Indian Journal of Medical Microbiology IAMM  | About us |  Subscription |  e-Alerts  | Feedback |  Login   
  Print this page Email this page   Small font sizeDefault font sizeIncrease font size
 Home | Ahead of Print | Current Issue | Archives | Search | Instructions  
Users Online: 542 Official Publication of Indian Association of Medical Microbiologists 
 ~  Similar in PUBMED
 ~  Search Pubmed for
 ~  Search in Google Scholar for
 ~Related articles
 ~  Article in PDF (387 KB)
 ~  Citation Manager
 ~  Access Statistics
 ~  Reader Comments
 ~  Email Alert *
 ~  Add to My List *
* Registration required (free)  

 ~  Abstract
 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusion
 ~  References
 ~  Article Tables

 Article Access Statistics
    PDF Downloaded48    
    Comments [Add]    

Recommend this journal


  Table of Contents  
Year : 2019  |  Volume : 37  |  Issue : 3  |  Page : 401-405

Dynamics of the occurrence of influenza in relation to seasonal variation in Chennai, Tamil Nadu: A 7 -year cumulative study

Department of Virology, King Institute of Preventive Medicine and Research, Chennai, Tamil Nadu, India

Date of Submission04-Dec-2019
Date of Decision12-Nov-2019
Date of Acceptance24-Dec-2019
Date of Web Publication29-Jan-2020

Correspondence Address:
Dr. Krishnasamy Kaveri
Department of Virology, King Institute of Preventive Medicine and Research, Guindy, Chennai - 600 032, Tamil Nadu
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_19_226

Rights and Permissions

 ~ Abstract 

Background: Influenza viruses have emerged as virulent pathogens causing considerable burden across the world. A thorough understanding of the pattern in occurrence of influenza globally is the need of hour. The present study deals with analysis of the dynamics of Influenza virus, especially the influence of seasonal change on viral circulation and causation of epidemics/pandemics in the context of subtropical region. Methods: During the 7 year (2009–2015) study, 36670 specimens were subjected to influenza analysis. Nasopharyngeal swabs collected from suspected patients from Chennai, Tamil Nadu, were tested and typed by real-time polymerase chain reaction assay. Results: During 2009 pandemic, among influenza A positives 95.16% were Apdm09, indicating that there was a predominant circulation of Apdm09. During postpandemic period, there were waves in the occurrence of Apdm09 which indicates fall in immunity with buildup in the susceptible population. Conclusion: In Chennai, Tamil Nadu, influenza positivity started with the onset of monsoon and peaks during the postmonsoon months throughout the study period. The assessment of meteorological factors compounding influenza activity can help in raising alerts to the public health officials of impending disaster which suggests that Influenza vaccination can be initiated before monsoon months in South India.

Keywords: Chennai, geographic circulation, influenza, pandemic, seasonality, surveillance

How to cite this article:
Kiruba R, Suresh Babu B V, Sheriff A K, Gunasekaran P, Anupama C P, Saran N, Kumar V S, Padmapriya P, Chakravarthy N N, Kaveri K. Dynamics of the occurrence of influenza in relation to seasonal variation in Chennai, Tamil Nadu: A 7 -year cumulative study. Indian J Med Microbiol 2019;37:401-5

How to cite this URL:
Kiruba R, Suresh Babu B V, Sheriff A K, Gunasekaran P, Anupama C P, Saran N, Kumar V S, Padmapriya P, Chakravarthy N N, Kaveri K. Dynamics of the occurrence of influenza in relation to seasonal variation in Chennai, Tamil Nadu: A 7 -year cumulative study. Indian J Med Microbiol [serial online] 2019 [cited 2020 Oct 28];37:401-5. Available from:

 ~ Introduction Top

Influenza is one of the most significant diseases in human beings causing high morbidity and mortality. It is associated with approximately 250,000–500,000 global deaths annually (World Health Organisation, 2009).

An improved understanding of the temporal and geographic variation in influenza viral circulation is essential for the development of influenza prevention and control strategies in tropical and subtropical regions.[1],[2],[3]

Further, recent studies point to a link between increased influenza activity and the rainy season in several tropical regions.[4],[5],[6],[7] The activity is also high when humidity is typically high in tropical regions, in contrast to its occurrence when humidity is low (indoor) in temperate regions. In variance to temperate regions, tropical region has significant influenza activity throughout the year and some tropical regions are characterized by two distinct influenza seasons, such as in Singapore and Hong Kong.[3],[8]

Several studies pertaining to the occurrence of influenza would be required distinctly belonging to different domains to have complete knowledge of the circulating strains. In this retrospective study, we propose to report the surveillance data of the occurrence of influenza and its subtypes in relation to seasonality during a 7-year period from 2009 to 2015, inclusive of the pandemic period and post-pandemic period in South India. This study was done under the Multi Site Epidemiological and Virological Monitoring of Human Influenza Viruses in India (MSM)/pandemic project under the Indian Council of Medical Research and we have also included samples referred to us during the pandemic period and outbreaks.

 ~ Materials and Methods Top

Case definition

Influenza like illness

A person presenting with sudden onset of fever >38°C or history of sudden onset of fever in the recent past (<3 days) and cough or sore throat or rhinorrhea.

Severe acute respiratory infection

Severe acute respiratory infection (SARI) was defined as an influenza-like illness (ILI) case with breathlessness or difficulty in breathing/tachypnea or clinically suspected pneumonia (in children) with increased respiratory rates as per Integrated Management of Childhood Illness.[9]

Laboratory diagnosis

Collection of clinical specimens

Nasopharyngeal swabs were collected in viral transport media and transported in the cold chain to the Department of Virology, King Institute of Preventive Medicine and Research, within 4 h of collection. The laboratory request form filled up with all necessary details and informed consent duly signed by the subject/guardian was taken for the subjects from whom samples were collected by us (for the referred samples we could not get the consent) before proceeding with the study. The specimens were collected from ILI/SARI (as per the World Health Organisation case definition) cases from different Government Hospitals and other Tertiary care centres in Chennai and from other parts of Tamil Nadu. For ILI cases outpatient departments of the hospitals mentioned above were visited and admission cases were included under SARI.

Nucleic acid extraction and real-time polymerase chain reaction

RNA was extracted from the clinical samples using an RNeasy Mini kit (Qiagen) following the manufacturer's instructions.

Real-time polymerase chain reaction (RT-PCR) assay was done using specific primers from conserved regions of the matrix (M) genes of Influenza viruses. The primers and probes for the detection of Influenza viruses and RNaseP(positive internal control) used in the study were provided by the Centres for Disease Control and Prevention. TaqMan qPCR was performed using a one-step RT-PCR kit (Invitrogen) with a 25 μl reaction mixture containing 5 μl extracted RNA, 12.5 μl × 2 reaction mix with ROX (Reference dye), 0.5 mM each primer and probe and 0.5 μl Superscript III RT/Platinum Taq mix following the kit protocol, on an ABI Prism 7500 system. The PCR cycling conditions consisted of an initial reverse transcriptase step at 50°C for 15 min, followed by a 2 min hold at 95°C and then 45 cycles of 15 s at 95°C and 30 s at 60°C. All Influenza A positive samples were further sub-typed for A/H1, A/H3 and AH1N1(pdm) 09.[10]

Meteorological data collection

Meteorological details including rainfall (in mm), humidity (percentage) and average temperature (°C) were collected during the study period from Regional Meteorological Centre, Nungambakkam, Chennai and Influenza positivity were correlated with seasonal activity.

Statistical analysis

The influenza patients were divided into four groups on the basis of detection of A/H1N1, A/H3N2, A (H1N1) pdm09 and influenza B. The laboratory data were analyzed using a Pearson's Chi-square test to compare the different strains. Statistical analysis was performed using Graph Prism 5.0., GraphPad Software, San Diego, CA. P values were considered statistically significant if found <0.05.

 ~ Results Top

During 2009-2015, 36670 specimens were tested for influenza by real-time RT-PCR of which 3505 (9.55%) were found positive for influenza viruses [Table 1]. Out of this, 3195 (91.15%) were found positive for Influenza A and 310 (8.85%) for influenza B. Sub-typing of Influenza A revealed that 2750 (86%) were A/(H1N1) pdm09, 441 (13.8%) as A/H3N2 and 4 (0.12%) seasonal A/H1N1 [Graph 1]. The Graph Pad Prism analysis which was carried out for calculation of P values for the occurrence of A pdm H1N1, H3N2, Flu B positivity was found to be statistically significant with P < 0.001 for all the strains during each year throughout the 7 year period.
Table 1: Year wise and strain wise influenza positivity

Click here to view

In 2009, there was very high positivity from July with predominant activity in August and September which gradually decreased from October to January 2010. There were no cases in February and March and relatively low positivity until May 2010. From June 2010, positive cases started again which was maximum in August, September and October 2010. There was a decline from Jan 2011 onwards.

We did not have any A pdm 09 positivity until March 2012. Initially, few cases started appearing in April 2012 and continued till July 2012. There was an increase in positivity from September 2012 till December 2012 with decline from January 2013. There were no cases till October 2013 and very few cases up to January 2014. By December 2014, pandemic H1N1 09 had started substantially increased and continued until July 2015. Thus, after pandemic H1N1 09 Tamil Nadu had witnessed outbreaks in waves, in 2012 followed by 2015.

 ~ Discussion Top

In 2009 and in 2010 with the advent of A H1N1 09 which formed the major chunk among the subtypes. There has been no case of seasonal H1N1 from 2009 till date, which has been totally eclipsed by A H1N1 09. In 2011, A H1N1 09 constituted only 5.37%, with A H3N2 predominating. In 2012, A H1N1 09 (68.15%) had made a comeback, with Type B constituting 37.6% and 20.06% respectively during 2011 and 2012. In 2013, 13.49% were positive A H1N109, with H3N2 incidence of 53.97%. In 2014, H3N2 was positive in 54.22% and A H1N109 in 31.33%, but this fall lead to a peak in the incidence of A H1N109 in 2015 (85.95%). Hence, it was one Flu strain which had predominated/was in circulation during each of the years. This was the case scenario throughout the country. Such waves are common following a pandemic. This pattern of alternation and predominance of one particular strain during one particular season reflects on the short immunity to previous strain and buildup of susceptible population, which happens to be cyclical rather than any major mutation in the pandemic A H1N1 strain.[11],[12],[13]

During the onset of the pandemic in June 2009, positive cases were observed from April onwards and the positivity started to increase with the onset of monsoon from August onwards. The peak was witnessed from September 09 to November 09 when there was a rapid decline in temperature with an increase in rainfall, especially in Chennai and northern districts of Tamil Nadu, wherein monsoon had set in late due to northeast monsoon [Graph 2]. Certain studies from different parts of South East Asia too followed a similar spectrum of infection which exhibited peaks in incidence during the rainy season.[3],[14],[15],[16],[17]

We have had successive peaks first in 2010, then in 2012 up to January 2013 and again from late 2014 to early 2015. The hikes in the occurrence indicate fall in the immunity among the general population and build of susceptible cohorts, it should be borne in mind that Influenza vaccination is given only to high-risk individuals and routine immunization is not in vogue.

The state of Tamil Nadu has two distinct period of rainfall, the southwest monsoon from June to September, with strong southwest winds; North-East monsoon from October to December, with dominant northeast winds. The dry, cooler season would be from January to March. The normal annual rainfall of the state is about 945 mm (37.2 inch), of which 48% is through the North East monsoon and 32% through the South West monsoon.[18],[19]

The occurrence of influenza outbreaks during these years started in July, with peaks in September and October followed by a decline in January. This indicated that monsoon and post-monsoon months faced maximum outbreaks in Chennai. Another article by Tamerius et al. was suggestive of two distinct types of climatic conditions are associated with influenza epidemics: cold/dry and humid/rainy across temperate and tropical climates,[20] respectively; hence, it could be concluded that Chennai falls in the second category with peaks during rainy season.

The present study identified that cold weather was not highly favourable for the propagation of the virus in our domain unlike in comparison with other tropical countries such as Vietnam and Taiwan where it was established the fact that winter proved to be favourable for influenza.[21],[22]

Hence, in Chennai with high levels (70%–82% maximum) of humidity throughout the year [Graph 3], the virus remains relatively stable, especially during the monsoon and post-monsoon months. Influenza viruses are more stable in the cold favouring robust and highly efficient transmission at 30°C that may be due to an increase in virus half-life at lower temperatures.[23,24] In Chennai, where it is hot and humid, the graph shows marginal fall in temperature in the months of September to January and with most of the outbreaks or positivity peaks occur during these months, probably lowering of temperature along with the increase in rainfall aids transmission. The increased shedding may be due to the effect of cold conditions in the host. Alternatively, virus may be more stable within the nasal passages when the cold ambient air cools the epithelial surface.[25] Increased virion stability at lower temperatures is likely due in part to decreased activity of proteases, hence augmented transmission. Transmission would be mainly affected by decrease in temperature and low humidity.[26]

As far as vaccination is concerned, initiation of vaccination before monsoon will be very effective in Tamil Nadu, hence the month of July – August can be the preferred month considering the districts bordering Western ghats which starts receiving monsoon earlier when compared to central districts and east coast of Tamil Nadu.[27]

As suggested in few articles, as a National policy, the latitude 30 can be taken to consideration and vaccination can be initiated accordingly,[28] with the region below 30 receiving vaccination by May–June.

 ~ Conclusion Top

The pattern of seasonality influencing influenza in different geographical regions remains unresolved. A thorough understanding of the meteorological factors affecting the virus is of major concern. Further research is particularly essential in tropical and subtropical areas, where the understanding of seasonality is negligible and requires a combination of experimental and observational studies. Moreover, understanding of the environmental factors that drive influenza circulation also may be useful to predict how dynamics will be affected at regional levels by global climate change. The National health authorities can plan vaccination against Influenza before the occurrence of Influenza with respect to the pattern of occurrence in different states.

The study proves the fact that influenza activity is more during monsoon and post-monsoon months with a tendency to cause outbreaks in waves within a span of 2 or 3 years. The public health authorities can also take cue from this analysis to initiate Institutional Ethical Committee (IEC) activities and other containment activities during the pre-monsoon period annually, with special educative programs conducted in schools, colleges and areas of congregation.

The role of environmental factors in the occurrence of Influenza in context to changing climatic and environmental scenario will give an insight to the perception on influenza which has profound value and of public health concern.

Financial support and sponsorship

This work was supported by ICMR (Grant Number: 5/8/7/14/2002-ECD-I dated: 21/04/2004 ICMR).

Conflicts of interest

There are no conflicts of interest.

 ~ References Top

World Health Organization. Acute Respiratory Infections: Influenza. World Health Organization; 2007. Available from: [Last accessed on 2011 Mar 15].  Back to cited text no. 1
Moura FE. Influenza in the tropics. Curr Opin Infect Dis 2010;23:415-20.  Back to cited text no. 2
Viboud C, Alonso WJ, Simonsen L. Influenza in tropical regions. PLoS Med 2006;3:e89.  Back to cited text no. 3
Chew FT, Doraisingham S, Ling AE, Kumarasinghe G, Lee BW. Seasonal trends of viral respiratory tract infections in the tropics. Epidemiol Infect 1998;121:121-8.  Back to cited text no. 4
Chumkiew S, Srisang W, Jaroensutasinee M, Jaroensutasinee K. Climatic factors affecting on influenza cases in Nakhon Si Thammarat. Proc World Acad Sci Eng Technol 2007;21:364-67.  Back to cited text no. 5
Mello WA, Paiva TM, Ishida MA, Benega MA, Santos MC, Viboud C, et al. The dilemma of influenza vaccine recommendations when applied to the tropics: The Brazilian case examined under alternative scenarios. PLoS One 2009;4:e5095.  Back to cited text no. 6
Dosseh A, Ndiaye K, Spiegel A, Sagna M, Mathiot C. Epidemiological and virological influenza survey in Dakar, Senegal: 1996-1998. Am J Trop Med Hyg 2000;62:639-43.  Back to cited text no. 7
Yang L, Wong CM, Lau EH, Chan KP, Ou CQ, Peiris JS. Synchrony of clinical and laboratory surveillance for influenza in Hong Kong. PLoS One 2008;3:e1399.  Back to cited text no. 8
World Health Organization. A Practical Guide to Harmonizing Virological and Epidemiological Influenza Surveillance. Western Pacific Region: World Health Organization; 2008. p. 5.  Back to cited text no. 9
World Health Organization. CDC Protocol of Realtime RTPCR for Swine Influenza A (H1N1). Atlanta, USA: World Health Organization; 2009. p. 5.  Back to cited text no. 10
Murhekar M, Mehendale S. The 2015 influenza A (H1N1) pdm09 outbreak in India. Indian J Med Res 2016;143:821-3.  Back to cited text no. 11
[PUBMED]  [Full text]  
Press Information Bureau, Government of India. Press Note from National Institute of Virology Pune. Press Information Bureau, Government of India; 12 March, 2015. Available from: [Last accessed on 2019 Sep 15].  Back to cited text no. 12
Finkelman BS, Viboud C, Koelle K, Ferrari MJ, Bharti N, Grenfell BT. Global patterns in seasonal activity of influenza A/H3N2, A/H1N1, and B from 1997 to 2005: viral coexistence and latitudinal gradients. PloS one. 2007;12;2:e1296.  Back to cited text no. 13
Waicharoen S, Thawatsupha P, Chittaganpitch M, Maneewong P, Thanadachakul T, Sawanpanyalert P. Influenza viruses circulating in Thailand in 2004 and 2005. Jpn J Infect Dis 2008;61:321-3.  Back to cited text no. 14
Doraisingham S, Ling AE. Acute non-bacterial infections of the respiratory tract in Singapore children: An analysis of three years' laboratory findings. Ann Acad Med Singapore 1981;10:69-78.  Back to cited text no. 15
Beckett CG, Kosasih H, Ma'roef C, Listiyaningsih E, Elyazar IR, Wuryadi S, et al. Influenza surveillance in Indonesia: 1999-2003. Clin Infect Dis 2004;39:443-9.  Back to cited text no. 16
Hasegawa GO, Kyaw Y, New HM, Danjuan LI, Saito R, Suzuki H, et al. Epidemiological study of influenza virus infections in Yangon, Myanmar. Trop Med Health. 2006;34:3-6.  Back to cited text no. 17
Ramakrishnan T. Entering 2006, City's Reservoirs Filled To The Brim. The Hindu; 3 January, 2006. Available from: [Last retrieved on 2012 Dec 28].  Back to cited text no. 18
Northeastern Monsoon. India Meteorological Department, Regional Meterological Centre, Chennai. Available from: [Last retrieved on 2016 Mar 19].  Back to cited text no. 19
Tamerius JD, Shaman J, Alonso WJ, Bloom-Feshbach K, Uejio CK, Comrie A, et al. Environmental predictors of seasonal influenza epidemics across temperate and tropical climates. PLoS Pathog 2013;9:e1003194.  Back to cited text no. 20
Park AW, Glass K. Dynamic patterns of avian and human influenza in East and Southeast Asia. Lancet Infect Dis 2007;7:543-8.  Back to cited text no. 21
Nguyen HL, Saito R, Ngiem HK, Nishikawa M, Shobugawa Y, Nguyen DC, et al. Epidemiology of influenza in Hanoi, Vietnam, from 2001 to 2003. J Infect 2007;55:58-63.  Back to cited text no. 22
Lowen AC, Mubareka S, Steel J, Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 2007;3:1470-6.  Back to cited text no. 23
Pica N, Chou YY, Bouvier NM, Palese P. Transmission of influenza B viruses in the guinea pig. J Virol 2012;86:4279-87.  Back to cited text no. 24
Eccles R. An explanation for the seasonality of acute upper respiratory tract viral infections. Acta Otolaryngol 2002;122:183-91.  Back to cited text no. 25
Lofgren E, Fefferman NH, Naumov YN, Gorski J, Naumova EN. Influenza seasonality: Underlying causes and modeling theories. J Virol 2007;81:5429-36.  Back to cited text no. 26
Chadha MS, Potdar VA, Saha S, Koul PA, Broor S, Dar L, et al. Dynamics of influenza seasonality at sub-regional levels in India and implications for vaccination timing. PLoS One 2015;10:e0124122.  Back to cited text no. 27
Koul PA, Broor S, Saha S, Barnes J, Smith C, Shaw M, et al. Differences in influenza seasonality by latitude, Northern India. Emerg Infect Dis 2014;20:1723-6.  Back to cited text no. 28


  [Table 1]


Print this article  Email this article


2004 - Indian Journal of Medical Microbiology
Published by Wolters Kluwer - Medknow

Online since April 2001, new site since 1st August '04