Skip to main content
Top
Published in: BMC Medicine 1/2014

Open Access 01-12-2014 | Research article

A clinical prediction rule for diagnosing human infections with avian influenza A(H7N9) in a hospital emergency department setting

Authors: Qiaohong Liao, Dennis K M Ip, Tim K Tsang, Bin Cao, Hui Jiang, Fengfeng Liu, Jiandong Zheng, Zhibin Peng, Peng Wu, Yang Huai, Eric H Y Lau, Luzhao Feng, Gabriel M Leung, Hongjie Yu, Benjamin J Cowling

Published in: BMC Medicine | Issue 1/2014

Login to get access

Abstract

Background

Human infections with avian influenza A(H7N9) virus are associated with severe illness and high mortality. To better inform triage decisions of hospitalization and management, we developed a clinical prediction rule for diagnosing patients with A(H7N9) and determined its predictive performance.

Methods

Clinical details on presentation of adult patients hospitalized with either A(H7N9)(n = 121) in China from March to May 2013 or other causes of acute respiratory infections (n = 2,603) in Jingzhou City, China from January 2010 through September 2012 were analyzed. A clinical prediction rule was developed using a two-step coefficient-based multivariable logistic regression scoring method and evaluated with internal validation by bootstrapping.

Results

In step 1, predictors for A(H7N9) included male sex, poultry exposure history, and fever, haemoptysis, or shortness of breath on history and physical examination. In step 2, haziness or pneumonic consolidation on chest radiographs and leukopenia were also associated with a higher probability of A(H7N9). The observed risk of A(H7N9) was 0.3% for those assigned to the low-risk group and 2.5%, 4.3%, and 44.0% for tertiles 1 through 3, respectively, in the high-risk group. This prediction rule achieved good model performance, with an optimism-corrected sensitivity of 0.93, a specificity of 0.80, and an area under the receiver-operating characteristic curve of 0.96.

Conclusions

A simple decision rule based on data readily obtainable in the setting of patients’ first clinical presentations from the first wave of the A/H7N9 epidemic in China has been developed. This prediction rule has achieved good model performance in predicting their risk of A(H7N9) infection and should be useful in guiding important clinical and public health decisions in a timely and objective manner. Data to be gathered with its use in the current evolving second wave of the A/H7N9 epidemic in China will help to inform its performance in the field and contribute to its further refinement.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, et al: Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013, 368: 1888-1897. 10.1056/NEJMoa1304459.CrossRefPubMed Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, et al: Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013, 368: 1888-1897. 10.1056/NEJMoa1304459.CrossRefPubMed
2.
go back to reference Wu Y, Gao GF: Compiling of comprehensive data of human infections with novel influenza A (H7N9) virus. Front Med. 2013, 7: 275-276. 10.1007/s11684-013-0285-z.CrossRefPubMed Wu Y, Gao GF: Compiling of comprehensive data of human infections with novel influenza A (H7N9) virus. Front Med. 2013, 7: 275-276. 10.1007/s11684-013-0285-z.CrossRefPubMed
3.
go back to reference Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, Ni MY, Zhang Q, Ip DK, Yu J, Li Y, Wang L, Tu W, Meng L, Wu JT, Luo H, Li Q, Shu Y, Li Z, Feng Z, Yang W, Wang Y, Leung GM, Yu H: Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet. 2013, 382: 129-137. 10.1016/S0140-6736(13)61171-X.CrossRefPubMedPubMedCentral Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, Ni MY, Zhang Q, Ip DK, Yu J, Li Y, Wang L, Tu W, Meng L, Wu JT, Luo H, Li Q, Shu Y, Li Z, Feng Z, Yang W, Wang Y, Leung GM, Yu H: Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet. 2013, 382: 129-137. 10.1016/S0140-6736(13)61171-X.CrossRefPubMedPubMedCentral
4.
go back to reference Gao HN, Lu HZ, Cao B, Du B, Shang H, Gan JH, Lu SH, Yang YD, Fang Q, Shen YZ, Xi XM, Gu Q, Zhou XM, Qu HP, Yan Z, Li FM, Zhao W, Gao ZC, Wang GF, Ruan LX, Wang WH, Ye J, Cao HF, Li XW, Zhang WH, Fang XC, He J, Liang WF, Xie J, Zeng M, et al: Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med. 2013, 368: 2277-2285. 10.1056/NEJMoa1305584.CrossRefPubMed Gao HN, Lu HZ, Cao B, Du B, Shang H, Gan JH, Lu SH, Yang YD, Fang Q, Shen YZ, Xi XM, Gu Q, Zhou XM, Qu HP, Yan Z, Li FM, Zhao W, Gao ZC, Wang GF, Ruan LX, Wang WH, Ye J, Cao HF, Li XW, Zhang WH, Fang XC, He J, Liang WF, Xie J, Zeng M, et al: Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med. 2013, 368: 2277-2285. 10.1056/NEJMoa1305584.CrossRefPubMed
5.
go back to reference Yu H, Cowling BJ, Feng L, Lau EH, Liao Q, Tsang TK, Peng Z, Wu P, Liu F, Fang VJ, Zhang H, Li M, Zeng L, Xu Z, Li Z, Luo H, Li Q, Feng Z, Cao B, Yang W, Wu JT, Wang Y, Leung GM: Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet. 2013, 382: 138-145. 10.1016/S0140-6736(13)61207-6.CrossRefPubMedPubMedCentral Yu H, Cowling BJ, Feng L, Lau EH, Liao Q, Tsang TK, Peng Z, Wu P, Liu F, Fang VJ, Zhang H, Li M, Zeng L, Xu Z, Li Z, Luo H, Li Q, Feng Z, Cao B, Yang W, Wu JT, Wang Y, Leung GM: Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet. 2013, 382: 138-145. 10.1016/S0140-6736(13)61207-6.CrossRefPubMedPubMedCentral
6.
go back to reference Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, Wu P, Zhou H, Lau EH, Guo D, Ni MY, Peng Z, Feng L, Jiang H, Luo H, Li Q, Feng Z, Wang Y, Yang W, Leung GM: Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet. 2014, 383: 541-548. 10.1016/S0140-6736(13)61904-2.CrossRefPubMed Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, Wu P, Zhou H, Lau EH, Guo D, Ni MY, Peng Z, Feng L, Jiang H, Luo H, Li Q, Feng Z, Wang Y, Yang W, Leung GM: Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet. 2014, 383: 541-548. 10.1016/S0140-6736(13)61904-2.CrossRefPubMed
7.
go back to reference Chen E, Chen Y, Fu L, Chen Z, Gong Z, Mao H, Wang D, Ni MY, Wu P, Yu Z, He T, Li Z, Gao J, Liu S, Shu Y, Cowling BJ, Xia S, Yu H: Human infection with avian influenza A(H7N9) virus re-emerges in China in winter 2013.Euro Surveill 2013, 18:20616.. Chen E, Chen Y, Fu L, Chen Z, Gong Z, Mao H, Wang D, Ni MY, Wu P, Yu Z, He T, Li Z, Gao J, Liu S, Shu Y, Cowling BJ, Xia S, Yu H: Human infection with avian influenza A(H7N9) virus re-emerges in China in winter 2013.Euro Surveill 2013, 18:20616..
8.
go back to reference Gabbard JD, Dlugolenski D, Van Riel D, Marshall N, Galloway SE, Howerth EW, Campbell PJ, Jones C, Johnson S, Byrd-Leotis L, Steinhauer DA, Kuiken T, Tompkins SM, Tripp R, Lowen AC, Steel J: Novel H7N9 influenza virus shows low infectious dose, high growth and efficient contact transmission in the guinea pig model. J Virol. 2014, 88: 1502-1512. 10.1128/JVI.02959-13.CrossRefPubMedPubMedCentral Gabbard JD, Dlugolenski D, Van Riel D, Marshall N, Galloway SE, Howerth EW, Campbell PJ, Jones C, Johnson S, Byrd-Leotis L, Steinhauer DA, Kuiken T, Tompkins SM, Tripp R, Lowen AC, Steel J: Novel H7N9 influenza virus shows low infectious dose, high growth and efficient contact transmission in the guinea pig model. J Virol. 2014, 88: 1502-1512. 10.1128/JVI.02959-13.CrossRefPubMedPubMedCentral
9.
go back to reference Ip DK, Liao Q, Wu P, Gao Z, Cao B, Feng L, Xu X, Jiang H, Li M, Bao J, Zheng J, Zhang Q, Chang Z, Li Y, Yu J, Liu F, Ni MY, Wu JT, Cowling BJ, Yang W, Leung GM, Yu H: Detection of mild to moderate influenza A/H7N9 infection by China’s national sentinel surveillance system for influenza-like illness: case series.BMJ 2013, 346:f3693.. Ip DK, Liao Q, Wu P, Gao Z, Cao B, Feng L, Xu X, Jiang H, Li M, Bao J, Zheng J, Zhang Q, Chang Z, Li Y, Yu J, Liu F, Ni MY, Wu JT, Cowling BJ, Yang W, Leung GM, Yu H: Detection of mild to moderate influenza A/H7N9 infection by China’s national sentinel surveillance system for influenza-like illness: case series.BMJ 2013, 346:f3693..
10.
go back to reference Li Q, Zhou L, Zhou M, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, Meng L, Hong Z, Tu W, Cao Y, Li L, Ding F, Liu B, Wang M, Xie R, Gao R, Li X, Bai T, Zou S, He J, Hu J, Xu Y, Chai C, Wang S, Gao Y, Jin L, Zhang Y, et al: Preliminary report: epidemiology of the avian influenza A (H7N9) outbreak in China. N Engl J Med. 2014, 370: 520-532. 10.1056/NEJMoa1304617.CrossRefPubMed Li Q, Zhou L, Zhou M, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, Meng L, Hong Z, Tu W, Cao Y, Li L, Ding F, Liu B, Wang M, Xie R, Gao R, Li X, Bai T, Zou S, He J, Hu J, Xu Y, Chai C, Wang S, Gao Y, Jin L, Zhang Y, et al: Preliminary report: epidemiology of the avian influenza A (H7N9) outbreak in China. N Engl J Med. 2014, 370: 520-532. 10.1056/NEJMoa1304617.CrossRefPubMed
11.
go back to reference Yu H, Huang J, Huai Y, Guan X, Klena J, Liu S, Peng Y, Yang H, Luo J, Zheng J, Chen M, Peng Z, Xiang N, Huo X, Xiao L, Jiang H, Chen H, Zhang Y, Xing X, Xu Z, Feng Z, Zhan F, Yang W, Uyeki TM, Wang Y, Varma JK: The substantial hospitalization burden of influenza in central China: surveillance for severe, acute respiratory infection, and influenza viruses, 2010-2012. Influenza Other Respir Viruses. 2014, 8: 53-65. 10.1111/irv.12205.CrossRefPubMed Yu H, Huang J, Huai Y, Guan X, Klena J, Liu S, Peng Y, Yang H, Luo J, Zheng J, Chen M, Peng Z, Xiang N, Huo X, Xiao L, Jiang H, Chen H, Zhang Y, Xing X, Xu Z, Feng Z, Zhan F, Yang W, Uyeki TM, Wang Y, Varma JK: The substantial hospitalization burden of influenza in central China: surveillance for severe, acute respiratory infection, and influenza viruses, 2010-2012. Influenza Other Respir Viruses. 2014, 8: 53-65. 10.1111/irv.12205.CrossRefPubMed
12.
go back to reference Fine MJ, Auble TE, Yealy DM, Hanusa BH, Weissfeld LA, Singer DE, Coley CM, Marrie TJ, Kapoor WN: A prediction rule to identify low-risk patients with community-acquired pneumonia. N Engl J Med. 1997, 336: 243-250. 10.1056/NEJM199701233360402.CrossRefPubMed Fine MJ, Auble TE, Yealy DM, Hanusa BH, Weissfeld LA, Singer DE, Coley CM, Marrie TJ, Kapoor WN: A prediction rule to identify low-risk patients with community-acquired pneumonia. N Engl J Med. 1997, 336: 243-250. 10.1056/NEJM199701233360402.CrossRefPubMed
13.
go back to reference Leung GM, Rainer TH, Lau FL, Wong IO, Tong A, Wong TW, Kong JH, Hedley AJ, Lam TH: A clinical prediction rule for diagnosing severe acute respiratory syndrome in the emergency department. Ann Intern Med. 2004, 141: 333-342. 10.7326/0003-4819-141-5-200409070-00106.CrossRefPubMed Leung GM, Rainer TH, Lau FL, Wong IO, Tong A, Wong TW, Kong JH, Hedley AJ, Lam TH: A clinical prediction rule for diagnosing severe acute respiratory syndrome in the emergency department. Ann Intern Med. 2004, 141: 333-342. 10.7326/0003-4819-141-5-200409070-00106.CrossRefPubMed
14.
go back to reference Schafer JL: Multiple imputation: a primer. Stat Methods Med Res. 1999, 8: 3-15. 10.1191/096228099671525676.CrossRefPubMed Schafer JL: Multiple imputation: a primer. Stat Methods Med Res. 1999, 8: 3-15. 10.1191/096228099671525676.CrossRefPubMed
15.
go back to reference Harrell FE: Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis. 2001, Springer Verlag, New YorkCrossRef Harrell FE: Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis. 2001, Springer Verlag, New YorkCrossRef
16.
go back to reference Little RJ, Rubin DB: Statistical Analysis with Missing Data. 2002, Wiley, Hoboken, NJCrossRef Little RJ, Rubin DB: Statistical Analysis with Missing Data. 2002, Wiley, Hoboken, NJCrossRef
17.
go back to reference Rubin DB: Multiple imputation after 18+ years. J Am Stat Assoc. 1996, 91: 473-489. 10.1080/01621459.1996.10476908.CrossRef Rubin DB: Multiple imputation after 18+ years. J Am Stat Assoc. 1996, 91: 473-489. 10.1080/01621459.1996.10476908.CrossRef
18.
go back to reference Sullivan LM, Massaro JM, D'Agostino RB: Presentation of multivariate data for clinical use: The Framingham Study risk score functions. Stat Med. 2004, 23: 1631-1660. 10.1002/sim.1742.CrossRefPubMed Sullivan LM, Massaro JM, D'Agostino RB: Presentation of multivariate data for clinical use: The Framingham Study risk score functions. Stat Med. 2004, 23: 1631-1660. 10.1002/sim.1742.CrossRefPubMed
19.
go back to reference Hanley JA, McNeil BJ: The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982, 143: 29-36. 10.1148/radiology.143.1.7063747.CrossRefPubMed Hanley JA, McNeil BJ: The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982, 143: 29-36. 10.1148/radiology.143.1.7063747.CrossRefPubMed
20.
21.
go back to reference Lee DS, Austin PC, Rouleau JL, Liu PP, Naimark D, Tu JV: Predicting mortality among patients hospitalized for heart failure: derivation and validation of a clinical model. JAMA. 2003, 290: 2581-2587. 10.1001/jama.290.19.2581.CrossRefPubMed Lee DS, Austin PC, Rouleau JL, Liu PP, Naimark D, Tu JV: Predicting mortality among patients hospitalized for heart failure: derivation and validation of a clinical model. JAMA. 2003, 290: 2581-2587. 10.1001/jama.290.19.2581.CrossRefPubMed
22.
go back to reference Efron B, Tibshirani RJ: An Introduction to the Bootstrap. Chapman & Hall/CRC Pr. 1998 Efron B, Tibshirani RJ: An Introduction to the Bootstrap. Chapman & Hall/CRC Pr. 1998
23.
go back to reference Harrell FE, Lee KL, Mark DB: Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996, 15: 361-387. 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4.CrossRefPubMed Harrell FE, Lee KL, Mark DB: Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996, 15: 361-387. 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4.CrossRefPubMed
24.
go back to reference Yu L, Wang Z, Chen Y, Ding W, Jia H, Chan JF, To KK, Chen H, Yang Y, Liang W, Zheng S, Yao H, Yang S, Cao H, Dai X, Zhao H, Li J, Bao Q, Chen P, Hou X, Li L, Yuen KY: Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A(H7N9) virus. Clin Infect Dis. 2013, 57: 1449-1457. 10.1093/cid/cit541.CrossRefPubMed Yu L, Wang Z, Chen Y, Ding W, Jia H, Chan JF, To KK, Chen H, Yang Y, Liang W, Zheng S, Yao H, Yang S, Cao H, Dai X, Zhao H, Li J, Bao Q, Chen P, Hou X, Li L, Yuen KY: Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A(H7N9) virus. Clin Infect Dis. 2013, 57: 1449-1457. 10.1093/cid/cit541.CrossRefPubMed
25.
go back to reference Qi X, Qian YH, Bao CJ, Guo XL, Cui LB, Tang FY, Ji H, Huang Y, Cai PQ, Lu B, Xu K, Shi C, Zhu FC, Zhou MH, Wang H: Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: epidemiological investigation.BMJ 2013, 347:f4752.. Qi X, Qian YH, Bao CJ, Guo XL, Cui LB, Tang FY, Ji H, Huang Y, Cai PQ, Lu B, Xu K, Shi C, Zhu FC, Zhou MH, Wang H: Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: epidemiological investigation.BMJ 2013, 347:f4752..
26.
go back to reference Bai T, Zhou J, Shu Y: Serologic study for influenza A (H7N9) among high-risk groups in China. N Engl J Med. 2013, 368: 2339-2340. 10.1056/NEJMc1305865.CrossRefPubMed Bai T, Zhou J, Shu Y: Serologic study for influenza A (H7N9) among high-risk groups in China. N Engl J Med. 2013, 368: 2339-2340. 10.1056/NEJMc1305865.CrossRefPubMed
Metadata
Title
A clinical prediction rule for diagnosing human infections with avian influenza A(H7N9) in a hospital emergency department setting
Authors
Qiaohong Liao
Dennis K M Ip
Tim K Tsang
Bin Cao
Hui Jiang
Fengfeng Liu
Jiandong Zheng
Zhibin Peng
Peng Wu
Yang Huai
Eric H Y Lau
Luzhao Feng
Gabriel M Leung
Hongjie Yu
Benjamin J Cowling
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2014
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-014-0127-0

Other articles of this Issue 1/2014

BMC Medicine 1/2014 Go to the issue