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. 2019 Dec 26;8(1):7. doi: 10.3390/vaccines8010007

Knowledge, Attitudes, and Behaviors (KAB) of Influenza Vaccination in China: A Cross-Sectional Study in 2017/2018

Xiang Ren 1,2, Elizabeth Geoffroy 3, Keqing Tian 4,5, Liping Wang 1, Luzhao Feng 1, Jun Feng 6, Ying Qin 1, Peng Wu 2, Shaosen Zhang 6, Mengjie Geng 1, Lingjia Zeng 1, Jianxing Yu 7, Benjamin J Cowling 2, Zhongjie Li 1,*
PMCID: PMC7158667  PMID: 31888035

Abstract

Background: This study aimed to estimate influenza-like illness (ILI) prevalence, influenza-related healthcare seeking behaviors, and willingness for vaccination. Methods: A retrospective cross-sectional study based on a random dialing telephone survey was conducted from October 2017 through March 2018 to assess influenza-like illness prevalence and vaccination willingness among different demographic groups. Results: 10,045 individuals were enrolled and completed the survey. A total of 2834 individuals (28%) self-reported that they have suffered from influenza-like illness, especially children under 15 years of age. Overall willingness for influenza vaccination in the 2018/2019 influenza season was 45% and was positively associated with higher education level, recommendation from doctors, cost-free vaccination, and vaccination campaigns with employers’ support. Hospitalization and seeking medicine from pharmacies was less frequent in urban locations. People under 15 and over 60 years of age sought medical service more frequently. Conclusions: ILI prevalence differed significantly by age and geographical location/population density. Vaccination policy for motivating key populations at highest risk to vaccinate should take into consideration the awareness-raising of vaccination benefits, barriers reduction of vaccination such as cost, and recommendation via healthcare professionals.

Keywords: knowledge, attitudes, and behaviors (KAB); influenza; influenza vaccine; vaccine willingness; telephone survey; China

1. Introduction

The year 2018 marked the 100-year anniversary of the most severe influenza pandemic in recorded history, which infected nearly 500 million and killed an estimated of 50 million people worldwide over 2 years [1]. The World Health Organization (WHO) estimated that seasonal influenza was responsible for up to 650,000 deaths worldwide annually, and in China alone there were 456,718 reported influenza cases in 2017 with up to 92,000 annual influenza-associated respiratory deaths [2,3,4]. Seasonal epidemics and outbreaks globally caused considerable morbidity and mortality, and posed a significant threat to high-risk populations, such as pregnant women, infants, children, elderly, healthcare professionals, and patients with chronic underlying conditions (2). Furthermore, the 2017/2018 influenza season was particularly severe compared with recent years across the northern hemisphere including in China [5,6,7,8].

Vaccination is the most effective tool for influenza prevention, yet the current Expanded Program on Immunization (EPI) in China does not include the influenza vaccine; individuals are required to pay out of pocket for the influenza vaccine, and only a few locations had limited special subsidy programs for high risk groups [9]. National influenza vaccination coverage in China was just 1.5% to 2.2% between 2004 and 2014 [10]. In contrast, influenza vaccination coverage of residents over 60 years of age in 2015 was 49% in Beijing, where free influenza vaccination has been provided to residents over the age of 60 since 2007 [11]. Even more regional governments started to provide full or partial subsidy for influenza vaccines, but national influenza vaccine uptake has failed to increase substantially [10].

Based on a WHO fact sheet and China’s local conditions, Chinese Center for Disease Control and Prevention developed “technical guidelines for seasonal influenza vaccination in China (2018/2019)” to decrease the risk of severe infections and complications due to influenza virus infection among high risk groups. The technical guidelines recommended prioritization of seasonal influenza vaccination for children aged 6–60 months, adults over 60 years of age, persons with specific chronic diseases, healthcare workers, family members and caregivers of infants less than 6 months of age, and pregnant women or women who plan to get pregnant during the influenza season [3,12].

Because the sentinel surveillance system in China reports only individuals with influenza-like illness (ILI) visiting sentinel hospitals, it does not provide a full picture of ILI activities among the community. This study therefore aims to estimate the prevalence of self-reported ILI and ILI-related healthcare-seeking behaviors during the 2017/2018 influenza season in China, as well as to estimate influenza vaccination willingness for the 2018/2019 influenza season. We conducted a telephone survey in six provinces, three in northern China and three in southern China, which were sampled according to the diversified economic statuses, climate zones, and vaccine policies of provinces in China. The selected call respondents were asked about knowledge, attitudes, and behaviors relating to influenza-like illness and influenza vaccination.

2. Material and Methods

2.1. Study Design

This is a retrospective cross-sectional study using a population-based telephone survey with random digit dialing.

2.2. Setting

Influenza in China: China is located in the northern hemisphere. The annual seasonality of influenza A epidemics increases with latitude, whereas influenza B activity predominates in colder months throughout most of China. Influenza A epidemics peak in January–February in Northern China and April–June in the southernmost regions [13]. With reference to the WHO standard ILI case definition, body temperature ≥38 °C with either cough or sore throat was used in the survey [14].

2.3. Study Population and Sampling

To account for differences in influenza seasonality and economic development status, six provinces, three in northern China and three in southern China, were selected for the telephone survey (Figure 1).

Figure 1.

Figure 1

Map of the six selected provinces in the influenza-like illness survey in China, 2017/2018.

A representative sample population in the six provinces was reached via stratified random sampling, which was based on different ILI attack rates among different age groups. The sample size of different age groups by province was calculated on the basis of an expected ILI prevalence of 5% in adults ±2.5%, and an expected ILI prevalence of 20% in children ±5%. A minimum sample size of 9438 participants with specific amounts of each age group was required to precisely represent age-specific ILI prevalence in each location. All respondents were recruited randomly. Family members of targeted individuals under 15 years and those over 60 years of age answered the survey questions on their behalf.

All survey respondents reached through telephone calls who agreed to participate and completed the telephone survey were included in the study. A total of 43,636 random telephone calls were made with an answer rate of 49.6% (21,658/43,636), of which 10,045 were willing to participate and successfully finished the questionnaire and met the requirement of five months’ residency in the study location (Figure 2).

Figure 2.

Figure 2

Flowchart of influenza-like illness reported in a telephone survey in six provinces of China, 2017/2018.

2.4. Data Collection

The cross-sectional survey was performed by provincial 12320 Health Hotline Centers via the government health hotline to collect data during the October 2017 to March 2018 influenza season. The survey was conducted during March to May 2018 and the survey questionnaire included demographic information, ILI symptoms, attitude toward vaccination and protection awareness, and healthcare-seeking behaviors related to ILI symptoms. Survey data collected was double-entered into EpiData, and the data was de-identified for analysis. Phone call surveys conducted were recorded for selective examination in order to ensure the quality of the data.

2.5. Analysis and Statistics

Post-hoc tests, chi-square tests for goodness of fit and for trend, and logistic regression were performed using R version 3.0.1 (R Foundation for Statistical Computing, Vienna, Austria) to compare ILI rates, vaccination willingness, prevention awareness, and healthcare-seeking behaviors among different demographic groups. Significance was assigned at 5% (p < 0.05).

2.6. Ethics Approval and Consent to Participate

Study ethics was approved the Institutional Review Board of the Chinese Center for Disease Control and Prevention (no. 201805) and the data are de-identified for protecting personal privacy. All survey respondents who agreed to participate and completed the telephone survey were included in the study.

2.7. Availability of Data and Materials

The datasets generated and analyzed during this study are not publicly available due to the institute’s data security and sharing policy, but are available from the corresponding author on reasonable request.

3. Results

Among the 10,045 enrolled individuals, 2834 self-reported suffering from influenza like illness, with a winter prevalence of 28% (2834/10,045) (Table 1). The proportion of self-reported influenza-like illness (ILI rate) in Yunnan, Inner Mongolia, and Beijing was above the overall average ILI rate (28%). In economically developed urban metropolises, such as Guangdong (mainly Guangzhou), Shanghai, and Beijing, the proportion of self-reported influenza-like illness increased from 17% to 32% as latitude increased. The influenza-like illness rate of those under age 5 (43%) and those aged 5–14 (40%) were significantly higher than the overall ILI rate. The ILI rate also increased significantly as household income increased (p < 0.005) (Table 1).

Table 1.

Demographic characteristics of individuals targeted in a telephone survey in six provinces of China, October 2017 to March 2018.

Characteristic N % Number of Self-Reported ILI * Symptoms ILI Rate % p-Value
Province
Beijing 1573 16 502 32 <0.001
Shanghai 1583 16 427 27
Guangdong 1754 17 291 17
Inner Mongolia 1684 17 544 32
Gansu 1859 19 525 28
Yunnan 1592 16 545 34
Age
0–4 1977 20 842 43 <0.001
5–14 2185 22 868 40
15–24 1657 16 330 20
25–59 2155 21 424 20
60+ 2067 21 369 18
Missing 4 < 1 1 25
Household Income (CNY)
Below 5,000 2137 21 582 27 0.004
5000–9999 2519 25 761 30
10,000–19,999 2019 20 622 31
20,000 and above 1216 12 385 32
Missing 2154 21 484 22
Total 10,045 100 2834 28

* ILI: influenza-like illness.

3.1. Knowledge and Attitudes toward Influenza Infection and Prevention

Among the 10,045 enrolled individuals, 75% (7564/10,045) reported knowing influenza is different from a common cold and 82% (8241/10,045) reported knowing influenza could cause severe consequences such as hospitalization and severe complications, even death. A total of 72% of enrolled individuals would recommend influenza vaccination to their family members. To be noted, individuals with awareness of a difference between influenza and common cold (odds ratio of 1.58 with 95% CI 1.35 to 1.86) and those with awareness of severe consequences caused by influenza (odds ratio of 1.70 with 95% CI 1.42 to 2.04) were found to be more likely to recommend their family members to be vaccinated for influenza in comparison with those who are not aware of these knowledge (both p < 0.001). In addition, people with higher education (junior college, undergraduate, and above) were found to be significantly more likely to recommend their family members to be vaccinated (p < 0.001), whereas household income was found to not significantly impact attitudes towards influenza vaccination.

Prevention awareness, including hand washing, mask wearing, and self-segregation when one has ILI symptoms, was over 70%; Beijing and Shanghai were found to have the highest prevention awareness. The overall self-reported hand washing rate was found to be 79% (range of 74–83%), and hand washing awareness in urban cities was found to be significantly higher than other provinces. The overall self-reported mask wearing rate and self-segregation rate was found to be 75% (range of 64–84%) and 72% (range of 63–80%) (Table 2). Males were found to have higher prevention awareness than females, and prevention awareness increased significantly with higher income level (p < 0.001) and education level (p < 0.001). Healthcare professionals had the highest prevention awareness, whereas full-time students were found to be the least likely to be aware of the need for self-segregation (Table 2).

Table 2.

Influenza prevention awareness of telephone survey respondents in six provinces of China, October 2017 to March 2018.

Prevention Method Washing Hands * Wearing Mask * Self-Segregation *
Number Responding Number Responding Yes % p-Value Number Responding Number Responding Yes % p-Value Number Responding Number Responding Yes % p-Value
Province
Beijing 1573 1306 83 <0.001 1573 1318 84 <0.001 1573 1255 80 <0.001
Shanghai 1580 1312 83 1579 1262 80 1581 1201 76
Guangdong 1754 1423 81 1754 1125 64 1754 1231 70
Yunnan 1553 1210 78 1559 1195 77 1522 1006 66
Gansu 1858 1444 78 1858 1423 77 1857 1386 75
Inner Mongolia 1678 1247 74 1679 1183 70 1679 1149 68
Sex
Female 4461 3332 75 <0.001 4466 3056 68 <0.001 4448 3002 67 <0.001
Male 5501 4581 83 5502 4421 80 5484 4201 77
Missing 34 29 85 34 29 85 34 25 74
Education
Elementary School and below 388 243 63 <0.001 389 191 49 <0.001 381 186 49 <0.001
Middle school 974 698 72 979 610 62 971 639 66
High school 1782 1380 77 1785 1255 70 1777 1210 68
College and above 6674 5492 82 6672 5324 80 6660 5077 76
Missing 178 129 72 177 126 71 177 116 66
Occupation
Farmer 385 233 61 <0.001 387 228 59 <0.001 376 219 58 <0.001
Company and enterprise employee 2978 2392 80 2980 2256 76 2976 2197 74
Government official 1826 1470 81 1829 1441 79 1824 1383 76
Full-time student 570 415 73 569 415 73 566 345 61
Housewife 385 323 84 386 289 75 384 299 78
Healthcare professional 808 735 91 808 747 92 808 698 86
Unemployed 250 180 72 250 161 64 250 158 63
Retired 887 690 78 887 535 60 884 580 66
Other 1453 1141 79 1452 1094 75 1448 1034 71
Missing 454 363 80 454 340 75 450 315 70
Household Income (CNY)
Below 5000 2110 1586 75 <0.001 2117 1495 71 <0.001 2089 1379 66 <0.001
5000–9999 2508 2017 80 2511 1926 77 2505 1867 75
10,000–19,999 2016 1603 80 2013 1546 77 2011 1486 74
20,000 and above 1215 1013 83 1216 977 80 1214 938 77
Missing 2147 1723 80 2145 1562 73 2147 1558 73
Total 9996 7942 79 10,002 7506 75 9966 7228 73

* The question was phrased so that a yes response meant that if the respondent had influenza-like symptoms they would take the following precautions to prevent the spread of flu: washing hands, wearing a mask, and self-segregation.

3.2. Healthcare-Seeking Behaviors Related to Influenza Infection

Information on healthcare seeking behaviors of individuals targeted in the telephone survey who were reported to have ILI symptoms was investigated (Table 3). Important to note is that Inner Mongolia had the highest rate of healthcare-seeking behaviors for ILI symptoms (96%), whereas Beijing and Shanghai had the lowest (82% and 82%). Hospitalization and seeking medicine from a pharmacy were found to be less frequent in economically developed urban metropolises (Beijing, Shanghai, and Guangdong). The average proportion of hospitalization and seeking medicine from a pharmacy in Yunnan, Gansu, and Inner Mongolia was four times that of economically developed urban metropolises (Beijing, Shanghai, and Guangdong). Compared with other areas, individuals in Yunnan preferred a private clinic/village doctor rather than a municipal hospital for their first visit. Those under the age of 15 and over the age of 60 sought treatment more often and from outpatient/emergency departments; also, they were more frequently hospitalized. As household income increased, treatment-seeking activity decreased significantly (p = 0.013), and the proportion choosing a municipal hospital for their first visits increased dramatically (Table 3).

Table 3.

Healthcare-seeking behaviors of individuals targeted in a telephone survey in six provinces of China, October 2017 to March 2018.

Healthcare-Seeking Behaviors Sought Treatment First Type of Treatment * First Visit Healthcare Facility
Total Yes % p-Value Outpatient/Emergency Hospitalization Medicines from Pharmacy Private Clinic/Village Doctor % Community Health Service Center % County and District Hospital % Municipal Hospital % Do Not Remember %
Province
Beijing 502 412 82 <0.001 367 16 55 11 3 43 10 96 23 227 55 35 8
Shanghai 427 351 82 285 11 90 10 3 28 9 87 29 160 53 17 6
Guangdong 291 255 88 221 11 47 9 4 46 19 40 17 133 56 8 3
Yunnan 545 477 88 248 47 306 158 41 82 21 31 8 92 24 22 6
Gansu 525 451 86 304 51 222 32 9 60 17 57 16 184 53 15 4
Inner Mongolia 544 524 96 353 46 222 64 15 73 17 62 14 210 48 26 6
Age
0–4 842 784 93 <0.001 646 69 211 51 7 78 11 124 17 437 61 24 3
5–14 868 781 90 600 46 266 69 10 111 16 138 20 326 48 42 6
15–24 330 272 82 186 11 137 48 21 52 23 47 20 71 31 12 5
25–59 424 324 76 185 19 162 59 24 46 18 30 12 90 36 26 10
60+ 369 308 83 160 37 165 57 24 44 19 34 14 82 35 19 8
Missing 1 1 100 1 1 0 1 100 0 0 0
Household Income (CNY)
Below 5000 582 522 90 0.013 325 50 262 118 27 96 22 77 18 122 28 20 5
5000–9999 761 681 89 454 52 304 68 12 109 20 93 17 243 44 38 7
10,000–19,999 622 540 87 420 44 175 34 7 60 13 95 20 261 56 20 4
20,000 and above 385 328 85 273 22 82 22 7 33 11 48 16 187 61 15 5
Missing 484 399 82 306 14 119 42 12 34 9 60 17 193 54 30 8
Total 2834 2470 87 1778 182 942 284 13 332 16 373 18 1006 47 123 6

* Multiple responses were allowed, so percentages were not reported and total will not equal the sum of the three options.

3.3. Factors Related to Willingness to Be Vaccinated for Influenza

The overall willingness for influenza vaccination during the 2018/2019 influenza season was found to be 45% (range of 30–54%). Gansu has the largest proportion of individuals with the intention of vaccination against influenza, whereas individuals in Guangdong are the least likely to be vaccinated against influenza for the 2018/2019 influenza season. Individuals with higher education level were found to be more likely to be vaccinated against influenza for the 2018/2019 influenza season than those with a low education level (p < 0.001). Household income was found not to significantly impact one’s influenza vaccination intention for the next influenza season. Government officials and full-time students were more likely to be vaccinated against influenza than individuals of other occupation groups during the 2018/2019 influenza season (p < 0.001).

In addition, 65% of respondents self-reported with the intention of receiving an influenza vaccination on the condition that the influenza vaccine was free, 65% of respondents self-reported with the intention for influenza vaccination on the condition that the influenza vaccine was recommended by their doctors, and 74% of respondents self-reported with the intention of receiving an influenza vaccination on the condition that their employer supported the influenza vaccination (Figure 3). Recommendation from one’s doctor was found to be the most effective factor for increasing the intention for influenza vaccination (odds ratio of 6.48 with 95% CI 5.53–7.60). Cost-free vaccination also had a large effect on increasing intention for influenza vaccination (odds ratio of 5.33 with 95% CI 4.54–6.25), followed by employer’s support for influenza vaccination (odds ratio of 2.23 with 95% CI 1.85–2.68).

Figure 3.

Figure 3

Figure 3

Influenza vaccination attitudes of telephone survey respondents during the October 2017 to March 2018 influenza season in six provinces of China. Panel (A) Willingness for influenza vaccination during the 2018/2019 influenza season in China; Panel (B) Willingness for influenza vaccination during the 2018/2019 influenza season on the condition that the influenza vaccine was recommended by their doctors; Panel (C): Willingness for influenza vaccination during the 2018/2019 influenza season on the condition that the influenza vaccine was free; Panel (D): Willingness for influenza vaccination during the 2018/2019 influenza season on the condition that their employer supported the influenza vaccination; Panel (E): Willingness for recommendation of influenza vaccination to one’s family members influenza vaccination during the 2018/2019 influenza season.

4. Discussion

Population-based estimates of seasonal ILI are important sources of information for determining the total burden of disease. This study used population-based data from six provinces of China representing both high population density urban districts and low population density rural districts, and used a representative sample across age ranges, the influenza-like illness rate of individuals under age 14 were significantly higher than other age groups [15]. High prevention awareness overall was identified, especially among the healthcare professionals, and the varying levels of willingness to be vaccinated illustrates the need for improved communication strategies that accurately reflect an individual’s risk for contracting seasonal influenza.

The high level of awareness of a difference between influenza and common cold and potential severe consequences caused by influenza virus infection may explain their attitudes towards influenza vaccination recommendation to their family members and the high prevention awareness. Individuals with New Rural Cooperative Medical Insurance for Rural Residents (NRCMIRR) may be reimbursed if they are vaccinated, which may account for the highest intention to vaccinate in Gansu [10]. Low willingness to vaccinate may result from individuals’ underestimation of their risk of contracting influenza and a lower ILI epidemic of the previous influenza season in their community [16].

Although overall prevention awareness was relatively high across all provinces studied, information, education, and communication (IEC) strategies could be targeted to the populations found to have lower awareness in this study, for instance, those with limited education and low household income who may be at increased risk for infection [17,18]. As household income does not significantly impact the influenza vaccination willingness and recommendation influenza vaccination to family members, thus IEC strategies for increasing vaccination rates should incorporate doctor’s recommendations and support from one’s employer. A policy of free influenza vaccinations for high-risk populations could also improve uptake.

Additionally, IEC campaigns that inform the public of the true estimated number of cases each year and the negative economic impacts illness has on individuals, families, and the economy as a whole may improve willingness to vaccinate, alongside expansion of free or subsidized vaccination programs. Further research is needed to estimate the cost of influenza morbidity and mortality to justify whether or not a nationwide vaccination program for key populations would improve vaccination coverage significantly [10].

The influenza seasons lasts longer with increasing latitude [19], and the influenza virus circulation patterns in the north and south of China are different [13,20]. Our results showed that the proportion of self-reported ILI in urban metropolises increases as latitude increases, which might indicate influenza transmission patterns are different in urban and rural areas as latitude increases.

The collected data may have a selection bias and recall bias, as telephone respondents were randomly selected by the 12320 Health Hotline and were asked about self-report health information. The elderly, unemployed individuals, and those who work at home may be more likely to be involved in telephone survey. Individuals are prone to focus on health issues via the 12320 Health Hotline and thus may not be representative for all members of the population of interest. However, because of the high rate of treatment-seeking for the study population (87%) and the fact that respondents were only asked to refer back to the current influenza season, recall bias may be limited. Missing data, though minimal, and respondents’ ability to refuse participation may have impacted study findings. In addition, the individuals may have confused the influenza vaccine and haemophilus influenza type B (Hib) vaccine, which could result in higher self-reported influenza vaccination willingness. Individuals may be not ideally randomized and be skewed to those who are more often available for the 12320 Health Hotline at the time the calls were made.

The strengths of this study included random digit dialing to obtain population-based estimates of ILI by age and provided a large representative sample of the population in the six provinces. The study also adhered to the strengthening the reporting of observational studies in epidemiology (STROBE) guidelines for observational research [21].

5. Conclusions

ILI prevalence in different groups differed significantly by age and geographical location/population density. Vaccination willingness was positively associated with higher education level, recommendation from doctors, cost-free vaccination, and support from employers. Vaccination policy should encourage key populations at the highest risk to vaccinate, and should be accompanied by awareness- and willingness-raising campaigns that promote the benefits of vaccination, reduce barriers to vaccination such as cost, and provide information on the risk of influenza for all age groups via healthcare professionals. Additionally, campaigns should promote and educate the population on prevention strategies for women, low-income households, full-time students, and those with low levels of education.

Acknowledgments

We thank the staff members of the 12320 Health Hotline Center in China CDC, Beijing, Shanghai, Guangzhou, Yunnan, Inner Mongolia, and Gansu, for their valuable assistance in survey data collection. Zhongjie Li had full access to all the data in the study and had final responsibility for the decision to submit the manuscript for publication. The views expressed are those of the authors and do not necessarily represent the policy of the Chinese Center for Disease Control and Prevention.

Author Contributions

Conceptualization, L.F., Y.Q., M.G., L.Z., B.J.C., and Z.L.; data curation, K.T.; formal analysis, X.R. and M.G.; funding acquisition, E.G., L.W., B.J.C., and Z.L.; investigation, X.R.; methodology, J.F., Y.Q., P.W., and S.Z.; project administration, X.R. and K.T.; resources, L.F., P.W., L.Z., B.J.C., and Z.L.; software, Y.Q.; supervision, L.W., B.J.C., and Z.L.; validation, S.Z.; visualization, X.R.; writing original draft, X.R., E.G., and B.J.C.; writing, review and editing, X.R., E.G., L.W., J.F., S.Z., J.Y., B.J.C., and Z.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by grants from the National Natural Science Foundation of China (NSFC) (no. 91846302), China Ministry of Science and Technology (grant no. 2018ZX10713001), and China CDC’s Key Laboratory of Surveillance and Early-Warning on Infectious Disease. The funding bodies had no role in study design, data collection and analysis, preparation of the manuscript, or the decision to publish. Open access publication costs will be covered by China CDC under the SORT IT program in Special Programme for Research and Training in Tropical Diseases (WHO/TDR).

Conflicts of Interest

B.J.C. has received research funding from Sanofi Pasteur and MedImmune Inc. for studies of influenza vaccination effectiveness. The authors who have taken part in this study declared that they do not have any other potential conflicts of interest.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated and analyzed during this study are not publicly available due to the institute’s data security and sharing policy, but are available from the corresponding author on reasonable request.


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