Prevalence of human coronaviruses in adults with acute respiratory tract infections in Beijing, China†
Lili Ren
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorRichard Gonzalez
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Fondation Mérieux, Lyon, France
Search for more papers by this authorJin Xu
Peking Union Medical College Hospital, CAMS, Beijing, China
Search for more papers by this authorYan Xiao
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorHongli Zhou
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorJianguo Li
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorQingqing Yang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorJing Zhang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorLan Chen
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorWei Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorCorresponding Author
Zhong Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Peking Union Medical College Hospital, CAMS, Beijing, China
Zhong Wang, 1# Shuai Fu Yuan, Dongcheng District, Beijing 100730, China.===
Jianwei Wang, 9# Dong Dan San Tiao, Dongcheng District, Beijing 100730, China.===
Search for more papers by this authorCorresponding Author
Jianwei Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Zhong Wang, 1# Shuai Fu Yuan, Dongcheng District, Beijing 100730, China.===
Jianwei Wang, 9# Dong Dan San Tiao, Dongcheng District, Beijing 100730, China.===
Search for more papers by this authorLili Ren
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorRichard Gonzalez
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Fondation Mérieux, Lyon, France
Search for more papers by this authorJin Xu
Peking Union Medical College Hospital, CAMS, Beijing, China
Search for more papers by this authorYan Xiao
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorHongli Zhou
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorJianguo Li
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorQingqing Yang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorJing Zhang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorLan Chen
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorWei Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Search for more papers by this authorCorresponding Author
Zhong Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Peking Union Medical College Hospital, CAMS, Beijing, China
Zhong Wang, 1# Shuai Fu Yuan, Dongcheng District, Beijing 100730, China.===
Jianwei Wang, 9# Dong Dan San Tiao, Dongcheng District, Beijing 100730, China.===
Search for more papers by this authorCorresponding Author
Jianwei Wang
State Key Laboratory for Molecular Virology and Genetic Engineering and Dr. Christophe Mérieux Laboratory, IPB, CAMS-Fondation Mérieux, Institute of Pathogen Biology (IPB), Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College, Beijing, China
Zhong Wang, 1# Shuai Fu Yuan, Dongcheng District, Beijing 100730, China.===
Jianwei Wang, 9# Dong Dan San Tiao, Dongcheng District, Beijing 100730, China.===
Search for more papers by this authorThe authors report no conflicts of interest in the publication of this article.
Abstract
Human coronaviruses (HCoVs) are a common etiological agent of acute respiratory tract infections. HCoV infections, especially those caused by the two HCoVs identified most recently, NL63 and HKU-1, have not been characterized fully. To evaluate the prevalence and clinical presentations of HKU1 and NL63 in adults with acute respiratory tract infections, an investigation of HCoV infections in Beijing, China from 2005 to 2009 was performed by using reverse transcriptase PCR assays and sequencing analysis. Among 8,396 respiratory specimens studied, 87 (1%) clinical samples were positive for HCoVs, of which 50 samples (0.6% of the total) were positive for HCoV-OC43, 15 (0.2%) for HCoV-229E, 14 (0.2%) for HCoV-HKU1, and 8 (0.1%) for HCoV-NL63. The prevalence of HCoV infection in adults exhibited distinct seasonal fluctuations during the study period. In addition, patients positive for HCoV-229E infections were more likely to be co-infected with other respiratory viruses. Enterovirus, rhinovirus, and parainfluenza virus type 3 were the most common viruses found in patients with HCoV infections. The demographic and clinical data present in this study of HCoV infections in adults with acute respiratory tract infections should improve our understanding of the pathogenesis of HCoVs. J. Med. Virol. 83:291–297, 2011. © 2010 Wiley-Liss, Inc.
REFERENCES
- Bastien N, Anderson K, Hart L, Van Caeseele P, Brandt K, Milley D, Hatchette T, Weiss EC, Li Y. 2005. Human coronavirus NL63 infection in Canada. J Infect Dis 15: 503–506.
- Bellei N, Carraro E, Perosa A, Watanabe A, Arruda E, Granato C. 2008. Acute respiratory infection and influenza-like illness viral etiologies in Brazilian adults. J Med Virol 80: 1824–1827.
- Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J. 1990. Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28: 495–503.
- Chan CM, Tse H, Wong SS, Woo PC, Lau SK, Chen L, Zheng BJ, Huang JD, Yuen KY. 2009. Examination of seroprevalence of coronavirus HKU1 infection with S protein-based ELISA and neutralization assay against viral spike pseudotyped virus. J Clin Virol 45: 54–60.
- Dijkman R, Jebbink MF, El Idrissi NB, Pyrc K, Müller MA, Kuijpers TW, Zaaijer HL, van der Hoek L. 2008. Human coronavirus NL63 and 229E seroconversion in children. J Clin Microbiol 46: 2368–2373.
- Drosten C, Günther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguière AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Müller S, Rickerts V, Stürmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348: 1967–1976.
- Esper F, Weibel C, Ferguson D, Landry ML, Kahn JS. 2005. Evidence of a novel human coronavirus that is associated with respiratory tract disease in infants and young children. J Infect Dis 191: 492–498.
- Fouchier RA, Hartwig NG, Bestebroer TM, Niemeyer B, de Jong JC, Simon JH, Osterhaus AD. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc Natl Acad Sci USA 101: 6212–6216.
- Gerna G, Campanini G, Rovida F, Percivalle E, Sarasini A, Marchi A, Baldanti F. 2006. 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 78: 938–949.
- Gibbs AJ, Gibbs MJ, Armstrong JS. 2004. The phylogeny of SARS coronavirus. Arch Virol 149: 621–624.
- Gorse GJ, O'Connor TZ, Hall SL, Vitale JN, Nichol KL. 2009. Human coronavirus and acute respiratory illness in older adults with chronic obstructive pulmonary disease. J Infect Dis 199: 847–857.
- Hamre D, Procknow JJ. 1966. A new virus isolated from the human respiratory tract. Proc Soc Exp Biol Med 121: 190–193.
- Holmes KV. 2001. Coronavirus. In: DM Knipe MD Howley editors. Fields virology Philadelphia, PA: Lippincott Williams and Wilkins. pp. 1187–1204.
- Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, Lim W, Ling AE, Chan PK, Tam JS, Zambon MC, Gopal R, Drosten C, van der Werf S, Escriou N, Manuguerra JC, Stöhr K, Peiris JS, Osterhaus AD. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362: 263–270.
- Lai MM, Cavanagh D. 1997. The molecular biology of coronaviruses. Adv Virus Res 48: 1–100.
- Lambert SB, Whiley DM, O'Neill NT, Andrews EC, Canavan FM, Bletchly C, Siebert DJ, Sloots TP, Nissen MD. 2008. Comparing nose–throat swabs and nasopharyngeal aspirates collected from children with symptoms for respiratory virus identification using real-time polymerase chain reaction. Pediatrics 122: e615–e620.
- Lau SK, Woo PC, Yip CC, Tse H, Tsoi HW, Cheng VC, Lee P, Tang BS, Cheung CH, Lee RA, So LY, Lau YL, Chan KH, Yuen KY. 2006. Coronavirus HKU1 and other coronavirus infections in Hong Kong. J Clin Microbiol 44: 2063–2071.
- Leung TF, Li CY, Lam WY, Wong GW, Cheuk E, Ip M, Ng PC, Chan PK. 2009. Epidemiology and clinical presentations of human coronavirus NL63 in Hong Kong children. J Clin Microbiol 47: 3486–3492.
- McIntosh K, Dees JH, Becker WB, Kapikian AZ, Chanock RM. 1967. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc Natl Acad Sci USA 57: 933–940.
- McIntosh K, Kapikian AZ, Turner HC, Hartley JW, Parrott RH, Chanock RM. 1970. Seroepidemiologic studies of coronavirus infection in adults and children. Am J Epidemiol 91: 585–592.
- Meerhoff TJ, Houben ML, Coenjaerts FE, Kimpen JL, Hofland RW, Schellevis F, Bont LJ. 2010. Detection of multiple respiratory pathogens during primary respiratory infection: Nasal swab versus nasopharyngeal aspirate using real-time polymerase chain reaction. Eur J Clin Microbiol Infect Dis 29: 365–371.
- Monto AS, Lim SK. The Tecumseh study of respiratory illness. VI. 1974.Frequency of and relationship between outbreaks of coronavirus infection. J Infect Dis 129: 271–276.
- Perlman S, Netland J. 2009. Coronaviruses post-SARS: Update on replication and pathogenesis. Nat Rev Microbiol 7: 439–450.
- Pierangeli A, Gentile M, Di Marco P, Pagnotti P, Scagnolari C, Trombetti S, Lo Russo L, Tromba V, Moretti C, Midulla F, Antonelli G. 2007. Detection and typing by molecular techniques of respiratory viruses in children hospitalized for acute respiratory infection in Rome, Italy. J Med Virol 79: 463–468.
- Ren L, Gonzalez R, Wang Z, Xiang Z, Wang Y, Zhou H, Li J, Xiao Y, Yang Q, Zhang J, Chen L, Wang W, Li Y, Li T, Meng X, Zhang Y, Vernet G, Paranhos-Baccalà G, Chen J, Jin Q, Wang J. 2009. Prevalence of human respiratory viruses in adults with acute respiratory tract infections in Beijing, 2005–2007. Clin Microbiol Infect 15: 1146–1153.
- Shao X, Guo X, Esper F, Weibel C, Kahn JS. 2007. Seroepidemiology of group I human coronaviruses in children. J Clin Virol 40: 207–213.
- Tamura K, Dudley J, Nei M, Kumar S. 2007. MEG A4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
- Tyrrell DA, Bynoe ML. 1965. Cultivation of a novel type of common cold virus in organ cultures. Br Med J 1: 1467–1470.
- van der Hoek L. 2007. Human coronaviruses: What do they cause? Antivirol Ther 12: 651–658.
- van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B. 2004. Identification of a new human coronavirus. Nat Med 10: 368–373.
- Varkey JB, Varkey B. 2008. Viral infections in patients with chronic obstructive pulmonary disease. Curr Opin Pulm Med 14: 89–94.
- Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol 79: 884–895.
- Woo PC, Lau SK, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med (Maywood) 234: 1117–1127.