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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Possible interference between seasonal epidemics of influenza and other respiratory viruses in Hong Kong, 2014–2017

Authors: Xueying Zheng, Zhengyu Song, Yapeng Li, Juanjuan Zhang, Xi-Ling Wang

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

Unlike influenza viruses, little is known about the prevalence and seasonality of other respiratory viruses because laboratory surveillance for non-influenza respiratory viruses is not well developed or supported in China and other resource-limited countries. We studied the interference between seasonal epidemics of influenza viruses and five other common viruses that cause respiratory illnesses in Hong Kong from 2014 to 2017.

Methods

The weekly laboratory-confirmed positive rates of each virus were analyzed from 2014 to 2017 in Hong Kong to describe the epidemiological trends and interference between influenza viruses, respiratory syncytial virus (RSV), parainfluenza virus (PIV), adenovirus, enterovirus and rhinovirus. A sinusoidal model was established to estimate the peak timing of each virus by phase angle parameters.

Results

Seasonal features of the influenza viruses, PIV, enterovirus and adenovirus were obvious, whereas annual peaks of RSV and rhinovirus were not observed. The incidence of the influenza viruses usually peaked in February and July, and the summer peaks in July were generally caused by the H3 subtype of influenza A alone. When influenza viruses were active, other viruses tended to have a low level of activity. The peaks of the influenza viruses were not synchronized. An epidemic of rhinovirus tended to shift the subsequent epidemics of the other viruses.

Conclusion

The evidence from recent surveillance data in Hong Kong suggests that viral interference during the epidemics of influenza viruses and other common respiratory viruses might affect the timing and duration of subsequent epidemics of a certain or several viruses.
Literature
1.
go back to reference Nair H, Brooks WA, Katz M, Roca A, Berkley JA, Madhi SA, Simmerman JM, Gordon A, Sato M, Howie S, et al. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet. 2011;378(9807):1917–30.CrossRefPubMed Nair H, Brooks WA, Katz M, Roca A, Berkley JA, Madhi SA, Simmerman JM, Gordon A, Sato M, Howie S, et al. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet. 2011;378(9807):1917–30.CrossRefPubMed
2.
go back to reference Guo RN, Zheng HZ, Li JS, Sun LM, Li LH, Lin JY, He JF. A population-based study on incidence and economic burden of influenza-like illness in south China, 2007. Public Health. 2011;125(6):389.CrossRefPubMed Guo RN, Zheng HZ, Li JS, Sun LM, Li LH, Lin JY, He JF. A population-based study on incidence and economic burden of influenza-like illness in south China, 2007. Public Health. 2011;125(6):389.CrossRefPubMed
3.
go back to reference Tang JW, Lam TT, Zaraket H, Lipkin WI, Drews SJ, Hatchette TF, Heraud JM, Koopmans MP. Investigators I: global epidemiology of non-influenza RNA respiratory viruses: data gaps and a growing need for surveillance. Lancet Infect Dis. 2017; Tang JW, Lam TT, Zaraket H, Lipkin WI, Drews SJ, Hatchette TF, Heraud JM, Koopmans MP. Investigators I: global epidemiology of non-influenza RNA respiratory viruses: data gaps and a growing need for surveillance. Lancet Infect Dis. 2017;
4.
go back to reference Goka E, Vallely P, Mutton K, Klapper P, Influenza A. Viruses dual and multiple infections with other respiratory viruses and risk of hospitalisation and mortality. Influenza Other Respir Viruses. 2013;7(6):1079–87.CrossRefPubMed Goka E, Vallely P, Mutton K, Klapper P, Influenza A. Viruses dual and multiple infections with other respiratory viruses and risk of hospitalisation and mortality. Influenza Other Respir Viruses. 2013;7(6):1079–87.CrossRefPubMed
5.
go back to reference Galindo-Fraga A, Ortiz-Hernandez AA, Ramirez-Venegas A, Vazquez RV, Moreno-Espinosa S, Llamosas-Gallardo B, Perez-Patrigeon S, Salinger M, Freimanis L, Huang CY, et al. Clinical characteristics and outcomes of influenza and other influenza-like illnesses in Mexico City. Int J Infect Dis. 2013;17(7):e510–7.CrossRefPubMedPubMedCentral Galindo-Fraga A, Ortiz-Hernandez AA, Ramirez-Venegas A, Vazquez RV, Moreno-Espinosa S, Llamosas-Gallardo B, Perez-Patrigeon S, Salinger M, Freimanis L, Huang CY, et al. Clinical characteristics and outcomes of influenza and other influenza-like illnesses in Mexico City. Int J Infect Dis. 2013;17(7):e510–7.CrossRefPubMedPubMedCentral
6.
go back to reference Influenza Fact sheet no.211. In.: World Health Organization. Influenza Fact sheet no.211. In.: World Health Organization.
7.
go back to reference Huo X, Qin Y, Qi X, Zu R, Tang F, Li L, Hu Z, Zhu F. Surveillance of 16 respiratory viruses in patients with influenza-like illness in Nanjing, China. J Med Virol. 2012;84(12):1980–4.CrossRefPubMed Huo X, Qin Y, Qi X, Zu R, Tang F, Li L, Hu Z, Zhu F. Surveillance of 16 respiratory viruses in patients with influenza-like illness in Nanjing, China. J Med Virol. 2012;84(12):1980–4.CrossRefPubMed
8.
go back to reference Monto AS. The seasonality of rhinovirus infections and its implications for clinical recognition. Clin Ther. 2002;24(12):1987–97.CrossRefPubMed Monto AS. The seasonality of rhinovirus infections and its implications for clinical recognition. Clin Ther. 2002;24(12):1987–97.CrossRefPubMed
9.
go back to reference Landes MB, Neil RB, McCool SS, Mason BP, Woron AM, Garman RL, Smalley DL. The frequency and seasonality of influenza and other respiratory viruses in Tennessee: two influenza seasons of surveillance data, 2010-2012. Influenza Other Respir Viruses. 2013;7(6):1122–7.CrossRefPubMedPubMedCentral Landes MB, Neil RB, McCool SS, Mason BP, Woron AM, Garman RL, Smalley DL. The frequency and seasonality of influenza and other respiratory viruses in Tennessee: two influenza seasons of surveillance data, 2010-2012. Influenza Other Respir Viruses. 2013;7(6):1122–7.CrossRefPubMedPubMedCentral
10.
go back to reference Linde A, Rotzén-Ostlund M, Zweygberg-Wirgart B, Rubinova S, Brytting M. Does viral interference affect spread of influenza? Euro Surveill. 2009;14:331–43. Linde A, Rotzén-Ostlund M, Zweygberg-Wirgart B, Rubinova S, Brytting M. Does viral interference affect spread of influenza? Euro Surveill. 2009;14:331–43.
11.
go back to reference Meningher T, Hindiyeh M, Regev L, Sherbany H, Mendelson E, Mandelboim M. Relationships between a(H1N1)pdm09 influenza infection and infections with other respiratory viruses. Influenza Other Respir Viruses. 2014;8(4):422–30.CrossRefPubMedPubMedCentral Meningher T, Hindiyeh M, Regev L, Sherbany H, Mendelson E, Mandelboim M. Relationships between a(H1N1)pdm09 influenza infection and infections with other respiratory viruses. Influenza Other Respir Viruses. 2014;8(4):422–30.CrossRefPubMedPubMedCentral
12.
go back to reference van Asten L, Bijkerk P, Fanoy E, van Ginkel A, Suijkerbuijk A, van der Hoek W, Meijer A, Vennema H. Early occurrence of influenza a epidemics coincided with changes in occurrence of other respiratory virus infections. Influenza Other Respir Viruses. 2016;10(1):14–26.CrossRefPubMed van Asten L, Bijkerk P, Fanoy E, van Ginkel A, Suijkerbuijk A, van der Hoek W, Meijer A, Vennema H. Early occurrence of influenza a epidemics coincided with changes in occurrence of other respiratory virus infections. Influenza Other Respir Viruses. 2016;10(1):14–26.CrossRefPubMed
14.
go back to reference Anestad G, Nordbo SA. Interference between outbreaks of respiratory viruses. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2009;14:19359. Anestad G, Nordbo SA. Interference between outbreaks of respiratory viruses. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2009;14:19359.
15.
go back to reference Wu P, Goldstein E, Ho LM, Yang L, Nishiura H, Wu JT, Ip DK, Chuang SK, Tsang T, Cowling BJ. Excess mortality associated with influenza a and B virus in Hong Kong, 1998-2009. J Infect Dis. 2012;206(12):1862–71.CrossRefPubMedPubMedCentral Wu P, Goldstein E, Ho LM, Yang L, Nishiura H, Wu JT, Ip DK, Chuang SK, Tsang T, Cowling BJ. Excess mortality associated with influenza a and B virus in Hong Kong, 1998-2009. J Infect Dis. 2012;206(12):1862–71.CrossRefPubMedPubMedCentral
16.
go back to reference Mak GC, Wong AH, Ho WY, Lim W. The impact of pandemic influenza a (H1N1) 2009 on the circulation of respiratory viruses 2009-2011. Influenza Other Respir Viruses. 2012;6(3):e6–10.CrossRefPubMedPubMedCentral Mak GC, Wong AH, Ho WY, Lim W. The impact of pandemic influenza a (H1N1) 2009 on the circulation of respiratory viruses 2009-2011. Influenza Other Respir Viruses. 2012;6(3):e6–10.CrossRefPubMedPubMedCentral
17.
go back to reference Cowling BJ, Wong IO, Ho LM, Riley S, Leung GM. Methods for monitoring influenza surveillance data. Int J Epidemiol. 2006;35(5):1314–21.CrossRefPubMed Cowling BJ, Wong IO, Ho LM, Riley S, Leung GM. Methods for monitoring influenza surveillance data. Int J Epidemiol. 2006;35(5):1314–21.CrossRefPubMed
18.
go back to reference Census and Statistics Department. Thematic household survey report number 12. Hong Kong: Census and Statistics Department; 2003. Census and Statistics Department. Thematic household survey report number 12. Hong Kong: Census and Statistics Department; 2003.
19.
go back to reference Yang L, Wong CM, Lau EHY, Chan KP, CQ O, Peiris JSM. Synchrony of clinical and laboratory surveillance for influenza in Hong Kong. PLoS One. 2008;3(1):e1399.CrossRefPubMedPubMedCentral Yang L, Wong CM, Lau EHY, Chan KP, CQ O, Peiris JSM. Synchrony of clinical and laboratory surveillance for influenza in Hong Kong. PLoS One. 2008;3(1):e1399.CrossRefPubMedPubMedCentral
21.
go back to reference Rogers DJ, Hay SI, Packer MJ. Predicting the distribution of tsetse flies in West Africa using temporal Fourier processed meteorological satellite data. Ann Trop Med Parasitol. 1996;90(3):225–41.CrossRefPubMed Rogers DJ, Hay SI, Packer MJ. Predicting the distribution of tsetse flies in West Africa using temporal Fourier processed meteorological satellite data. Ann Trop Med Parasitol. 1996;90(3):225–41.CrossRefPubMed
22.
go back to reference Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect. 2007;135(2):281–92.CrossRefPubMed Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect. 2007;135(2):281–92.CrossRefPubMed
23.
go back to reference Zou J, Yang H, Cui H, Shu Y, Xu P, Xu C, Chen T. Geographic divisions and modeling of virological data on seasonal influenza in the Chinese mainland during the 2006-2009 monitoring years. PLoS One. 2013;8(3):e58434.CrossRefPubMedPubMedCentral Zou J, Yang H, Cui H, Shu Y, Xu P, Xu C, Chen T. Geographic divisions and modeling of virological data on seasonal influenza in the Chinese mainland during the 2006-2009 monitoring years. PLoS One. 2013;8(3):e58434.CrossRefPubMedPubMedCentral
24.
go back to reference Yu H, Alonso WJ, Feng L, Tan Y, Shu Y, Yang W, Viboud C. Characterization of regional influenza seasonality patterns in China and implications for vaccination strategies: spatio-temporal modeling of surveillance data. PLoS Med. 2013;10(11):e1001552.CrossRefPubMedPubMedCentral Yu H, Alonso WJ, Feng L, Tan Y, Shu Y, Yang W, Viboud C. Characterization of regional influenza seasonality patterns in China and implications for vaccination strategies: spatio-temporal modeling of surveillance data. PLoS Med. 2013;10(11):e1001552.CrossRefPubMedPubMedCentral
25.
go back to reference Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, Miller MA. Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol. 2007;165(12):1434–42.CrossRefPubMed Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, Miller MA. Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol. 2007;165(12):1434–42.CrossRefPubMed
26.
go back to reference Ooi MH, Solomon T, Podin Y, Mohan A, Akin W, Yusuf MA, Del SS, Kontol KM, Lai BF, Clear D. Evaluation of different clinical sample types in diagnosis of human enterovirus 71-associated hand-foot-and-mouth disease. J Clin Microbiol. 2007;45(6):1858.CrossRefPubMedPubMedCentral Ooi MH, Solomon T, Podin Y, Mohan A, Akin W, Yusuf MA, Del SS, Kontol KM, Lai BF, Clear D. Evaluation of different clinical sample types in diagnosis of human enterovirus 71-associated hand-foot-and-mouth disease. J Clin Microbiol. 2007;45(6):1858.CrossRefPubMedPubMedCentral
27.
go back to reference Garcia J, Espejo V, Nelson M, Sovero M, Villaran MV, Gomez J, Barrantes M, Sanchez F, Comach G, Arango AE: Human rhinoviruses and enteroviruses in influenza-like illness in Latin America. Virol J 2013, 10(1):305–305. Garcia J, Espejo V, Nelson M, Sovero M, Villaran MV, Gomez J, Barrantes M, Sanchez F, Comach G, Arango AE: Human rhinoviruses and enteroviruses in influenza-like illness in Latin America. Virol J 2013, 10(1):305–305.
28.
go back to reference Fisman D. Seasonality of viral infections: mechanisms and unknowns. Clin Microbiol Infect. 2012;18(10):946–54.CrossRefPubMed Fisman D. Seasonality of viral infections: mechanisms and unknowns. Clin Microbiol Infect. 2012;18(10):946–54.CrossRefPubMed
29.
go back to reference Caini S, Andrade W, Badur S, Balmaseda A, Barakat A, Bella A, Bimohuen A, Brammer L, Bresee J, Bruno A, et al. Temporal patterns of influenza a and B in tropical and temperate countries: what are the lessons for influenza vaccination? PLoS One. 2016;11(3):e0152310.CrossRefPubMedPubMedCentral Caini S, Andrade W, Badur S, Balmaseda A, Barakat A, Bella A, Bimohuen A, Brammer L, Bresee J, Bruno A, et al. Temporal patterns of influenza a and B in tropical and temperate countries: what are the lessons for influenza vaccination? PLoS One. 2016;11(3):e0152310.CrossRefPubMedPubMedCentral
30.
go back to reference Moa AM, Muscatello DJ, Turner RM, MacIntyre CR. Epidemiology of influenza B in Australia: 2001-2014 influenza seasons. Influenza Other Respir Viruses. 2017;11(2):102–9.CrossRefPubMed Moa AM, Muscatello DJ, Turner RM, MacIntyre CR. Epidemiology of influenza B in Australia: 2001-2014 influenza seasons. Influenza Other Respir Viruses. 2017;11(2):102–9.CrossRefPubMed
31.
go back to reference DaPalma T, Doonan BP, Trager NM, Kasman LM. A systematic approach to virus-virus interactions. Virus Res. 2010;149(1):1–9.CrossRefPubMed DaPalma T, Doonan BP, Trager NM, Kasman LM. A systematic approach to virus-virus interactions. Virus Res. 2010;149(1):1–9.CrossRefPubMed
32.
go back to reference Greer RM, McErlean P, Arden KE, Faux CE, Nitsche A, Lambert SB, Nissen MD, Sloots TP, Mackay IM. Do rhinoviruses reduce the probability of viral co-detection during acute respiratory tract infections? J Clin Virol. 2009;45(1):10–5.CrossRefPubMed Greer RM, McErlean P, Arden KE, Faux CE, Nitsche A, Lambert SB, Nissen MD, Sloots TP, Mackay IM. Do rhinoviruses reduce the probability of viral co-detection during acute respiratory tract infections? J Clin Virol. 2009;45(1):10–5.CrossRefPubMed
33.
go back to reference Casalegno JS, Ottmann M, Duchamp MB, Escuret V, Billaud G, Frobert E, Morfin F, Lina B. Rhinoviruses delayed the circulation of the pandemic influenza a (H1N1) 2009 virus in France. Clin Microbiol Infect. 2010;16(4):326–9.CrossRefPubMed Casalegno JS, Ottmann M, Duchamp MB, Escuret V, Billaud G, Frobert E, Morfin F, Lina B. Rhinoviruses delayed the circulation of the pandemic influenza a (H1N1) 2009 virus in France. Clin Microbiol Infect. 2010;16(4):326–9.CrossRefPubMed
Metadata
Title
Possible interference between seasonal epidemics of influenza and other respiratory viruses in Hong Kong, 2014–2017
Authors
Xueying Zheng
Zhengyu Song
Yapeng Li
Juanjuan Zhang
Xi-Ling Wang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2888-5

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