Skip to main content
Top
Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Influenza Virus | Research article

Surveillance and characterisation of influenza viruses among patients with influenza-like illness in Bali, Indonesia, July 2010–June 2014

Authors: Wiku Adisasmito, Sri Budayanti, Dewi Nur Aisyah, Richard Coker, Ayu Rai Andayani, Gavin J. D. Smith, James W. Rudge

Published in: BMC Infectious Diseases | Issue 1/2019

Login to get access

Abstract

Background

Although Indonesia has high fatality rate of human A/H5N1 cases, epidemiological and clinical data on influenza virus circulation among humans has been limited. Within Indonesia, Bali province is of interest due to high population densities of humans, pigs and poultry. This study aims to characterize and compare the epidemiological and clinical patterns of influenza viruses in humans through surveillance among patients with influenza-like illness (ILI) in Bali, Indonesia.

Methods

ILI patients were recruited at 21 sentinel health facilities across all nine regencies in Bali, from July 2010 to June 2014. PCR-based assays were used for detection and subtyping of influenza viruses. Demographic, behavioural and clinical data were tested for associations with influenza using chi-squared tests and logistic regression.

Results

Of 2077 ILI patients, 291 (14.0%) tested positive for influenza A, 152 (7.3%) for influenza B, and 16 (0.77%) for both influenza A and B. Of the influenza A isolates, the majority 61.2% were A/H3N2, followed by A/H1N1-pdm09 (80; 26.1%). Two A/H5N1 were identified. Influenza positive rates were significantly higher during wet season months (28.3%), compared with the dry season (13.8%; χ2 = 61.1; df = 1; p < 0.0001). Clinical predictors for infection varied by virus type, with measured fever (≥38 °C) more strongly associated with influenza B (AOR: 1.62; 95% CI: 1.10, 2.39).

Conclusion

Influenza circulates year-round among humans in Bali with higher activity during the wet season. High contact rates with poultry and pigs, along with influenza virus detection that could not be subtyped through conventional assays, highlight the need for molecular studies to characterize epidemiological and evolutionary dynamics of influenza in this setting.
Appendix
Available only for authorised users
Literature
1.
go back to reference Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC. The global circulation of seasonal influenza a (H3N2) viruses. Science. 2008;320(5874):340–6.CrossRef Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC. The global circulation of seasonal influenza a (H3N2) viruses. Science. 2008;320(5874):340–6.CrossRef
2.
go back to reference Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–3.CrossRef Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–3.CrossRef
3.
go back to reference FAO Emergency Centre for Transboundary Animal Diseases (ECTAD): FAO Animal Influenza Disease Emergency news: Situation Update 66 15 May 2010. In: Health (San Francisco). FAO ECTAD; 2010: 1–20. FAO Emergency Centre for Transboundary Animal Diseases (ECTAD): FAO Animal Influenza Disease Emergency news: Situation Update 66 15 May 2010. In: Health (San Francisco). FAO ECTAD; 2010: 1–20.
7.
go back to reference Cyranoski D. Bird flu spreads among Java's pigs. Nature. 2005;435(7041):390–1.CrossRef Cyranoski D. Bird flu spreads among Java's pigs. Nature. 2005;435(7041):390–1.CrossRef
8.
go back to reference Takano R, Nidom CA, Kiso M, Muramoto Y, Yamada S, Shinya K, Sakai-Tagawa Y, Kawaoka Y. A comparison of the pathogenicity of avian and swine H5N1 influenza viruses in Indonesia. Arch Virol. 2009;154(4):677–81.CrossRef Takano R, Nidom CA, Kiso M, Muramoto Y, Yamada S, Shinya K, Sakai-Tagawa Y, Kawaoka Y. A comparison of the pathogenicity of avian and swine H5N1 influenza viruses in Indonesia. Arch Virol. 2009;154(4):677–81.CrossRef
9.
go back to reference Nidom Ca: Influenza a (H5N1) viruses from pigs, Indonesia. Emerg Infect Dis 2010, 16(10):1515–1523. Nidom Ca: Influenza a (H5N1) viruses from pigs, Indonesia. Emerg Infect Dis 2010, 16(10):1515–1523.
10.
go back to reference Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, et al. Molecular basis for the generation in pigs of influenza a viruses with pandemic potential. J Virol. 1998;72(9):7367–73.PubMedPubMedCentral Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, et al. Molecular basis for the generation in pigs of influenza a viruses with pandemic potential. J Virol. 1998;72(9):7367–73.PubMedPubMedCentral
11.
go back to reference Simmons P. Perspectives on the 2003 and 2004 avian influenza outbreak in Bali and Lombok. Agribusiness. 2006;22(4):435–50.CrossRef Simmons P. Perspectives on the 2003 and 2004 avian influenza outbreak in Bali and Lombok. Agribusiness. 2006;22(4):435–50.CrossRef
12.
go back to reference Santhia K, Ramy A, Jayaningsih P, Samaan G, Putra AAG, Dibia N, Sulaimin C, Joni G, Leung CY, Malik Peiris JS. Avian influenza a H5N1 infections in Bali Province, Indonesia: a behavioral, virological and seroepidemiological study. Influenza Other Respir Viruses. 2009;3(3):81–9.CrossRef Santhia K, Ramy A, Jayaningsih P, Samaan G, Putra AAG, Dibia N, Sulaimin C, Joni G, Leung CY, Malik Peiris JS. Avian influenza a H5N1 infections in Bali Province, Indonesia: a behavioral, virological and seroepidemiological study. Influenza Other Respir Viruses. 2009;3(3):81–9.CrossRef
13.
go back to reference Siagiaan PH: Pig production in Indonesia. Proceedings of the Recent Progress in Swine Breeding and Raising Technologies, Tainan, Taiwan 2014. Siagiaan PH: Pig production in Indonesia. Proceedings of the Recent Progress in Swine Breeding and Raising Technologies, Tainan, Taiwan 2014.
15.
go back to reference World Health Organization: WHO global technical consultation: global standards and tools for influenza surveillance. In. Geneva, Switzerland: WHO; 2011: 45. World Health Organization: WHO global technical consultation: global standards and tools for influenza surveillance. In. Geneva, Switzerland: WHO; 2011: 45.
17.
go back to reference Zaman RU, Alamgir A, Rahman M, Azziz-Baumgartner E, Gurley ES, Sharker M, Brooks WA, Azim T, Fry AM, Lindstrom S: Influenza in outpatient ILI case-patients in national hospital-based surveillance, Bangladesh, 2007–2008. PLoS One 2009, 4(12):e8452-e8452. Zaman RU, Alamgir A, Rahman M, Azziz-Baumgartner E, Gurley ES, Sharker M, Brooks WA, Azim T, Fry AM, Lindstrom S: Influenza in outpatient ILI case-patients in national hospital-based surveillance, Bangladesh, 2007–2008. PLoS One 2009, 4(12):e8452-e8452.
18.
go back to reference Navarro-Marí JM, Pérez-Ruiz M, Cantudo-Muñoz P, Petit-Gancedo C, Jiménez-Valera M, Rosa-Fraile M, in Andalusia ISN: Influenza-like illness criteria were poorly related to laboratory-confirmed influenza in a sentinel surveillance study. J Clin Epidemiol 2005, 58(3):275–279. Navarro-Marí JM, Pérez-Ruiz M, Cantudo-Muñoz P, Petit-Gancedo C, Jiménez-Valera M, Rosa-Fraile M, in Andalusia ISN: Influenza-like illness criteria were poorly related to laboratory-confirmed influenza in a sentinel surveillance study. J Clin Epidemiol 2005, 58(3):275–279.
19.
go back to reference Yang L, Wong CM, Lau EH, Chan KP, Ou CQ, Peiris JS: Synchrony of clinical and laboratory surveillance for influenza in Hong Kong 2008. Yang L, Wong CM, Lau EH, Chan KP, Ou CQ, Peiris JS: Synchrony of clinical and laboratory surveillance for influenza in Hong Kong 2008.
20.
go back to reference Prachayangprecha S, Vichaiwattana P, Korkong S, Felber JA, Poovorawan Y: Influenza activity in Thailand and occurrence in different climates. SpringerPlus 2015, 4(1):1. Prachayangprecha S, Vichaiwattana P, Korkong S, Felber JA, Poovorawan Y: Influenza activity in Thailand and occurrence in different climates. SpringerPlus 2015, 4(1):1.
21.
go back to reference Azziz-Baumgartner E, Alamgir AS, Rahman M, Homaira N, Sohel BM, Sharker MA, Zaman RU, Dee J, Gurley ES, Al Mamun A et al: Incidence of influenza-like illness and severe acute respiratory infection during three influenza seasons in Bangladesh, 2008-2010. Bull World Health Organ 2012, 90(1):12–19. Azziz-Baumgartner E, Alamgir AS, Rahman M, Homaira N, Sohel BM, Sharker MA, Zaman RU, Dee J, Gurley ES, Al Mamun A et al: Incidence of influenza-like illness and severe acute respiratory infection during three influenza seasons in Bangladesh, 2008-2010. Bull World Health Organ 2012, 90(1):12–19.
22.
go back to reference Nguyen DNT, Bryant JE, Hang NLK, Nadjm B, Thai PQ, Duong TN, Anh DD, Horby P, van Doorn HR, Wertheim HF. Epidemiology and etiology of influenza-like-illness in households in Vietnam; it’s not all about the kids! J Clin Virol. 2016;82:126–32.CrossRef Nguyen DNT, Bryant JE, Hang NLK, Nadjm B, Thai PQ, Duong TN, Anh DD, Horby P, van Doorn HR, Wertheim HF. Epidemiology and etiology of influenza-like-illness in households in Vietnam; it’s not all about the kids! J Clin Virol. 2016;82:126–32.CrossRef
23.
go back to reference Setiawaty V: Surveilans Virologi Influenza Like Illness di Empat Provinsi di Indonesia. In. Jakarta: Pusat Biomedis dan Teknologi Dasar Kesehatan, Badan Litbang Kesehatan; 2011. Setiawaty V: Surveilans Virologi Influenza Like Illness di Empat Provinsi di Indonesia. In. Jakarta: Pusat Biomedis dan Teknologi Dasar Kesehatan, Badan Litbang Kesehatan; 2011.
24.
go back to reference Puspa KD, Pangesti KNA, Setiawaty V: Effects of climate change on the distribution of influenza virus in Indonesia in 2012-2013. Health Science Journal of Indonesia 2014, 5(2 Dec):78–82. Puspa KD, Pangesti KNA, Setiawaty V: Effects of climate change on the distribution of influenza virus in Indonesia in 2012-2013. Health Science Journal of Indonesia 2014, 5(2 Dec):78–82.
25.
go back to reference Setiawaty V, Pangesti KNA, Pawesti HA, Agustiningsih: Karakterisasi Virus Influenza dari Pemantauan Berkala Kasus Influenza Like Illness (ILI) di Indonesia. In. Jakarta: National Institute of Health Research and Development; 2014. Setiawaty V, Pangesti KNA, Pawesti HA, Agustiningsih: Karakterisasi Virus Influenza dari Pemantauan Berkala Kasus Influenza Like Illness (ILI) di Indonesia. In. Jakarta: National Institute of Health Research and Development; 2014.
26.
go back to reference Moura FE: Influenza in the tropics. Curr Opin Infect Dis 2010, 23(5):415–420. Moura FE: Influenza in the tropics. Curr Opin Infect Dis 2010, 23(5):415–420.
27.
go back to reference Bloom-Feshbach K, Alonso WJ, Charu V, Tamerius J, Simonsen L, Miller MA, Viboud C. Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): a global comparative review. PLoS One. 2013;8(2):e54445.CrossRef Bloom-Feshbach K, Alonso WJ, Charu V, Tamerius J, Simonsen L, Miller MA, Viboud C. Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): a global comparative review. PLoS One. 2013;8(2):e54445.CrossRef
28.
go back to reference Kosasih H, Klimov A, Xiyan X, Lindstrom S, Mahoney F, Beckett C, Burgess TH, Blair PJ, Uyeki TM, Sedyaningsih ER. Surveillance of influenza in Indonesia, 2003–2007. Influenza Other Respir Viruses. 2013;7(3):312–20.CrossRef Kosasih H, Klimov A, Xiyan X, Lindstrom S, Mahoney F, Beckett C, Burgess TH, Blair PJ, Uyeki TM, Sedyaningsih ER. Surveillance of influenza in Indonesia, 2003–2007. Influenza Other Respir Viruses. 2013;7(3):312–20.CrossRef
29.
go back to reference Zambon M, Hays J, Webster A, Newman R, Keene O. Diagnosis of influenza in the community: relationship of clinical diagnosis to confirmed virological, serologic, or molecular detection of influenza. Arch Intern Med. 2001;161(17):2116–22.CrossRef Zambon M, Hays J, Webster A, Newman R, Keene O. Diagnosis of influenza in the community: relationship of clinical diagnosis to confirmed virological, serologic, or molecular detection of influenza. Arch Intern Med. 2001;161(17):2116–22.CrossRef
30.
go back to reference Monto AS, Gravenstein S, Elliott M, Colopy M, Schweinle J. Clinical signs and symptoms predicting influenza infection. Arch Intern Med. 2000;160(21):3243–7.CrossRef Monto AS, Gravenstein S, Elliott M, Colopy M, Schweinle J. Clinical signs and symptoms predicting influenza infection. Arch Intern Med. 2000;160(21):3243–7.CrossRef
31.
go back to reference Van Elden L, Van Essen G, Boucher C, Van Loon A, Nijhuis M, Schipper P, Verheij T, Hoepelman I. Clinical diagnosis of influenza virus infection: evaluation of diagnostic tools in general practice. Br J Gen Pract. 2001;51(469):630–4.PubMedPubMedCentral Van Elden L, Van Essen G, Boucher C, Van Loon A, Nijhuis M, Schipper P, Verheij T, Hoepelman I. Clinical diagnosis of influenza virus infection: evaluation of diagnostic tools in general practice. Br J Gen Pract. 2001;51(469):630–4.PubMedPubMedCentral
32.
go back to reference MONTO AS, Kioumehr F: the Tecumseh study of respiratory illness IX. Occurrence of influenza in the community, 1966–1971. Am J Epidemiol 1975, 102(6):553–563. MONTO AS, Kioumehr F: the Tecumseh study of respiratory illness IX. Occurrence of influenza in the community, 1966–1971. Am J Epidemiol 1975, 102(6):553–563.
33.
go back to reference Kerkhove MD, Hirve S, Koukounari A, Mounts AW: Estimating age-specific cumulative incidence for the 2009 influenza pandemic: a meta-analysis of a (H1N1) pdm09 serological studies from 19 countries. Influenza Other Respir Viruses 2013, 7(5):872–886. Kerkhove MD, Hirve S, Koukounari A, Mounts AW: Estimating age-specific cumulative incidence for the 2009 influenza pandemic: a meta-analysis of a (H1N1) pdm09 serological studies from 19 countries. Influenza Other Respir Viruses 2013, 7(5):872–886.
34.
go back to reference Muñoz FM: The impact of influenza in children. In: Semin Pediatr Infect Dis: 2002: Elsevier; 2002: 72–78. Muñoz FM: The impact of influenza in children. In: Semin Pediatr Infect Dis: 2002: Elsevier; 2002: 72–78.
35.
go back to reference Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, Massari M, Salmaso S, Tomba GS, Wallinga J. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008;5(3):e74.CrossRef Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, Massari M, Salmaso S, Tomba GS, Wallinga J. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008;5(3):e74.CrossRef
36.
go back to reference Wallinga J, Teunis P, Kretzschmar M. Using data on social contacts to estimate age-specific transmission parameters for respiratory-spread infectious agents. Am J Epidemiol. 2006;164(10):936–44.CrossRef Wallinga J, Teunis P, Kretzschmar M. Using data on social contacts to estimate age-specific transmission parameters for respiratory-spread infectious agents. Am J Epidemiol. 2006;164(10):936–44.CrossRef
Metadata
Title
Surveillance and characterisation of influenza viruses among patients with influenza-like illness in Bali, Indonesia, July 2010–June 2014
Authors
Wiku Adisasmito
Sri Budayanti
Dewi Nur Aisyah
Richard Coker
Ayu Rai Andayani
Gavin J. D. Smith
James W. Rudge
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-3842-5

Other articles of this Issue 1/2019

BMC Infectious Diseases 1/2019 Go to the issue