Top

European Journal of Clinical Microbiology & Infectious Diseases

Published in:

01-08-2021 | Influenza Virus | Original Article

Comparison of clinical characteristics and outcomes between respiratory syncytial virus and influenza-related pneumonia in China from 2013 to 2019

Authors: Liang Chen, Xiudi Han, YanLi Li, Chunxiao Zhang, Xiqian Xing

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 8/2021

Abstract

This study aims to compare clinical characteristics and severity between adults with respiratory syncytial virus (RSV-p) and influenza-related pneumonia (Flu-p). A total of 127 patients with RSV-p, 693 patients with influenza A-related pneumonia (FluA-p), and 386 patients with influenza B-related pneumonia (FluB-p) were retrospectively reviewed from 2013 through 2019 in five teaching hospitals in China. A multivariate logistic regression model indicated that age ≥ 50 years, cerebrovascular disease, chronic kidney disease, solid malignant tumor, nasal congestion, myalgia, sputum production, respiratory rates ≥ 30 beats/min, lymphocytes < 0.8×10⁹/L, and blood albumin < 35 g/L were predictors that differentiated RSV-p from Flu-p. After adjusting for confounders, a multivariate logistic regression analysis confirmed that, relative to RSV-p, FluA-p (OR 2.313, 95% CI 1.377–3.885, p = 0.002) incurred an increased risk for severe outcomes, including invasive ventilation, ICU admission, and 30-day mortality; FluB-p (OR 1.630, 95% CI 0.958–2.741, p = 0.071) was not associated with increased risk. Some clinical variables were useful for discriminating RSV-p from Flu-p. The severity of RSV-p was less than that of FluA-p, but was comparable to FluB-p.

Available only for authorised users

Fineberg HV (2014) Pandemic preparedness and response--lessons from the H1N1 influenza of 2009. N Engl J Med 370(14):1335–1342. https://doi.org/10.1056/NEJMra1208802CrossRefPubMed

Abdel-Hady DM, Al Balushi RM, Al Abri BA, Al Abri SS, Al Kindi HS, Al-Jardani AK, Al Yaqubi FM, Al Abaidani IS (2018) Estimating the burden of influenza-associated hospitalization and deaths in Oman (2012-2015). Influenza Other Respir Viruses 12(1):146–152. https://doi.org/10.1111/irv.12500CrossRefPubMed

Jones RM, Xia Y (2018) Annual burden of occupationally-acquired influenza infections in hospitals and emergency departments in the United States. Risk Anal 38(3):442–453. https://doi.org/10.1111/risa.12854CrossRefPubMed

Ly S, Arashiro T, Ieng V, Tsuyuoka R, Parry A, Horwood P, Heng S, Hamid S, Vandemaele K, Chin S, Sar B, Arima Y (2017) Establishing seasonal and alert influenza thresholds in Cambodia using the WHO method: implications for effective utilization of influenza surveillance in the tropics and subtropics. Western Pac Surveill Response J 8(1):22–32. https://doi.org/10.5365/WPSAR.2017.8.1.002CrossRefPubMedPubMedCentral

Stein RT, Bont LJ, Zar H, Polack FP, Park C, Claxton A, Borok G, Butylkova Y, Wegzyn C (2017) Respiratory syncytial virus hospitalization and mortality: systematic review and meta-analysis. Pediatr Pulmonol 52(4):556–569. https://doi.org/10.1002/ppul.23570CrossRefPubMed

Kodama F, Nace DA, Jump RLP (2017) Respiratory syncytial virus and other noninfluenza respiratory viruses in older adults. Infect Dis Clin N Am 31(4):767–790. https://doi.org/10.1016/j.idc.2017.07.006CrossRef

Malosh RE, Martin ET, Callear AP, Petrie JG, Lauring AS, Lamerato L, Fry AM, Ferdinands J, Flannery B, Monto AS (2017) Respiratory syncytial virus hospitalization in middle-aged and older adults. J Clin Virol 96:37–43. https://doi.org/10.1016/j.jcv.2017.09.001CrossRefPubMedPubMedCentral

Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE (2005) Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352(17):1749–1759. https://doi.org/10.1056/NEJMoa043951CrossRefPubMed

Matias G, Taylor R, Haguinet F, Schuck-Paim C, Lustig R, Shinde V (2014) Estimates of mortality attributable to influenza and RSV in the United States during 1997-2009 by influenza type or subtype, age, cause of death, and risk status. Influenza Other Respir Viruses 8(5):507–515. https://doi.org/10.1111/irv.12258CrossRefPubMedPubMedCentral

10.

Sundaram ME, Meece JK, Sifakis F, Gasser RA Jr, Belongia EA (2014) Medically attended respiratory syncytial virus infections in adults aged ≥ 50 years: clinical characteristics and outcomes. Clin Infect Dis 58(3):342–349. https://doi.org/10.1093/cid/cit767CrossRefPubMed

11.

Griffiths C, Drews SJ, Marchant DJ (2017) Respiratory syncytial virus: infection, detection, and new options for prevention and treatment. Clin Microbiol Rev 30(1):277–319. https://doi.org/10.1128/CMR.00010-16CrossRefPubMed

12.

Jain S, Self WH, Wunderink RG, Fakhran S, Balk R, Bramley AM, Reed C, Grijalva CG, Anderson EJ, Courtney DM, Chappell JD, Qi C, Hart EM, Carroll F, Trabue C, Donnelly HK, Williams DJ, Zhu Y, Arnold SR, Ampofo K, Waterer GW, Levine M, Lindstrom S, Winchell JM, Katz JM, Erdman D, Schneider E, Hicks LA, McCullers JA, Pavia AT, Edwards KM, Finelli L, Team CES (2015) Community-acquired pneumonia requiring hospitalization among U.S. adults. N Engl J Med 373(5):415–427. https://doi.org/10.1056/NEJMoa1500245CrossRefPubMedPubMedCentral

13.

Nam HH, Ison MG (2019) Respiratory syncytial virus infection in adults. BMJ 366:l5021. https://doi.org/10.1136/bmj.l5021CrossRefPubMed

14.

Ackerson B, Tseng HF, Sy LS, Solano Z, Slezak J, Luo Y, Fischetti CA, Shinde V (2019) Severe morbidity and mortality associated with respiratory syncytial virus versus influenza infection in hospitalized older adults. Clin Infect Dis 69(2):197–203. https://doi.org/10.1093/cid/ciy991CrossRefPubMed

15.

Kestler M, Munoz P, Mateos M, Adrados D, Bouza E (2018) Respiratory syncytial virus burden among adults during flu season: an underestimated pathology. J Hosp Infect 100(4):463–468. https://doi.org/10.1016/j.jhin.2018.03.034CrossRefPubMed

16.

Malley R, DeVincenzo J, Ramilo O, Dennehy PH, Meissner HC, Gruber WC, Sanchez PJ, Jafri H, Balsley J, Carlin D, Buckingham S, Vernacchio L, Ambrosino DM (1998) Reduction of respiratory syncytial virus (RSV) in tracheal aspirates in intubated infants by use of humanized monoclonal antibody to RSV F protein. J Infect Dis 178(6):1555–1561. https://doi.org/10.1086/314523CrossRefPubMed

17.

Jansen AG, Sanders EA, Hoes AW, van Loon AM, Hak E (2007) Influenza- and respiratory syncytial virus-associated mortality and hospitalisations. Eur Respir J 30(6):1158–1166. https://doi.org/10.1183/09031936.00034407CrossRefPubMed

18.

Bednarska K, Hallmann-Szelinska E, Kondratiuk K, Brydak LB (2015) Evaluation of the activity of influenza and influenza-like viruses in the epidemic season 2013/2014. Adv Exp Med Biol 857:1–7. https://doi.org/10.1007/5584_2015_116CrossRefPubMedPubMedCentral

19.

Panozzo CA, Fowlkes AL, Anderson LJ (2007) Variation in timing of respiratory syncytial virus outbreaks: lessons from national surveillance. Pediatr Infect Dis J 26(11 Suppl):S41–S45. https://doi.org/10.1097/INF.0b013e318157da82CrossRefPubMed

20.

Chen L, Zhou F, Li H, Xing X, Han X, Wang Y, Zhang C, Suo L, Wang J, Yu G, Wang G, Yao X, Yu H, Wang L, Liu M, Xue C, Liu B, Zhu X, Li Y, Xiao Y, Cui X, Li L, Uyeki TM, Wang C, Cao B, network CA-C (2018) Disease characteristics and management of hospitalised adolescents and adults with community-acquired pneumonia in China: a retrospective multicentre survey. BMJ Open 8 (2):e018709. https://doi.org/10.1136/bmjopen-2017-018709.

21.

Chatzis O, Darbre S, Pasquier J, Meylan P, Manuel O, Aubert JD, Beck-Popovic M, Masouridi-Levrat S, Ansari M, Kaiser L, Posfay-Barbe KM, Asner SA (2018) Burden of severe RSV disease among immunocompromised children and adults: a 10 year retrospective study. BMC Infect Dis 18(1):111. https://doi.org/10.1186/s12879-018-3002-3CrossRefPubMedPubMedCentral

22.

Kossyvakis A, Mentis AA, Tryfinopoulou K, Pogka V, Kalliaropoulos A, Antalis E, Lytras T, Meijer A, Tsiodras S, Karakitsos P, Mentis AF (2017) Antiviral susceptibility profile of influenza A viruses; keep an eye on immunocompromised patients under prolonged treatment. Eur J Clin Microbiol Infect Dis 36(2):361–371. https://doi.org/10.1007/s10096-016-2809-3CrossRefPubMed

23.

Muthuri SG, Venkatesan S, Myles PR, Leonardi-Bee J, Al Khuwaitir TS, Al Mamun A, Anovadiya AP, Azziz-Baumgartner E, Baez C, Bassetti M, Beovic B, Bertisch B, Bonmarin I, Booy R, Borja-Aburto VH, Burgmann H, Cao B, Carratala J, Denholm JT, Dominguez SR, Duarte PA, Dubnov-Raz G, Echavarria M, Fanella S, Gao Z, Gerardin P, Giannella M, Gubbels S, Herberg J, Iglesias AL, Hoger PH, Hu X, Islam QT, Jimenez MF, Kandeel A, Keijzers G, Khalili H, Knight M, Kudo K, Kusznierz G, Kuzman I, Kwan AM, Amine IL, Langenegger E, Lankarani KB, Leo YS, Linko R, Liu P, Madanat F, Mayo-Montero E, McGeer A, Memish Z, Metan G, Mickiene A, Mikic D, Mohn KG, Moradi A, Nymadawa P, Oliva ME, Ozkan M, Parekh D, Paul M, Polack FP, Rath BA, Rodriguez AH, Sarrouf EB, Seale AC, Sertogullarindan B, Siqueira MM, Skret-Magierlo J, Stephan F, Talarek E, Tang JW, To KK, Torres A, Torun SH, Tran D, Uyeki TM, Van Zwol A, Vaudry W, Vidmar T, Yokota RT, Zarogoulidis P, Investigators PC, Nguyen-Van-Tam JS (2014) Effectiveness of neuraminidase inhibitors in reducing mortality in patients admitted to hospital with influenza A H1N1pdm09 virus infection: a meta-analysis of individual participant data. Lancet Respir Med 2(5):395–404. https://doi.org/10.1016/S2213-2600(14)70041-4CrossRefPubMedPubMedCentral

24.

Ku YH, Chan KS, Yang CC, Tan CK, Chuang YC, Yu WL (2017) Higher mortality of severe influenza patients with probable aspergillosis than those with and without other coinfections. J Formos Med Assoc 116(9):660–670. https://doi.org/10.1016/j.jfma.2017.06.002CrossRefPubMed

25.

Lee N, Lui GC, Wong KT, Li TC, Tse EC, Chan JY, Yu J, Wong SS, Choi KW, Wong RY, Ngai KL, Hui DS, Chan PK (2013) High morbidity and mortality in adults hospitalized for respiratory syncytial virus infections. Clin Infect Dis 57(8):1069–1077. https://doi.org/10.1093/cid/cit471CrossRefPubMed

26.

Loubet P, Lenzi N, Valette M, Foulongne V, Krivine A, Houhou N, Lagathu G, Rogez S, Alain S, Duval X, Galtier F, Postil D, Tattevin P, Vanhems P, Carrat F, Lina B, Launay O, Group FS (2017) Clinical characteristics and outcome of respiratory syncytial virus infection among adults hospitalized with influenza-like illness in France. Clin Microbiol Infect 23(4):253–259. https://doi.org/10.1016/j.cmi.2016.11.014CrossRefPubMed

27.

Casalegno JS, Eibach D, Valette M, Enouf V, Daviaud I, Behillil S, Vabret A, Soulary JC, Benchaib M, Cohen JM, van der Werf S, Mosnier A, Lina B (2017) Performance of influenza case definitions for influenza community surveillance: based on the French influenza surveillance network GROG, 2009-2014. Euro Surveill 22(14):30504. https://doi.org/10.2807/1560-7917.ES.2017.22.14.30504CrossRefPubMedPubMedCentral

28.

Pedersen CJ, Quinn JV, Rogan DT, Yang S (2019) Factors associated with influenza in an emergency department setting. J Emerg Med 56(5):478–483. https://doi.org/10.1016/j.jemermed.2018.12.012CrossRefPubMed

29.

Lalueza A, Folgueira D, Diaz-Pedroche C, Hernandez-Jimenez P, Ayuso B, Castillo C, Laureiro J, Trujillo H, Torres M, Lumbreras C (2019) Severe lymphopenia in hospitalized patients with influenza virus infection as a marker of a poor outcome. Infect Dis (Lond) 51(7):543–546. https://doi.org/10.1080/23744235.2019.1598572CrossRef

30.

Bellelli V, d'Ettorre G, Celani L, Borrazzo C, Ceccarelli G, Venditti M (2019) Clinical significance of lymphocytopenia in patients hospitalized with pneumonia caused by influenza virus. Crit Care 23(1):330. https://doi.org/10.1186/s13054-019-2608-1CrossRefPubMedPubMedCentral

31.

Fox A, Le NM, Horby P, van Doorn HR, Nguyen VT, Nguyen HH, Nguyen TC, Vu DP, Nguyen MH, Diep NT, Bich VT, Huong HT, Taylor WR, Farrar J, Wertheim H, Nguyen VK (2012) Severe pandemic H1N1 2009 infection is associated with transient NK and T deficiency and aberrant CD8 responses. PLoS One 7(2):e31535. https://doi.org/10.1371/journal.pone.0031535CrossRefPubMedPubMedCentral

32.

Russell CD, Unger SA, Walton M, Schwarze J (2017) The human immune response to respiratory syncytial virus infection. Clin Microbiol Rev 30(2):481–502. https://doi.org/10.1128/CMR.00090-16CrossRefPubMedPubMedCentral

33.

O'Donnell DR, Carrington D (2002) Peripheral blood lymphopenia and neutrophilia in children with severe respiratory syncytial virus disease. Pediatr Pulmonol 34(2):128–130. https://doi.org/10.1002/ppul.10140CrossRefPubMed

34.

Shi SJ, Li H, Liu M, Liu YM, Zhou F, Liu B, Qu JX, Cao B (2017) Mortality prediction to hospitalized patients with influenza pneumonia: PO2/FiO2 combined lymphocyte count is the answer. Clin Respir J 11(3):352–360. https://doi.org/10.1111/crj.12346CrossRefPubMed

35.

Guo L, Wei D, Zhang X, Wu Y, Li Q, Zhou M, Qu J (2019) Clinical features predicting mortality risk in patients with viral pneumonia: the MuLBSTA score. Front Microbiol 10:2752. https://doi.org/10.3389/fmicb.2019.02752CrossRefPubMedPubMedCentral

36.

Vakil E, Sheshadri A, Faiz SA, Shah DP, Zhu Y, Li L, Kmeid J, Azzi J, Balagani A, Bashoura L, Ariza-Heredia E, Chemaly RF (2018) Risk factors for mortality after respiratory syncytial virus lower respiratory tract infection in adults with hematologic malignancies. Transpl Infect Dis 20(6):e12994. https://doi.org/10.1111/tid.12994CrossRefPubMedPubMedCentral

37.

Roe MF, Bloxham DM, White DK, Ross-Russell RI, Tasker RT, O'Donnell DR (2004) Lymphocyte apoptosis in acute respiratory syncytial virus bronchiolitis. Clin Exp Immunol 137(1):139–145. https://doi.org/10.1111/j.1365-2249.2004.02512.xCrossRefPubMedPubMedCentral

38.

Smith PK, Wang SZ, Dowling KD, Forsyth KD (2001) Leucocyte populations in respiratory syncytial virus-induced bronchiolitis. J Paediatr Child Health 37(2):146–151. https://doi.org/10.1046/j.1440-1754.2001.00618.xCrossRefPubMed

39.

Kim HJ, Choi SM, Lee J, Park YS, Lee CH, Yim JJ, Yoo CG, Kim YW, Han SK, Lee SM (2018) Respiratory virus of severe pneumonia in South Korea: prevalence and clinical implications. PLoS One 13(6):e0198902. https://doi.org/10.1371/journal.pone.0198902CrossRefPubMedPubMedCentral

40.

Gamino-Arroyo AE, Moreno-Espinosa S, Llamosas-Gallardo B, Ortiz-Hernandez AA, Guerrero ML, Galindo-Fraga A, Galan-Herrera JF, Prado-Galbarro FJ, Beigel JH, Ruiz-Palacios GM, Noyola DE, Mexico Emerging Infectious Diseases Clinical Research N (2017) Epidemiology and clinical characteristics of respiratory syncytial virus infections among children and adults in Mexico. Influenza Other Respir Viruses 11(1):48–56. https://doi.org/10.1111/irv.12414CrossRefPubMed

41.

Katsurada N, Suzuki M, Aoshima M, Yaegashi M, Ishifuji T, Asoh N, Hamashige N, Abe M, Ariyoshi K, Morimoto K, Adult Pneumonia Study G-J (2017) The impact of virus infections on pneumonia mortality is complex in adults: a prospective multicentre observational study. BMC Infect Dis 17(1):755. https://doi.org/10.1186/s12879-017-2858-yCrossRefPubMedPubMedCentral

42.

Mullooly JP, Bridges CB, Thompson WW, Chen J, Weintraub E, Jackson LA, Black S, Shay DK, Vaccine Safety Datalink Adult Working G (2007) Influenza- and RSV-associated hospitalizations among adults. Vaccine 25(5):846–855. https://doi.org/10.1016/j.vaccine.2006.09.041CrossRefPubMed

43.

Caini S, de Mora D, Olmedo M, Portugal D, Becerra MA, Mejia M, Pacurucu MC, Ojeda J, Bonaccorsi G, Lorini C, Paget J, Bruno A (2019) The epidemiology and severity of respiratory viral infections in a tropical country: Ecuador, 2009-2016. J Infect Public Health 12(3):357–363. https://doi.org/10.1016/j.jiph.2018.12.003CrossRefPubMed

44.

Minney-Smith CA, Selvey LA, Levy A, Smith DW (2019) Post-pandemic influenza A/H1N1pdm09 is associated with more severe outcomes than A/H3N2 and other respiratory viruses in adult hospitalisations. Epidemiol Infect 147:e310. https://doi.org/10.1017/S095026881900195XCrossRefPubMedPubMedCentral

45.

Ishiguro T, Takayanagi N, Kanauchi T, Uozumi R, Kawate E, Takaku Y, Kagiyama N, Shimizu Y, Hoshi T, Morita S, Sugita Y (2016) Clinical and radiographic comparison of influenza virus-associated pneumonia among three viral subtypes. Intern Med 55(7):731–737. https://doi.org/10.2169/internalmedicine.55.5227CrossRefPubMed

Title: Comparison of clinical characteristics and outcomes between respiratory syncytial virus and influenza-related pneumonia in China from 2013 to 2019
Authors: Liang Chen
Xiudi Han
YanLi Li
Chunxiao Zhang
Xiqian Xing
Publication date: 01-08-2021
Publisher: Springer Berlin Heidelberg
Keywords: Influenza Virus
Respiratory Syncytial Virus Infection
Pneumonia
Influenza
Published in: European Journal of Clinical Microbiology & Infectious Diseases / Issue 8/2021
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI: https://doi.org/10.1007/s10096-021-04217-2

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2021

Epigenetic alterations and genetic variations of angiotensin-converting enzyme 2 (ACE2) as a functional receptor for SARS-CoV-2: potential clinical implications

Changes in antimicrobial resistance and outcomes of health care–associated infections

Therapeutic efficacy of chitosan nanoparticles loaded with BCG-polysaccharide nucleic acid and ovalbumin on airway inflammation in asthmatic mice

Antimicrobial stewardship experience in paediatrics: first-year activity report

Bloodstream infections in older population: epidemiology, outcome, and impact of multidrug resistance

Clinical characteristics of SARS-CoV-2 by re-infection vs. reactivation: a case series from Iran

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage