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Please cite this paper as: Chittaganpitch et al. (2012) Influenza viruses in Thailand: 7 years of sentinel surveillance data, 2004–2010. Influenza and Other Respiratory Viruses 6(4), 276–283.
Background The re-emergence of avian influenza A (H5N1) in 2004 and the pandemic of influenza A (H1N1) in 2009 highlight the need for routine surveillance systems to monitor influenza viruses, particularly in Southeast Asia where H5N1 is endemic in poultry. In 2004, the Thai National Institute of Health, in collaboration with the US Centers for Disease Control and Prevention, established influenza sentinel surveillance throughout Thailand.
Objectives To review routine epidemiologic and virologic surveillance for influenza viruses for public health action.
Methods Throat swabs from persons with influenza-like illness and severe acute respiratory illness were collected at 11 sentinel sites during 2004–2010. Influenza viruses were identified using the standard protocol for polymerase chain reaction. Viruses were cultured and identified by immunofluorescence assay; strains were identified by hemagglutination inhibition assay. Data were analyzed to describe frequency, seasonality, and distribution of circulating strains.
Results Of the 19 457 throat swabs, 3967 (20%) were positive for influenza viruses: 2663 (67%) were influenza A and able to be subtyped [21% H1N1, 25% H3N2, 21% pandemic (pdm) H1N1] and 1304 (33%) were influenza B. During 2009–2010, the surveillance system detected three waves of pdm H1N1. Influenza annually presents two peaks, a major peak during the rainy season (June–August) and a minor peak in winter (October–February).
Conclusions These data suggest that March–April may be the most appropriate months for seasonal influenza vaccination in Thailand. This system provides a robust profile of the epidemiology of influenza viruses in Thailand and has proven useful for public health planning.
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Since 2004, a widespread epidemic of highly pathogenic avian influenza caused by influenza A (H5N1) viruses in animal populations, particularly chickens, has swept through Southeast Asia. The disease poses a considerable public health risk. Not only can viruses infect humans directly, causing severe disease with high mortality,1 but there is also potential for these viruses to acquire the ability to transmit from human to human either by reassortment with other influenza viruses or by mutation and give rise to new pandemic strains.2 Avian influenza viruses were first detected in Thailand in January 2004, and through 2006, there were 25 persons infected with laboratory-confirmed influenza A (H5N1) viruses, including 17 deaths, reported to the World Health Organization (WHO).3 No cases have been identified since 2006.
In response to the spread of avian influenza A (H5N1) viruses, and in recognition that pandemic influenza preparedness is a core communicable disease control function, the Thai National Institute of Health (Thai NIH) at the Ministry of Public Health (MOPH), in collaboration with the US Centers for Disease Control and Prevention (CDC), established a series of influenza surveillance networks. In 2004, Thai NIH set up surveillance sites across the country. The surveillance system was established to monitor the frequency of influenza, identify new strains and describe seasonality.
In this manuscript, we present data on frequency, seasonality, and strain distribution of circulating influenza viruses from 2004 to 2010, at the 11 sentinel sites across the country. These virological and epidemiological data can support the public health service to better understand influenza viruses circulating in Thailand and to better plan effective prevention and control strategies in Thailand.
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We conducted surveillance for human influenza between September 2004 and December 2010 in 11 sites in Thailand. Of the 11 sites, 10 were in hospitals (one tertiary, four general, four community, and one private) and one was in a health center. Specimens were collected from 19 116 ILI cases (9638 in children <15 years and 9478 in persons ≥15 years) and 336 SARI cases (119 in children <5 years, 177 in persons 6–64 years and 40 in elderly ≥65 years). Of the 19 457 throat swabs, 3967 (20%) were positive for influenza viruses. Of the 3967 influenza positive specimens, 98% were from patients with ILI.
Among the 3896 influenza viruses from patients with ILI, 2612 (67%) were influenza A viruses and able to be subtyped [21% influenza A (H1N1), 25% influenza A (H3N2), 21% pandemic (pdm) H1N1] and 1284 (33%) were influenza B viruses (Table 1). No influenza A (H5N1) virus was identified. Less than 1% of influenza A viruses were not able to subtyped (data not shown). The proportion of samples that tested positive for influenza viruses ranged from a low of 15% in 2006 to a high of 25% in 2010 (Table 1). After implementing rRT-PCR, the percent of samples that was influenza positive increased from 19% (1564/8139) in 2004–2007 to 23% (2332/9982) in 2008–2010 (P < 0·001). The most frequently identified influenza virus in circulation by year was influenza A (H3N2) in 2005, influenza A (H1N1) in 2006, influenza A (H3N2) and influenza B in 2007, all three viruses in 2008 and pdm H1N1 in 2009 and 2010. The proportion positive in children <5 years ranged from a low of 10% in 2006 and 2009, where >60% of viruses identified were influenza A (H1N1) and pdm H1N1 virus, respectively, to a high of 18% in 2008, where influenza A (H1N1), influenza A (H3N2), and influenza B viruses circulated in roughly equal proportions. In addition to the general predominance of influenza A strains, the system also detected the emergence of pdm H1N1 in June 2009 and its persistence into 2010, and the emergence of a new variant of influenza, A/Brisbane/10/2007 (H3N2), which caused an outbreak in January 2007.
Table 1. Number and percent positive for influenza viruses by type/subtype and age groups among outpatients with ILI, September 2004–December 2010
|Year||% influenza positive in ILI||Distribution of influenza virus type/subtype|
|Age group (in years)||No. tested for ILI||Number positive for Influenza viruses (%)||A (H1N1)n (%)||A (H3N2)n (%)||A (pdm H1N1) n (%)||Bn (%)|
|5–64||10||4 (40)||2 (50)||0||–||2 (50)|
|Total||11||4 (36)||2 (50)||0||–||2 (50)|
|2005||<5||301||39 (13)||2 (5)||20 (51)||–||17 (44)|
|5–64||981||218 (22)||6 (3)||138 (63)||–||74 (34)|
|≥65||48||4 (8)||0||3 (75)||–||1 (25)|
|Total||1330||261 (20)||8 (3)||161 (62)||–||92 (35)|
|2006||<5||746||71 (10)||52 (73)||3 (4)||–||16 (23)|
|5–64||2675||432 (16)||263 (61)||44 (10)||–||125 (29)|
|≥65||66||3 (5)||3 (100)||0||–||0|
|Total||3487||506 (15)||318 (63)||47 (9)||–||141 (28)|
|2007||<5||1076||171 (16)||42 (25)||80 (47)||–||49 (29)|
|5–64||2119||612 (20)||88 (14)||257 (42)||–||267 (44)|
|≥65||116||10 (9)||0||8 (80)||–||2 (20)|
|Total||3311||793 (24)||130 (16)||345 (44)||–||318 (40)|
|2008||<5||995||184 (18)||59 (32)||53 (29)||–||72 (39)|
|5–64||2636||710 (27)||210 (30)||189 (27)||–||311 (44)|
|≥65||104||12 (12)||2 (17)||5 (42)||–||5 (42)|
|Total||3735||906 (24)||271 (30)||247 (27)||–||388 (43)|
|2009||<5||639||67 (10)||17 (25)||12 (18)||34 (51)||4 (6)|
|5–64||2352||554 (24)||69 (12)||65 (12)||344 (62)||76 (14)|
|≥65||87||9 (10)||1 (11)||4 (44)||4 (44)||0|
|Total||3078||630 (20)||87 (14)||81 (13)||382 (61)||80 (13)|
|2010||<5||885||119 (13)||0||21 (18)||50 (42)||48 (40)|
|5–64||2157||654 (30)||0||74 (11)||370 (57)||210 (32)|
|≥65||127||23 (18)||0||11 (48)||7 (30)||5 (22)|
|Total||3169||796 (25)||0||106 (13)||427 (54)||263 (33)|
|Total||19 121||3896 (20)||816 (21)||987 (25)||809 (21)||1284 (33)|
Among hospitalized patients in 2010, 21% had an influenza virus identified. The age group 5–64 years had a 28% influenza positive rate while young children <5 years and elderly ≥65 years had a similar influenza positive rate of 13%. Among children <5 years, influenza B virus was most commonly identified (44%), among persons aged 5–64 it was pdm H1N1 virus (64%) and among persons ≥65 years it was influenza A (H3N2) viruses (60%) (Table 2).
Table 2. Number and percent positive for influenza viruses by type/subtype among hospitalized patients with SARI in three sites, September–December 2010
|Age group (in years)||% influenza positive in SARI||Distribution of influenza virus type/subtype|
| || ||A (H1N1)||A (H3N2)||A (pdm H1N1)||B|
|No. Tested for SARI||Number positive for influenza viruses (%)||n (%)||n (%)||n (%)||n (%)|
|<5||119||16 (13)||–||5 (31)||4 (25)||7 (44)|
|5–64||177||50 (28)||–||5 (31)||32 (64)||13 (26)|
|≥65||40||5 (13)||–||3 (60)||2 (40)||–|
|Total||336||71 (21)||–||13 (18)||38 (54)||20 (28)|
Influenza viruses occurred throughout the year but the major peaks of influenza viruses in most regions were found in the rainy season from June through August (average 3-month range, 18–33% positive) with influenza A viruses dominating and a minor peak in the winter from October through February (average 5-month range, 11–17% positive) with influenza B viruses dominating circulation (Figure 2). In general, the peaks became more diffuse as the sites progressed south (Figure 3). In the 7 years of surveillance, the southern sites had only 2 months where no influenza virus was identified. In 2009, pdm H1N1 virus was first detected in the surveillance sites in June in Mae Sot, Phra Pok Klao, Koh Chang, Bangkok Samui, Koh Samui, and the Health Center in Bangkok. The number rapidly increased, and the greatest percent positive, 38%, was seen in August 2009. The second wave of pdm H1N1 virus began in November 2009 and peaked in mid-February 2010, and the third wave began in July 2010 and peaked in September 2010. During 2009–2010, pdm H1N1 virus was the predominant strain in both years and seasonal influenza A (H1N1) disappeared after September 2009. Among patients with ILI, influenza A (H3N2) and influenza B viruses were detected before September 2009 and throughout 2010, and the proportion positive for influenza A (H3N2) and influenza B viruses was similar in 2009 (13%), but in 2010, influenza B increased to 33% and influenza A (H3N2) was 13%.
Figure 2. Number of influenza cases and percentage of influenza-like illness and severe acute respiratory infection cases positive for influenza virus by type/subtype and month, Thailand, September 2004–December 2010.
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Figure 3. Percent positive of influenza cases by region (North, Northeast, East, South, and Central), September 2004–July 2010.
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During most years, the majority of circulating influenza A strains were well matched to the influenza strains in both the Southern and Northern Hemisphere vaccine compositions (Table 3). In 2007, the new A (H3N2) variant, A/Brisbane/10/2007, was first introduced and caused infections among persons presenting in most sentinel sites in January 2007. During 2004–2008, influenza B viruses of both Victoria and Yamagata lineages co-circulated and each year there was a change in lineage predominance suggesting that nearly half of the circulating influenza B viruses were mismatched with the influenza B component of the annual vaccine. In 2009 and 2010, only influenza B viruses of the Victoria lineage circulated so there was a complete match with the annual vaccine in these years.
Table 3. Influenza strains isolated in Thailand and Northern and Southern Hemisphere vaccine strains, 2004–2010
|Year||No. isolates||Thai strains||Vaccine strains for Northern Hemisphere||Vaccine strains for Southern Hemisphere|
|A (H1N1)||A (H3N2)||B|
|2004||344||A/New Caledonia/20/99||34||A/Fujian/411/2002||24||B/Shanghai/361/2002||5·2||A/New Caledonia/20/99(H1N1)||A/New Caledonia/20/99(H1N1)|
| || ||A/Wellington/1/2004||20||B/Hong Kong/330/2001||11||A/Fujian/411/2002(H3N2)||A/Fujian/411/2002(H3N2)|
| || ||A/California/7/2004||6·4|| || ||B/Shanghai/361/2002||B/Hong Kong/330/2001|
|2005||263||A/New Caledonia/20/99||3·4||A/California/7/2004||39||B/Shanghai/361/2002||19||A/New Caledonia/20/99(H1N1)||A/New Caledonia/20/99(H1N1)|
| || ||A/Wellington/1/2004||22||B/Hong Kong/330/2001||8·0||A/California/7/2004(H3N2)||A/Wellington/1/2004(H3N2)|
| || ||A/Wisconsin/67/2005||3·0||B/Malaysia/2506/2004||4·6||B/Shanghai/361/2002||B/Shanghai/361/2002|
|2006||353||A/New Caledonia/20/99||52||A/Wisconsin/67/2005||16||B/Shanghai/361/2002||13||A/New Caledonia/20/99(H1N1)||A/New Caledonia/20/99(H1N1)|
|A/Hawaii/15/2001||1·7|| || ||B/Malaysia/2506/2004||9·6||A/Wisconsin/67/2005(H3N2)||A/California/7/2004 (H3N2)|
|A/Solomon Islands/03/2006||1·7|| || ||B/Ohio/1/2005||3·7||B/Malaysia/2506/2004||B/Malaysia/2506/2004|
| || || || ||B/Hong Kong/330/2001||2·6|| || |
|2007||218||A/Solomon Islands/03/2006||11||A/Wisconsin/67/2005||28||B/Ohio/1/2005||13||A/Solomon Islands/3/2006(H1N1)||A/New Caledonia/20/99(H1N1)|
| || || || ||B/Malaysia/2506/2004||7·8||B/Malaysia/2506/2004||B/Malaysia/2506/2004|
|A/Solomon Islands/03/2006||1·2|| || ||B/Malaysia/2506/2004||16||A/Brisbane/10/2007 (H3N2)||A/Brisbane/10/2007 (H3N2)|
| || || || || || ||B/Florida/04/2006||B/Florida/04/2006|
|A/Brisbane/59/2007||13||A/Perth/16/2009||4·6||B/Malaysia/2506/2004||2·8||A/Brisbane/10/2007 (H3N2)||A/Brisbane/10/2007 (H3N2)|
| || || || || || ||B/Brisbane/60/2008||B/Florida/04/2006|
|2010||131||A/California/7/2009||52||A/Perth/16/2009||13||B/Brisbane/60/2008||31||A/California/07/2009 (H1N1)||A/California/07/2009 (H1N1)|
| || || || ||B/Malaysia/2506/2004||3·8||A/Perth/16/2009 (H3N2)||A/Perth/16/2009 (H3N2)|
| || || || || || ||B/Brisbane/60/2008||B/Brisbane/60/2008|
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We found that from 2004 to 2010, influenza viruses caused a substantial proportion of disease among ILI (20%) and SARI (21%) patients in Thailand. In the hospitalized patients from 2010, the age group 5–64 years had a 28% influenza positive rate while young children <5 years and elderly ≥65 years had a similar influenza positive rate of 13%. Although respiratory syncytial virus (RSV) is known to cause respiratory illness in young children,8 Thailand has limited data on the role of RSV in children.9 Our study demonstrates that the burden of disease caused by influenza viruses in young children is substantial and in some years (18% in 2008) approached the average level seen from RSV (19% in 2004–2007).9
Additionally, we detected influenza viruses in all months throughout the year, especially in the southern region of Thailand. While we cannot explain the differences in seasonality between Northern and Southern Thailand, it may be that climate or tourist differences play a role by contributing to viral persistence or viral re-introduction, respectively. The one private hospital that treated both Thai and foreign expatriates had less pronounced periods of viral activity (data not shown). Despite the annual presence of viruses, influenza viruses in Thailand annually presents two peaks, a major peak during the rainy season (June–August) and a minor peak in winter (October–February). Neighboring countries, such as Burma, Cambodia, Laos, and Vietnam, appear to have a similar peak of influenza viruses in the rainy season but the secondary peak was not as consistent.10–13 Our study suggests that March and April may be the most appropriate months for seasonal influenza vaccination in Thailand.
Our surveillance system is important to monitor for novel subtypes or new strains of an existing subtype that could affect the normal seasonality. An example is our detection of the new variant, A/Brisbane/10/2007 (H3N2), in January 2007, which produced a low HI titer with the WHO subtying reagent kit. This strain was identified in Thailand prior to its being included as a vaccine component in either the Southern or Northern Hemisphere influenza vaccines or the subtying reagent kit provided by WHO. This new variant subsequently caused sporadic outbreaks in many countries.14 This event highlights the importance of these data for international vaccine strain selection.
Our surveillance system has several limitations. Taking a convenience sample at each site may limit the generalizability of our data if there were biases in how these persons were selected. Our data on hospitalized SARI cases are too few to make inferences on more severe clinical forms of the disease, and we recognize the need to improve and strengthen this aspect of surveillance by expanding our surveillance for hospitalized patients. We also need to improve the linkage of virological data and epidemiological data to be more rapid and complete with information for an early warning system. Despite these limitations, we believe that our system provides a robust profile of the epidemiology of influenza in Thailand and has proven useful for public health planning and outbreak control.
During the past 7 years, the virologic surveillance system in Thailand was dramatically expanded and improved. Molecular diagnostics were added in 2008, resulting in an overall increase in the proportion of influenza virus detection. Because of the recent influenza pandemic from a novel swine origin influenza A (H1N1) virus and the continued occurrence of avian influenza outbreaks worldwide, there needs to be a continued emphasis on developing and improving the existing surveillance system in Thailand and support to strengthen the early warning system. Harmonization of virologic and epidemiologic surveillance has just been established using existing passive surveillance data from the Bureau of Epidemiology in the MOPH, which is currently collected weekly using ICD-10 codes, and virologic surveillance data from Thai NIH for the purpose of establishing a sensitive and timely influenza surveillance system capable of detecting and reporting increases in influenza activity that lead to public health action. To maintain its sustainability, the sentinel influenza surveillance system will need to continue to be flexible and meet new needs as they arise.
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We would like to thank the following for their valuable assistance in this study: the staff of Thai National Influenza Center, National Institute of Health, Department of Medical Science; the staff of Bureau of Epidemiology, Thailand Ministry of Public Health; the staff of Health Center 17, Mae Sot Hospital, Nong Khai Hospital, Pra Pok Klao Hospital, Chiang Saen Hospital, Mae Chan Hospital, Koh Chang Hospital, Koh Samui Hospital, Bangkok Hospital Samui, Hat Yai Hospital, and Bamrasnaradura Infectious Diseases Institute. We are grateful to WHO Collaborating Centers in Melbourne, Australia and US CDC, Atlanta, USA for providing reagents kits and for their technical assistance, and to Ann Moen, Influenza Division, National Center for Immunization and Respiratory Diseases, US CDC and Ms. Pranee Thawatsupha, Dr. Busarawan Sriwantana and Dr. Natteewan Poonwan from National Institute of Health, Department of Medical Sciences for their valuable advice and technical assistance. This work was supported by funding from the Department of Medical Sciences, Thailand Ministry of Public Health and US CDC (cooperative agreement 5U51IP000345).