Influenza Vaccine for Prevention of Laboratory-Confirmed Influenza
Virus Infection in the Korean Adult Population
Won Suk Choi,aJi Yun Noh,aYu bin Seo,aJi Hyeon Baek,bJacob Lee,cJoon Young Song,aDae Won Park,aJin Soo Lee,b Hee Jin Cheong,aWoo Joo Kima,d
Division of Infectious Diseases, Department of Internal Medicine, Korea University College of Medicine, Seoul,aDivision of Infectious Diseases, Department of Internal
Medicine, Inha University College of Medicine, Icheon,bDivision of Infectious Diseases, Department of Internal Medicine, Hallym University College of Medicine,
Chuncheon,cand Transgovernmental Enterprise for Pandemic Influenza in Korea, Seoul,dRepublic of Korea
We evaluated the effectiveness of the 2010-2011 seasonal influenza vaccine for preventing laboratory-confirmed influenza in a South Korean population. A retrospective case-control study was conducted among patients who visited selected hospitals from September 2010 to May 2011. A total of 483 laboratory-confirmed influenza patients were included in the analysis as case sub-jects. For each case patient, two types of control patients were chosen at a ratio of 1:1:1, and 966 control subjects were selected. Vaccine effectiveness (VE) was defined as 100ⴛ(1ⴚodds ratio for influenza in vaccinated versus nonvaccinated persons). The VE of the 2010-2011 seasonal influenza vaccine was 49.5% to 45.8% for both influenza A and B viruses and 50.8% to 47.2% for influenza A virus, according to the control type. The age-specific adjusted VE was 50.8% to 46.5% among subjects aged 19 to 49 years and 58.7% to 63.3% among those aged 50 to 64 years, according to the control type. Statistically significant VE was not found among those aged>65 years or against influenza B virus. The 2010-2011 seasonal influenza vaccine was effective for pre-venting laboratory-confirmed influenza, especially for influenza A virus, in a South Korean population. Evidence of the effective-ness of the influenza vaccine in older adults or against influenza B virus was not found.
T
he influenza pandemic caused by A/H1N1 2009 (A/H1N1 2009pdm) virus officially ended in August 2010, but the epi-demic caused by the A/H1N1 influenza virus continued in the 2010-2011 season. Many people experienced influenza A/H1N1 2009pdm through natural infection during 2009 and 2010. How-ever, the effect of the seasonal influenza vaccine in 2010-2011 could have been different from that in previous seasons. In fact, according to one report, prior vaccination and immunity to A/H1N1 2009pdm had a suppressive impact on the immune re-sponse induced by the 2010-2011 influenza vaccine (1). There were some reports on the clinical effectiveness of the 2010-2011 influenza vaccine in a relatively small population of children (2–5).The seasonal influenza vaccine has been used widely in South Korea, especially among the elderly (6), and the need for the in-fluenza vaccine has been increasing since the 2009 inin-fluenza pan-demic. Groups at high risk for influenza, such as patients with chronic medical conditions or the elderly, are priority groups for influenza vaccination. The influenza vaccine has especially been given to the elderly free of charge by the government. Almost all of the influenza vaccines used for the elderly are traditional unadju-vanted split vaccines. However, studies on the effectiveness of the vaccine are lacking, and debate concerning vaccine use continues in South Korea.
This study evaluated the effectiveness of the 2010-2011 sea-sonal influenza vaccine for preventing laboratory-confirmed in-fluenza virus infection in a population of South Korean adults.
MATERIALS AND METHODS
Study population and data collection.A matched case-control study was conducted among patients who visited four university hospitals with in-fluenza-like illness (ILI) from September 2010 to May 2011. ILI was de-fined as fever with cough, sore throat, or rhinorrhea. The patients with ILI
were usually tested for influenza virus in the participating hospitals ac-cording to the physician’s decision, especially in the emergency room or outpatient department. In this study, if a patient was an inpatient and ILI occurred after more than 48 h from the time of hospitalization, the patient
was excluded. Patientsⱖ18 years of age with laboratory-confirmed
influ-enza were selected as case patients. Laboratory-confirmed influinflu-enza was defined as a positive result from a rapid antigen test (RAT), PCR test, or influenza virus culture, regardless of when the symptoms started. For each case patient, two types of control (control 1 and 2) patients were chosen at a ratio of 1:1:1. A control 1 patient was defined as an age group-matched patient who visited the same hospital with ILI within 48 h of symptom onset but for whom laboratory tests were negative for influenza virus. A control 2 patient was defined as an age group-matched patient who visited the same clinic in the same hospital without ILI. Control 2 subjects visited the hospital for their underlying diseases or other acute diseases, such as acute gastroenteritis and cellulitis. Age group and visit date were matched between the case and both controls. All subjects were stratified into three age groups: 18 to 50, 51 to 64, and over 65 years. If two or more control subjects fulfilled the matching criteria, the subject with the smallest age difference from the case patient was selected from among them. If a se-lected control subject had an obscure influenza vaccination history or refused to have a telephone interview, a new control subject was chosen by use of the same criteria.
Data collection.Using a standardized questionnaire, the following data were collected for the subjects by reviewing their medical records:
Received5 January 2013 Returned for modification28 January 2013
Accepted2 April 2013
Published ahead of print10 April 2013
Address correspondence to Hee Jin Cheong, heejinmd@korea.ac.kr.
Copyright © 2013, American Society for Microbiology. All Rights Reserved.
doi:10.1128/CVI.00009-13
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age, sex, clinical symptoms, date of symptom onset, date of clinic visits, vaccination status for the 2010-2011 season, diagnostic laboratory results for influenza, chronic medical conditions, and pregnancy and smoking status (current or previous smoker or nonsmoker). The patients were defined as having a chronic medical condition if they had any of the following: diabetes mellitus, cardiovascular disease, cerebrovascular dis-ease, neuromuscular disdis-ease, chronic pulmonary disdis-ease, chronic renal disease, chronic hepatic disease, treatment for malignancy, congenital or acquired immunodeficiency, and medication with immunosuppressant agents. The 2010-2011 seasonal influenza vaccination history for each subject was checked by reviewing the medical records and conducting a telephone interview. We defined vaccinated individuals as those who had received the seasonal influenza vaccine before 14 days before the date of symptom onset.
Laboratory analysis. All four hospitals used the same laboratory methods for confirmation of influenza. Nasopharyngeal or throat swab specimens were used for the influenza laboratory tests. RAT was per-formed using a commercial kit, the SD Bioline influenza antigen test (Standard Diagnostic, Inc., South Korea), according to the manufactur-er’s instructions. PCR was performed using a commercial multiplex real-time PCR kit, the Anyplex II RV16 detection kit (Seegene, South Korea). An influenza virus culture was performed using an R-Mix Too (A549/ MDCK) shell vial culture. After the virus culture, immunofluorescence staining was performed using a Respiratory Virus Screening & ID kit (Dow Biomedical, South Korea) to identify the virus.
Data analyses.Statistical analyses were performed using SPSS, version 12.0 (SPSS, Chicago, IL). Logistic regression was used to estimate the odds ratio for laboratory-confirmed influenza in vaccinated versus
unvacci-nated subjects. Vaccine effectiveness (VE) was defined as 100⫻(1⫺odds
ratio for influenza in vaccinated versus nonvaccinated persons) according
to previous similar study protocols (7). Logistic regression models were
adjusted for age, smoker status, and comorbidities. The significant differ-ence in the distribution of variables between cases and controls was
esti-mated by the chi-square or Fisher’s exact test for categorical variables and
Student’sttest for quantitative variables. A bilateralPvalue of⬍0.05 was
considered a significant result.
Review of the research plan.The study was performed with the ap-proval of the institutional review board (IRB) from each of the four hos-pitals. The requirement for written informed consent was waived because most of the data were collected retrospectively by reviewing medical re-cords. A telephone interview was done only for checking the 2010-2011 seasonal influenza vaccination history. If a subject refused to have a tele-phone interview, the subject was excluded from the analysis.
RESULTS
During the study period, a total of 796 ILI patients were diagnosed with laboratory-confirmed influenza. Among these patients, 313 patients were excluded due to an obscure influenza vaccination history. As a result, a total of 1,449 subjects were included in this study: 483 cases in each group (Table 1). Among the case subjects, 473 (97.9%) subjects were tested with RAT and 435 (90.1%) sub-jects were positive for influenza virus, 114 (23.6%) subsub-jects were tested with PCR and 98 (86.0%) subjects were positive for influ-enza virus, and 69 (14.2%) subjects were tested with virus culture and 48 (69.6%) subjects were positive for influenza virus. Among the control 1 subjects, 470 (97.3%) subjects were tested with RAT, 53 (11.0%) subjects were tested with PCR, and 66 (13.7%) subjects were tested with virus culture.
Among the case subjects, 473 (97.9%) subjects were positive for influenza A virus, 9 (1.9%) subjects were positive for influenza B virus, and 1 (0.2%) subject was positive for both influenza A and B viruses. Among the patients in the three groups, 981 (67.7%) patients were younger than 50 years of age, 309 (21.3%) patients were 50 to 64 years of age, and 159 (11.0%) patients wereⱖ65 TABLE 1Demographic characteristics of the study cases and controls
Characteristic Cases (n⫽483) Control 1 (n⫽483) Control 2 (n⫽483) Pvalue
No. (%) of male patients 199 (41.2) 190 (39.3) 194 (40.2) NSb
No. (%) of patients by age group NS
⬍50 yr 327 (67.7) 327 (67.7) 327 (67.7)
50–64 yr 103 (21.3) 103 (21.3) 103 (21.3)
ⱖ65 yr 53 (11.0) 53 (11.0) 53 (11.0)
No. (%) of patients by smoker status ⬍0.01
Current smoker 91 (18.8) 69 (14.3) 68 (29.8)
Ex-smoker 38 (7.9) 17 (3.5) 17 (3.5)
Nonsmoker 237 (49.1) 295 (61.1) 259 (53.6)
No. (%) of patients with the following comorbiditiesa: 160 (33.1) 162 (33.3) 221 (45.8) ⬍0.01
Diabetes mellitus 42 (8.7) 34 (7.0) 44 (9.1) NS
Hypertension 69 (14.3) 76 (15.7) 67 (13.9) NS
Cardiovascular diseases 27 (5.6) 17 (3.5) 17 (3.5) NS
Cerebrovascular diseases 13 (2.7) 9 (1.9) 10 (2.1) NS
Neuromuscular diseases 5 (1.0) 2 (0.4) 6 (1.2) NS
Chronic pulmonary diseases 34 (7.0) 41 (8.5) 8 (1.7) ⬍0.01
Chronic renal failure 8 (1.7) 10 (2.1) 8 (1.7) NS
Chronic liver diseases 19 (3.9) 25 (5.2) 46 (9.5) NS
Malignancy 21 (4.3) 17 (3.5) 17 (3.5) NS
No. (%) of pregnant patients 23 (4.8) 12 (2.5) 8 (1.7) NS
No. (%) of patients with 2010-2011 season influenza vaccination history
85 (17.6) 142 (29.4) 146 (30.2) ⬍0.01
aSome patients had one or more comorbidities. b
NS, not significant.
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years of age. Five hundred eight-three (40.2%) patients were male, and 543 (37.5%) patients had one or more underlying diseases. There was no significant difference in gender among the three groups, but chronic medical conditions were more common in control 2 patients.
Among the 1,449 subjects, 273 (18.8%) were vaccinated with a dose of 2010-2011 seasonal influenza vaccine. In univariate anal-ysis, the influenza vaccination rate was significantly higher in both control 1 and 2 patients than in the case group (P⬍0.01 for both comparisons). For control 1, the VE of the 2010-2011 seasonal influenza vaccine was calculated to be 49.5% (95% confidence interval [CI], 30.4% to 63.3%) for influenza A and B viruses and 50.8% (95% CI, 31.9% to 64.4%) for influenza A virus (Table 2). For control 2, the VE of the 2010-2011 seasonal influenza vaccine was calculated to be 45.8% (95% CI, 24.6% to 61.1%) for influ-enza A and B viruses and 47.2% (95% CI, 26.0% to 62.3%) for influenza A virus. The age-specific adjusted VE was 50.8% (95% CI, 25.1% to 67.7%) to 46.5% (95% CI, 16.6% to 65.6%) among subjects aged 19 to 49 years, 58.7% (95% CI, 16.9% to 79.5%) to 63.3% (95% CI, 26.0% to 81.8%) among those aged 50 to 64 years, and 0.2% (95% CI, ⫺155.8% to 61.1%) to 53.0% (95% CI,
⫺31.8% to 83.2%) among those aged 65 years or more (Table 3). DISCUSSION
The study findings indicate that the 2010-2011 seasonal influenza vaccine was effective for preventing laboratory-confirmed influ-enza, especially for influenza A virus, in adults younger than 65 years of age. However, the influenza vaccine was not effective in the elderly or against influenza B virus. Because the main epidemic strain in the 2010-2011 season was influenza A virus, the number of case patients with laboratory-confirmed influenza B virus in-fection was too small to show the effectiveness of the influenza vaccine against influenza B virus. For the elderly, however, the present data indicate the limited effectiveness of the 2010-2011 seasonal influenza vaccine. A similar result was shown in another
study performed in Europe during the same season (8). The low level of effectiveness of the seasonal influenza vaccine in the el-derly for the prevention of influenza itself has been well docu-mented (9–11), although a reduction in influenza-associated morbidity and mortality has been shown with influenza vaccina-tion in the elderly. Recently, several types of vaccines, including an adjuvant-containing, high-dose, and intradermal vaccine, were developed for the elderly to overcome these limitations. In South Korea, almost all of the influenza vaccines used for the elderly are the traditional unadjuvanted split vaccine. During the 2010-2011 season, 95.2% of influenza vaccines approved for use by the South Korea Food and Drug Administration were traditional un-adjuvanted split vaccines (http://www.kfda.go.kr/index.kfda?mid ⫽50&cmd⫽v&seq⫽16220). Therefore, we have to carefully con-sider the use of adjuvanted, intradermal, or high-dose vaccines for the elderly if the cost-benefit of those vaccines is proven (9).
For influenza A virus, the 2010-2011 seasonal influenza vac-cine showed a deteriorated effectiveness compared with that of the pandemic influenza A/H1N1 2009pdm monovalent vaccine. In a previous study evaluating the effectiveness of the pandemic influ-enza vaccine using similar methods, the overall VE against the A/H1N1 2009pdm virus was 73.4%, although the age-specific VE was not identified for adults (7). The main epidemic strain in the 2010-2011 season was the A/H1N1 2009pdm virus. Because a large segment of the population was vaccinated with the pandemic influenza vaccine when the pandemic influenza occurred, a large portion of the study subjects might have already been exposed to the A/H1N1 2009pdm virus through natural infection or vaccina-tion. The pandemic influenza vaccination rate in South Korea was 26.1% for the total population and 54.4% for priority groups tar-geted by a national vaccination campaign (12). If many control subjects were exposed to the A/H1N1 2009pdm virus, it could have influenced the results of this study, by manifesting as an apparent deteriorated effectiveness of the influenza vaccine. We TABLE 2Effectiveness of 2010-2011 influenza virus vaccine according to influenza virus type
Comparison group
No. (%) of patients % VE (95% CI)
Cases Controls Unadjusted Adjusted
Case vs control 1
Influenza A virus 474 474 49.9 (31.8 to 63.2) 50.8 (31.9 to 64.4)
Vaccinees 83 (17.5) 141 (29.7)
Nonvaccinees 391 (82.5) 333 (70.3)
Influenza B virus 10 10 55.6 (⫺488.0 to 96.6) ⫺12.8 (⫺2,279.8 to 94.7)
Vaccinees 2 (20.0) 1 (10.0)
Nonvaccinees 8 (80.0) 9 (90.0)
Overall 483 483 48.7 (30.4 to 62.2) 49.5 (25.1 to 67.7)
Vaccinees 85 (17.6) 142 (29.4)
Nonvaccinees 398 (82.4) 341 (70.6)
Case vs control 2
Influenza A virus 474 474 51.4 (33.9 to 64.2) 47.2 (26.0 to 62.3)
Vaccinees 83 (17.5) 144 (30.4)
Nonvaccinees 391 (82.5) 330 (69.6)
Influenza B virus 10 10 41.7 (⫺356.2 to 92.5) 72.9 (⫺305.6 to 98.2)
Vaccinees 2 (20.0) 3 (30.0)
Nonvaccinees 8 (80.0) 7 (70.0)
Overall 483 483 50.7 (33.2 to 53.6) 45.8 (24.6 to 61.1)
Vaccinees 85 (17.6) 146 (30.2)
Nonvaccinees 398 (82.4) 337 (69.8)
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could not draw a conclusion on that issue because we did not check the pandemic influenza infection or vaccination history of the subjects.
In this study, we used two kinds of controls. Control 1 has generally been used in analyzing the effectiveness of the influ-enza vaccine in preventing laboratory-confirmed influinflu-enza. However, this has a limitation, in that some subjects are true influenza patients with false-negative results, especially with the RAT (13–16). This can produce a biased estimation of the effectiveness of the influenza vaccine. To minimize this limita-tion, we introduced control 2 in this analysis. Control 2 pa-tients were non-ILI papa-tients who visited the selected hospitals without an ILI. In fact, the control 2 subjects were not repre-sentative of cases, and they had more comorbidities than the case or control 1 subjects. When we compared the results of the analyses with control 1 and 2 subjects, there was no obvious difference except in those in the age groupⱖ65 years old. The adjusted VE in that age group showed different results accord-ing to the kinds of controls. This difference is due to the differ-ence of the proportion of the comorbidities.
This study had several limitations. First, among the control subjects, some may have been influenza patients because they showed false-negative results or asymptomatic status. The RAT is well-known to have low sensitivity, especially for patients who take the test afterⱖ3 days of symptom onset (14). To minimize the false-negative results, however, control 1 subjects were re-stricted to patients with an ILI who visited the same hospital within 48 h of symptom onset in this study. Second, this study focused on the effect of the influenza vaccine on the occurrence of laboratory-confirmed influenza. Although the influenza vaccine was not found to be effective in older adults in this study, the influenza vaccine could reduce influenza-associated morbidity and mortality in that population. A study performed in Spain reported that the 2010-2011 influenza vaccine had a moderate
effect in preventing hospitalization in the at-risk population (17). Third, we did not check the A/H1N1 2009pdm virus vac-cination or infection history. During the pandemic period, the South Korea Centers for Disease Control and Prevention rec-ommended that healthy people with flu-like symptoms seek medical attention only if they had influenza-related complica-tions or were getting worse. Therefore, a considerable number of influenza patients might not be diagnosed with pandemic influenza. In addition, the pandemic influenza vaccine was given at various health care institutions, and the individual vaccination history could be checked only through personal interview. The authors decided not to check the A/H1N1 2009pdm vaccination or infection history, considering the un-reliability of the data. Lastly, it would be useful to apply the results of this study to the traditional unadjuvanted split influ-enza vaccine. Other types of influinflu-enza vaccines, such as the adjuvanted vaccine or the high-dose vaccine, may show differ-ent results.
In conclusion, the 2010-2011 seasonal influenza vaccine was effective for preventing laboratory-confirmed influenza, espe-cially for influenza A virus, in a South Korean adult population. However, evidence of the effectiveness of the influenza vaccine in the elderly or against influenza B virus was not found. For the elderly, in particular, the use of next-generation influenza vac-cines such as adjuvanted, intradermal, or high-dose vacvac-cines should be considered if improved effectiveness and cost-effective-ness are proven.
ACKNOWLEDGMENTS
This study was supported by a grant from the South Korea Healthcare Technology R&D Project, Ministry of Health & Welfare, Republic of Ko-rea (grant no. A103001).
We have no conflicts of interest to declare.
TABLE 3Effectiveness of 2010-2011 influenza virus vaccine according to age group
Comparison group
No. (%) of patients % VE (95% CI)
Cases Controls Unadjusted Adjusted
Case vs control 1
19–49 yr 327 327 53.3 (29.7 to 68.9) 50.8 (25.1 to 67.7)
Vaccinees 43 (13.1) 80 (24.5)
Nonvaccinees 284 (86.9) 247 (75.5)
50–64 yr 103 103 52.3 (10.7 to 74.6) 58.7 (16.9 to 79.5)
Vaccinees 21 (20.4) 36 (35.0)
Nonvaccinees 82 (79.6) 67 (65.0)
ⱖ65 yr 53 53 31.9 (⫺47.2 to 68.4) 0.2 (⫺155.8 to 61.1)
Vaccinees 21 (39.6) 26 (49.1)
Nonvaccinees 32 (60.4) 27 (50.9)
Case vs control 2
19–49 yr 327 327 49.1 (23.2 to 66.3) 46.5 (16.6 to 65.6)
Vaccinees 43 (13.1) 75 (22.9)
Nonvaccinees 284 (86.9) 252 (77.1)
50–64 yr 103 103 56.2 (18.2 to 76.5) 63.3 (26.0 to 81.8)
Vaccinees 21 (20.4) 38 (30.7)
Nonvaccinees 82 (79.6) 65 (63.1)
ⱖ65 yr 53 53 60.2 (13.1 to 81.8) 53.0 (⫺31.8 to 83.2)
Vaccinees 21 (39.6) 33 (62.3)
Nonvaccinees 32 (60.4) 20 (37.7)
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