porcher R. , et al. Palivizumab treatment of respiratory syncytial virus infection after allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 2007; 45 (08) 1019-1024
105 Falsey AR, Koval C, DeVincenzo JP, Walsh EE. Compassionate use experience with high-titer respiratory syncytical virus (RSV) immunoglobulin in RSV-infected immunocompromised persons. Transpl Infect Dis 2017; 19 (02) 19
106 Marty FM, Chemaly RF, Mullane KM. , et al. A phase 2b, randomized, double-blind, placebo-controlled multicenter study evaluating antiviral effects, pharmacokinetics, safety, and tolerability of presatovir in hematopoietic cell transplant recipients with respiratory syncytial virus (RSV) infection of the lower respiratory tract. Clin Infect Dis 2019; (e-pub ahead of print)
107 Gottlieb J, Torres F, Haddad T. , et al. A phase 2b randomized controlled trial of presatovir, an oral rsv fusion inhibitor, for the treatment of respiratory syncytial virus (RSV) in lung transplant (LT) recipients. J Heart Lung Transplant 2018; 37: S155
108 DeVincenzo JP, McClure MW, Symons JA. , et al. Activity of oral ALS-008176 in a respiratory syncytial virus challenge study. N Engl J Med 2015; 373 (21) 2048-2058
109 Chiu C. Novel immunological insights in accelerating RSV vaccine development. Vaccine 2017; 35 (03) 459-460
110 Chanock RM. Association of a new type of cytopathogenic myxovirus with infantile croup. J Exp Med 1956; 104 (04) 555-576
111 Russell E, Ison MG. Parainfluenza virus in the hospitalized adult. Clin Infect Dis 2017; 65 (09) 1570-1576
112 Fry AM, Curns AT, Harbour K, Hutwagner L, Holman RC, Anderson LJ. Seasonal trends of human parainfluenza viral infections: United States, 1990-2004. Clin Infect Dis 2006; 43 (08) 1016-1022
113 Bailey ES, Lobaugh-Jin E, Smith B. , et al. Molecular epidemiology of an outbreak of human parainfluenza virus 3 among oncology patients. J Hosp Infect 2019; 103 (03) 349-353
114 Ryan S, Gillespie E, Stuart RL. A parainfluenza virus type 3 outbreak at a residential aged care facility: the role of microbiologic testing in early identification and antimicrobial stewardship. Am J Infect Control 2017; 45 (02) 203-205
115 Vilchez RA, 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 (02) 116-120
116 Shah DP, Shah PK, Azzi JM, Chemaly RF. Parainfluenza virus infections in hematopoietic cell transplant recipients and hematologic malignancy patients: a systematic review. Cancer Lett 2016; 370 (02) 358-364
117 Alimi Y, Lim WS, Lansbury L, Leonardi-Bee J, Nguyen-Van-Tam JS. Systematic review of respiratory viral pathogens identified in adults with community-acquired pneumonia in Europe. J Clin Virol 2017; 95: 26-35
118 Fiore AE, Iverson C, Messmer T. , et al. Outbreak of pneumonia in a long-term care facility: antecedent human parainfluenza virus 1 infection may predispose to bacterial pneumonia. J Am Geriatr Soc 1998; 46 (09) 1112-1117
119 Greenberg SB, Allen M, Wilson J, Atmar RL. Respiratory viral infections in adults with and without chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 162 (01) 167-173
120 Marx A, Gary Jr HE, Marston BJ. , et al. Parainfluenza virus infection among adults hospitalized for lower respiratory tract infection. Clin Infect Dis 1999; 29 (01) 134-140
121 Ferguson PE, Sorrell TC, Bradstock K, Carr P, Gilroy NM. Parainfluenza virus type 3 pneumonia in bone marrow transplant recipients: multiple small nodules in high- resolution lung computed tomography scans provide a radiological clue to diagnosis. Clin Infect Dis 2009; 48 (07) 905-909
122 Branche AR, Falsey AR. Parainfluenza virus infection. Semin Respir Crit Care Med 2016; 37 (04) 538-554
123 Park SY, Baek S, Lee SO. , et al. Efficacy of oral ribavirin in hematologic disease patients with paramyxovirus infection: analytic strategy using propensity scores. Antimicrob Agents Chemother 2013; 57 (02) 983-989
124 Salvatore M, Satlin MJ, Jacobs SE. , et al. DAS181 for treatment of parainfluenza virus infections in hematopoietic stem cell transplant recipients at a single center. Biol Blood Marrow Transplant 2016; 22 (05) 965-970
125 Chemaly RF, Moss R, Marty FM. , et al. 1715. A randomized, double-blind, placebo-controlled multicenter phase 2 trial to examine the effects of DAS181 in immunocompromised (IC) patients with parainfluenza virus (PIV) lower respiratory tract infection (LRTI) on supplemental oxygen (SO). Open Forum Infect Dis 2018; 5: S50-S51
126 Lion T. Adenovirus infections in immunocompetent and immunocompromised patients. Clin Microbiol Rev 2014; 27 (03) 441-462
127 Ison MG, Hirsch HH. Community-acquired respiratory viruses in transplant patients: diversity, impact, unmet clinical needs. Clin Microbiol Rev 2019; 32 (04) 32
128 Ison MG, Hayden RT. Adenovirus. Microbiol Spectr 2016; 4 (04) DMIH2-0020-2015
129 Sandrock C, Stollenwerk N. Acute febrile respiratory illness in the ICU: reducing disease transmission. Chest 2008; 133 (05) 1221-1231
130 Cassir N, Hraiech S, Nougairede A, Zandotti C, Fournier PE, Papazian L. Outbreak of adenovirus type 1 severe pneumonia in a French intensive care unit, September-October 2012. Euro Surveill 2014; 19 (39) 19
131 Lynch III JP, Kajon AE. Adenovirus: epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin Respir Crit Care Med 2016; 37 (04) 586-602
132 Centers for Disease Control and Prevention (CDC). Acute respiratory disease associated with adenovirus serotype 14--four states, 2006-2007. MMWR Morb Mortal Wkly Rep 2007; 56 (45) 1181-1184
133 Zhou F, Wang Y, Liu Y. , et al; and the CAP-China Network. Disease severity and clinical outcomes of community-acquired pneumonia caused by non-influenza respiratory viruses in adults: a multicentre prospective registry study from the CAP-China Network. Eur Respir J 2019; 54 (02) 54
134 Klinger JR, Sanchez MP, Curtin LA, Durkin M, Matyas B. Multiple cases of life-threatening adenovirus pneumonia in a mental health care center. Am J Respir Crit Care Med 1998; 157 (02) 645-649
135 Centers for Disease Control and Prevention (CDC). Civilian outbreak of adenovirus acute respiratory disease--South Dakota, 1997. MMWR Morb Mortal Wkly Rep 1998; 47 (27) 567-570
136 Zhu Z, Zhang Y, Xu S. , et al. Outbreak of acute respiratory disease in China caused by B2 species of adenovirus type 11. J Clin Microbiol 2009; 47 (03) 697-703
137 Parcell BJ, McIntyre PG, Yirrell DL. , et al. Prison and community outbreak of severe respiratory infection due to adenovirus type 14p1 in Tayside, UK. J Public Health (Oxf) 2015; 37 (01) 64-69
138 Potter RN, Cantrell JA, Mallak CT, Gaydos JC. Adenovirus-associated deaths in US military during postvaccination period, 1999-2010. Emerg Infect Dis 2012; 18 (03) 507-509
139 Kolavic-Gray SA, Binn LN, Sanchez JL. , et al. Large epidemic of adenovirus type 4 infection among military trainees: epidemiological, clinical, and laboratory studies. Clin Infect Dis 2002; 35 (07) 808-818
140 Tate JE, Bunning ML, Lott L. , et al. Outbreak of severe respiratory disease associated with emergent human adenovirus serotype 14 at a US air force training facility in 2007. J Infect Dis 2009; 199 (10) 1419-1426
141 Rogers AE, Lu X, Killerby M. , et al. Outbreak of acute respiratory illness associated with adenovirus type 4 at the U.S. Naval Academy, 2016. MSMR 2019; 26 (02) 21-27
142 Lewis PF, Schmidt MA, Lu X. , et al. A community-based outbreak of severe respiratory illness caused by human adenovirus serotype 14. J Infect Dis 2009; 199 (10) 1427-1434
143 Centers for Disease Control and Prevention (CDC). Outbreak of adenovirus 14 respiratory illness--Prince of Wales Island, Alaska, 2008. MMWR Morb Mortal Wkly Rep 2010; 59 (01) 6-10
144 Cao B, Huang GH, Pu ZH. , et al. Emergence of community-acquired adenovirus type 55 as a cause of community-onset pneumonia. Chest 2014; 145 (01) 79-86
145 Tan D, Zhu H, Fu Y. , et al. Severe community-acquired pneumonia caused by human adenovirus in immunocompetent adults: a multicenter case series. PLoS One 2016; 11 (03) e0151199
146 Vento TJ, Prakash V, Murray CK. , et al. Pneumonia in military trainees: a comparison study based on adenovirus serotype 14 infection. J Infect Dis 2011; 203 (10) 1388-1395
147 Yoon H, Jhun BW, Kim SJ, Kim K. Clinical characteristics and factors predicting respiratory failure in adenovirus pneumonia. Respirology 2016; 21 (07) 1243-1250
148 Park JY, Kim BJ, Lee EJ. , et al. Clinical features and courses of adenovirus pneumonia in healthy young adults during an outbreak among Korean military personnel. PLoS One 2017; 12 (01) e0170592
149 Park CK, Kwon H, Park JY. Thin-section computed tomography findings in 104 immunocompetent patients with adenovirus pneumonia. Acta Radiol 2017; 58 (08) 937-943
150 Hiwarkar P, Kosulin K, Cesaro S. , et al. Management of adenovirus infection in patients after haematopoietic stem cell transplantation: state-of-the-art and real-life current approach: a position statement on behalf of the Infectious Diseases Working Party of the European Society of Blood and Marrow Transplantation. Rev Med Virol 2018; 28 (03) e1980
151 Kim SJ, Kim K, Park SB, Hong DJ, Jhun BW. Outcomes of early administration of cidofovir in non-immunocompromised patients with severe adenovirus pneumonia. PLoS One 2015; 10 (04) e0122642
152 Lee M, Kim S, Kwon OJ. , et al. Treatment of adenoviral acute respiratory distress syndrome using cidofovir with extracorporeal membrane oxygenation: case series and literature review. J Intensive Care Med 2017; 32 (03) 231-238
153 Ko JH, Lim JU, Choi JY. , et al. Early cidofovir administration might be associated with a lower probability of respiratory failure in treating human adenovirus pneumonia: a retrospective cohort study. Clin Microbiol Infect 2019; (e-pub ahead of print)
154 Ison MG, Green M. ; AST Infectious Diseases Community of Practice. Adenovirus in solid organ transplant recipients. Am J Transplant 2009; 9 (Suppl. 04) S161-S165
155 Ljungman P, Ribaud P, Eyrich M. , et al; Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. 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 (06) 481-486
156 Ramsay ID, Attwood C, Irish D, Griffiths PD, Kyriakou C, Lowe DM. Disseminated adenovirus infection after allogeneic stem cell transplant and the potential role of brincidofovir - case series and 10 year experience of management in an adult transplant cohort. J Clin Virol 2017; 96: 73-79
157 Schultze-Florey RE, Tischer-Zimmermann S, Heuft HG. , et al. Transfer of Hexon- and Penton-selected adenovirus-specific T cells for refractory adenovirus infection after haploidentical stem cell transplantation. Transpl Infect Dis 2020; 22 (01) e13201
158 Talbot HK, Falsey AR. The diagnosis of viral respiratory disease in older adults. Clin Infect Dis 2010; 50 (05) 747-751
159 Wen SC, Williams JV. New approaches for immunization and therapy against human metapneumovirus. Clin Vaccine Immunol 2015; 22 (08) 858-866
160 She RC, Polage CR, Caram LB. , et al. Performance of diagnostic tests to detect respiratory viruses in older adults. Diagn Microbiol Infect Dis 2010; 67 (03) 246-250
161 McAdam AJ, Riley AM. Developments in tissue culture detection of respiratory viruses. Clin Lab Med 2009; 29 (04) 623-634
162 Chartrand C, Tremblay N, Renaud C, Papenburg J. Diagnostic accuracy of rapid antigen detection tests for respiratory syncytial virus infection: systematic review and meta-analysis. J Clin Microbiol 2015; 53 (12) 3738-3749
163 Chartrand C, Leeflang MM, Minion J, Brewer T, Pai M. Accuracy of rapid influenza diagnostic tests: a meta-analysis. Ann Intern Med 2012; 156 (07) 500-511
164 Ishmael FT, Stellato C. Principles and applications of polymerase chain reaction: basic science for the practicing physician. Ann Allergy Asthma Immunol 2008; 101 (04) 437-443
165 Popowitch EB, O'Neill SS, Miller MB. Comparison of the Biofire FilmArray RP, Genmark eSensor RVP, Luminex xTAG RVPv1, and Luminex xTAG RVP fast multiplex assays for detection of respiratory viruses. J Clin Microbiol 2013; 51 (05) 1528-1533
166 Mulpuru S, Aaron SD, Ronksley PE, Lawrence N, Forster AJ. Hospital resource utilization and patient outcomes associated with respiratory viral testing in hospitalized patients. Emerg Infect Dis 2015; 21 (08) 1366-1371
167 Shiley KT, Lautenbach E, Lee I. The use of antimicrobial agents after diagnosis of viral respiratory tract infections in hospitalized adults: antibiotics or anxiolytics?. Infect Control Hosp Epidemiol 2010; 31 (11) 1177-1183
168 Hernes SS, Hagen E, Quarsten H, Bjorvatn B, Bakke PS. No impact of early real-time PCR screening for respiratory viruses on length of stay and use of antibiotics in elderly patients hospitalized with symptoms of a respiratory tract infection in a single center in Norway. Eur J Clin Microbiol Infect Dis 2014; 33 (03) 359-364
169 Oosterheert JJ, van Loon AM, Schuurman R. , et al. Impact of rapid detection of viral and atypical bacterial pathogens by real-time polymerase chain reaction for patients with lower respiratory tract infection. Clin Infect Dis 2005; 41 (10) 1438-1444
170 Branche AR, Walsh EE, Vargas R. , et al. Serum procalcitonin measurement and viral testing to guide antibiotic use for respiratory infections in hospitalized adults: a randomized controlled trial. J Infect Dis 2015; 212 (11) 1692-1700
171 Brendish NJ, Malachira AK, Armstrong L. , et al. Routine molecular point-of-care testing for respiratory viruses in adults presenting to hospital with acute respiratory illness (ResPOC): a pragmatic, open-label, randomised controlled trial. Lancet Respir Med 2017; 5 (05) 401-411
172 Zautner AE, Groß U, Emele MF, Hagen RM, Frickmann H. More pathogenicity or just more pathogens?—on the interpretation problem of multiple pathogen detections with diagnostic multiplex assays. Front Microbiol 2017; 8: 1210
173 Self WH, Williams DJ, Zhu Y. , et al. Respiratory viral detection in children and adults: comparing asymptomatic controls and patients with community-acquired pneumonia. J Infect Dis 2016; 213 (04) 584-591
174 Boonyaratanakornkit J, Vivek M, Xie H. , et al. Predictive value of respiratory viral detection in the upper respiratory tract for infection of the lower respiratory tract with hematopoietic stem cell transplantation. J Infect Dis 2020; 221 (03) 379-388
175 Ruuskanen O, Lahti E, Jennings LC, Murdoch DR. Viral pneumonia. Lancet 2011; 377 (9773): 1264-1275
176 Semret M, Schiller I, Jardin BA. , et al. Multiplex respiratory virus testing for antimicrobial stewardship: a prospective assessment of antimicrobial use and clinical outcomes among hospitalized adults. J Infect Dis 2017; 216 (08) 936-944
177 Johnston SL, Szigeti M, Cross M. , et al; AZALEA Trial Team. Azithromycin for acute exacerbations of asthma: the AZALEA randomized clinical trial. JAMA Intern Med 2016; 176 (11) 1630-1637
178 Meeker D, Linder JA, Fox CR. , et al. Effect of behavioral interventions on inappropriate antibiotic prescribing among primary care practices: a randomized clinical trial. JAMA 2016; 315 (06) 562-570
179 Smith SB, Ruhnke GW, Weiss CH, Waterer GW, Wunderink RG. Trends in pathogens among patients hospitalized for pneumonia from 1993 to 2011. JAMA Intern Med 2014; 174 (11) 1837-1839
180 Nathan C, Cars O. Antibiotic resistance--problems, progress, and prospects. N Engl J Med 2014; 371 (19) 1761-1763