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BMC Infectious Diseases
Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | Influenza | Research

Sentinel surveillance for influenza A viruses in Lahore District Pakistan in flu season 2015–2016

Authors: Saima Hasan, Richard J. Webby, Muhammad Iqbal, Hamad Bin Rashid, Mansur-ud-Din Ahmad, Jawad Nazir, Jennifer DeBeauchamp, Shakera Sadiq, Mamoona Chaudhry

Published in: BMC Infectious Diseases | Issue 1/2022

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Abstract

Background

Influenza A virus (IAV) remains an important global public health threat with limited epidemiological information available from low-and-middle-income countries. The major objective of this study was to describe the proportions, temporal and spatial distribution, and demographic and clinical characteristics of IAV positive patients with influenza like illness (ILI) and severe acute respiratory illness (SARI) in Lahore, Pakistan.

Methods

Prospective surveillance was established in a sentinel hospital from October 2015 to May 2016. All eligible outpatients and inpatients with ILI or SARI were enrolled in the study. Nasal and/or throat swabs were collected along with clinico-epidemiological data. Samples were tested by real-time RT-PCR (rRT-PCR) to identify IAV and subtype. The descriptive analysis of data was done in R software.

Results

Out of 311 enrolled patients, 284 (91.3%) were ILI and 27 (8.7%) were SARI cases. A distinct peak of ILI and SARI activity was observed in February. Fifty individuals (16%) were positive for IAV with peak positivity observed in December. Of 50 IAV, 15 were seasonal H3N2, 14 were H1N1pdm09 and 21 were unable to be typed. The majority of IAV positive cases (98%) presented with current or history of fever, 88% reported cough and 82% reported sore throat. The most common comorbidities in IAV positive cases were hepatitis C (4%), obesity (4%) and tuberculosis (6%). The highest incidence of patients reporting to the hospital was seen three days post symptoms onset (66/311) with 14 of these (14/66) positive for IAV.

Conclusion

Distinct trends of ILI, SARI and IAV positive cases were observed which can be used to inform public health interventions (vaccinations, hand and respiratory hygiene) at appropriate times among high-risk groups. We suggest sampling from both ILI and SARI patients in routine surveillance as recommended by WHO.
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Literature
1.
Lambert LC, Fauci AS. Influenza vaccines for the future. N Engl J Med. 2010;363(21):2036–44.PubMed
2.
Korsun N, Angelova S, Teodosieva A. Virological surveillance of influenza in four recent post-pandemic seasons (2010/11 to 2013/14) in Bulgaria. Cent Eur J Public Health. 2016;24(3):180.PubMed
3.
Molinari N-AM, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine. 2007;25(27):5086–96.PubMed
4.
Simmerman JM, Chittaganpitch M, Levy J, Chantra S, Maloney S, Uyeki T, Areerat P, Thamthitiwat S, Olsen SJ, Fry A, et al. Incidence, seasonality and mortality associated with influenza pneumonia in Thailand: 2005–2008. PLoS ONE. 2009;4(11): e7776.PubMedPubMedCentral
5.
6.
Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ. Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect. 2010;119(4):439–45.PubMedPubMedCentral
7.
Newman LP, Bhat N, Fleming JA, Neuzil KM. Global influenza seasonality to inform country-level vaccine programs: an analysis of WHO FluNet influenza surveillance data between 2011 and 2016. PLoS ONE. 2018;13(2): e0193263.PubMedPubMedCentral
8.
UNO: World Population Prospects. In.; 2017.
9.
10.
11.
Shao W, Li X, Goraya MU, Wang S, Chen J-L. Evolution of influenza a virus by mutation and re-assortment. Int J Mol Sci. 2017;18(8):1650.PubMedCentral
12.
Kyaw Win SM, Saito R, Win NC, Lasham DJ, Kyaw Y, Lin N, Thein KN, Chon I, Odagiri T, Thein W, et al. Epidemic of influenza A(H1N1)pdm09 analyzed by full genome sequences and the first case of oseltamivir-resistant strain in Myanmar 2017. PLoS ONE. 2020;15(3): e0229601.PubMedPubMedCentral
13.
Nisar N, Aamir UB, Badar N, Mehmood MR, Alam MM, Kazi BM, Zaidi SSZ. Prediction of clinical factors associated with pandemic influenza A (H1N1) 2009 in Pakistan. PLoS ONE. 2014;9(2): e89178.PubMedPubMedCentral
14.
Bashir Aamir U, Badar N, Mehmood MR, Nisar N, Suleman RM, Shaukat S, Sharif S, Kamran J, Zaidi SSZ, Kazi BM, et al. Molecular epidemiology of influenza A(H1N1)pdm09 viruses from Pakistan in 2009–2010. PLoS ONE. 2012;7(8): e41866.PubMedPubMedCentral
15.
Chaudhry M, Webby R, Swayne D, Rashid HB, DeBeauchamp J, Killmaster L, Criado MF, Lee D-H, Webb A, Yousaf S, et al. Avian influenza at animal-human interface: One-health challenge in live poultry retail stalls of Chakwal, Pakistan. Influenza Other Respir Viruses. 2020;14(3):257–65.PubMedPubMedCentral
16.
Chaudhry M, Angot A, Rashid HB, Cattoli G, Hussain M, Trovò G, Drago A, Valastro V, Thrusfield M, Welburn S, et al. Reassortant avian influenza A(H9N2) viruses in chickens in retail poultry shops, Pakistan, 2009–2010. Emerg Infect Dis. 2015;21(4):673–6.PubMedPubMedCentral
17.
Ahad A, Thornton RN, Rabbani M, Yaqub T, Younus M, Muhammad K, Mahmood A, Shabbir MZ, Kashem MA, Islam MZ, et al. Risk factors for H7 and H9 infection in commercial poultry farm workers in provinces within Pakistan. Prev Vet Med. 2014;117(3):610–4.PubMed
18.
Nisar N, Aamir UB, Badar N, Mahmood MR, Yaqoob A, Tripathy JP, Laxmeshwar C, Tenzin K, Zaidi SSZ, Salman M, et al. Epidemiology of Influenza among patients with influenza-like illness and severe acute respiratory illness in Pakistan: a 10-year surveillance study 2008–17. J Med Virol. 2020. https://​doi.​org/​10.​1002/​jmv.​25913.CrossRefPubMed
19.
Anonymous: Area, population by sex, sex ratio, population density, urban proportion, household size and annual growth rate. In. Islamabad: Pakistan Bureau of Statistics, Government of Pakistan; 2017.
20.
Sarfaraz S, Arsalan MH, Fatima H. Regionalizing the climate of Pakistan using Köppen classification system. Pak Geogr Rev. 2014;69:111–32.
21.
Sajjad SH, Batool R, Qadri ST, Shirazi SA, Shakrullah K. The long-term variability in minimum and maximum temperature trends and heat island of Lahore city, Pakistan. Sci Int. 2015;27(2):1321–5.
22.
23.
24.
Zaman RU, Alamgir A, Rahman M, Azziz-Baumgartner E, Gurley ES, Sharker MAY, 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.PubMedPubMedCentral
25.
Center for Disease Control and Prevention. CDC real time RTPCR (rRTPCR) protocol for detection and chatacterization of swine influenza (version 2009). www.​who.​int.
26.
Shu B, Wu K-H, Emery S, Villanueva J, Johnson R, Guthrie E, Berman L, Warnes C, Barnes N, Klimov A. Design and performance of the CDC real-time reverse transcriptase PCR swine flu panel for detection of 2009 A (H1N1) pandemic influenza virus. J Clin Microbiol. 2011;49(7):2614–9.PubMedPubMedCentral
27.
Team RDC: a language and environment for statistical computing. In., 3.2.3 edn. Vienna, Austria: R Foundation for Statistical Computing; 2015.
28.
Nisar N, Badar N, Aamir UB, Yaqoob A, Tripathy JP, Laxmeshwar C, Munir F, Zaidi SSZ. Seasonality of influenza and its association with meteorological parameters in two cities of Pakistan: a time series analysis. PLoS ONE. 2019;14(7):e0219376–e0219376.PubMedPubMedCentral
29.
Yu H, Huang J, Huai Y, Guan X, Klena J, Liu S, Peng Y, Yang H, Luo J, Zheng J, et al. 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(1):53–65.PubMed
30.
Peng Z, Feng L, Carolyn GM, Wang K, Zhu G, Zhang Y, Hu J, Huang Y, Pan H, Guo N, et al. Characterizing the epidemiology, virology, and clinical features of influenza in China’s first severe acute respiratory infection sentinel surveillance system, February 2011–October 2013. BMC Infect Dis. 2015;15(1):143.PubMedPubMedCentral
31.
Tadesse M, Mengesha M, Tayachew A, Belay D, Hassen A, Woyessa AB, Zemelak E, Beyene B, Kassa W, Ayele W, et al. Burden and seasonality of medically attended influenza like illness (ILI) in Ethiopia, 2012 to 2017. BMC Infect Dis. 2020;20(1):148.PubMedPubMedCentral
32.
33.
Qi L, Xiong Y, Xiao B, Tang W, Ling H, Long J, Xiao D, Zhao H, Ye S, Chen S, et al. Epidemiological and virological characteristics of influenza in Chongqing, China, 2011–2015. PLoS ONE. 2016;11(12): e0167866.PubMedPubMedCentral
34.
Stellrecht KA. Chapter 11—molecular testing for respiratory viruses. In: Coleman WB, Tsongalis GJ, editors. Diagnostic molecular pathology. Academic Press: Cambridge; 2017. p. 123–37.
35.
Broor S, Parveen S, Bharaj P, Prasad VS, Srinivasulu KN, Sumanth KM, Kapoor SK, Fowler K, Sullender WM. A prospective three-year cohort study of the epidemiology and virology of acute respiratory infections of children in rural India. PLoS ONE. 2007;2(6):e491–e491.PubMedPubMedCentral
36.
Comach G, Teneza-Mora N, Kochel TJ, Espino C, Sierra G, Camacho DE, Laguna-Torres VA, Garcia J, Chauca G, Gamero ME, et al. Sentinel surveillance of influenza-like illness in two hospitals in Maracay, Venezuela: 2006–2010. PLoS ONE. 2012;7(9): e44511.PubMedPubMedCentral
37.
Lafond KE, Nair H, Rasooly MH, Valente F, Booy R, Rahman M, Kitsutani P, Yu H, Guzman G, Coulibaly D, et al. Global role and burden of influenza in pediatric respiratory hospitalizations, 1982–2012: a systematic analysis. PLOS Med. 2016;13(3): e1001977.PubMedPubMedCentral
38.
Pițigoi D, Streinu-Cercel A, Ivanciuc AE, Lazãr M, Cherciu CM, Mihai ME, Nițescu M, Aramă V, Crăciun MD, Streinu-Cercel A, et al. Surveillance of medically-attended influenza in elderly patients from Romania-data from three consecutive influenza seasons (2015/16, 2016/17, and 2017/18). Influenza Other Respir Viruses. 2020;14(5):530–40.PubMedPubMedCentral
39.
40.
41.
Baldo V, Bertoncello C, Cocchio S, Fonzo M, Pillon P, Buja A, Baldovin T. The new pandemic influenza A/(H1N1)pdm09 virus: is it really “new”? J Prev Med Hyg. 2016;57(1):E19–22.PubMedPubMedCentral
42.
Rubin R. Influenza’s unprecedented low profile during COVID-19 pandemic leaves experts wondering what this flu season has in store. JAMA. 2021;326(10):899–900.PubMed
43.
Lutwama JJ, Bakamutumaho B, Kayiwa JT, Chiiza R, Namagambo B, Katz MA, Geissler AL. Clinic- and hospital-based sentinel influenza surveillance, Uganda 2007–2010. J Infect Dis. 2012;206(suppl_1):S87–93.PubMed
44.
Drăgănescu A, Săndulescu O, Florea D, Vlaicu O, Streinu-Cercel A, Oţelea D, Aramă V, Luminos ML, Streinu-Cercel A, Niţescu M, et al. The influenza season 2016/17 in Bucharest, Romania—surveillance data and clinical characteristics of patients with influenza-like illness admitted to a tertiary infectious diseases hospital. Braz J Infect Dis. 2018;22(5):377–86.PubMed
45.
Badar N, Aamir UB, Mehmood MR, Nisar N, Alam MM, Kazi BM, Zaidi SSZ. Influenza virus surveillance in Pakistan during 2008–2011. PLoS ONE. 2013;8(11): e79959.PubMedPubMedCentral
46.
Worby CJ, Chaves SS, Wallinga J, Lipsitch M, Finelli L, Goldstein E. On the relative role of different age groups in influenza epidemics. Epidemics. 2015;13:10–6.PubMedPubMedCentral
47.
Maïnassara HB, Lagare A, Tempia S, Sidiki A, Issaka B, Sidikou BA, Oukem-Boyer OOM. Influenza sentinel surveillance among patients with influenza-like-illness and severe acute respiratory illness within the framework of the National Reference Laboratory, Niger, 2009–2013. PLoS ONE. 2015;10(7): e0133178.PubMedPubMedCentral
48.
Beauté J, Zucs P, Korsun N, Bragstad K, Enouf V, Kossyvakis A, Griškevičius A, Olinger C, Meijer A, Guiomar R. Age-specific differences in influenza virus type and subtype distribution in the 2012/2013 season in 12 European countries. Epidemiol Infect. 2015;143(14):2950–8.PubMed
49.
Wong KC, Luscombe GM, Hawke C. Influenza infections in Australia 2009–2015: is there a combined effect of age and sex on susceptibility to virus subtypes? BMC Infect Dis. 2019;19(1):42.PubMedPubMedCentral
50.
Gabriel G, Arck PC. Sex, immunity and influenza. J Infect Dis. 2014;209(suppl_3):S93–9.PubMed
51.
52.
Farrukh MJ, Ming LC, Zaidi STR, Khan TM. Barriers and strategies to improve influenza vaccination in Pakistan. J Infect Public Health. 2017;10(6):881–3.PubMed
53.
Casalegno J-S, Eibach D, Valette M, Enouf V, Daviaud I, Behillil S, Vabret A, Soulary JC, Benchaib M, Cohen JM, et al. Performance of influenza case definitions for influenza community surveillance: based on the French influenza surveillance network GROG, 2009–2014. Euro Surveill. 2017;22(14):30504.PubMedPubMedCentral
54.
Jones AH, Ampofo W, Akuffo R, Doman B, Duplessis C, Amankwa JA, Sarpong C, Sagoe K, Agbenohevi P, Puplampu N, et al. Sentinel surveillance for influenza among severe acute respiratory infection and acute febrile illness inpatients at three hospitals in Ghana. Influenza Other Respir Viruses. 2016;10(5):367–74.PubMedPubMedCentral
55.
Ohmit SE, Monto AS. Symptomatic predictors of influenza virus positivity in children during the influenza season. Clin Infect Dis. 2006;43(5):564–8.PubMed
56.
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.PubMed
57.
Fitzner J, Qasmieh S, Mounts AW, Alexander B, Besselaar T, Briand S, Brown C, Clark S, Dueger E, Gross D. Revision of clinical case definitions: influenza-like illness and severe acute respiratory infection. Bull World Health Organ. 2018;96(2):122.PubMed
58.
Ohfuji S, Fukushima W, Sasaki Y, Tamori A, Kurai O, Kioka K, Maeda K, Maeda A, Hirota Y. Influenza A (H1N1) pdm09 vaccine effectiveness and other characteristics associated with hospitalization in chronic liver disease patients. Liver Int. 2014;34(5):700–6.PubMed
59.
Honce RR, Schultz-Cherry S. Impact of obesity on influenza A virus pathogenesis, immune response, and evolution. Front Immunol. 2019;10:1071.PubMedPubMedCentral
60.
Walaza S, Tempia S, Dawood H, Variava E, Wolter N, Dreyer A, Moyes J, Von Mollendorf C, McMorrow M, Von Gottberg A, et al. The impact of influenza and tuberculosis interaction on mortality among individuals aged ≥15 years hospitalized with severe respiratory illness in South Africa, 2010–2016. Open Forum Infect Dis. 2019;6(3):020.
61.
Katz MA, Muthoka P, Emukule GO, Kalani R, Njuguna H, Waiboci LW, Ahmed JA, Bigogo G, Feikin DR, Njenga MK. Results from the first six years of national sentinel surveillance for influenza in Kenya, July 2007–June 2013. PLoS ONE. 2014;9(6): e98615.PubMedPubMedCentral
62.
63.
Metadata
Title
Sentinel surveillance for influenza A viruses in Lahore District Pakistan in flu season 2015–2016
Authors
Saima Hasan
Richard J. Webby
Muhammad Iqbal
Hamad Bin Rashid
Mansur-ud-Din Ahmad
Jawad Nazir
Jennifer DeBeauchamp
Shakera Sadiq
Mamoona Chaudhry
Publication date
01-12-2022
Publisher
BioMed Central
Keyword
Influenza
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-07021-7

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