Knowledge, Attitude, and Practice towards Influenza Vaccination among Older Adults in Southern China during the COVID-19 Pandemic

Influenza is prevalent globally, leading to severe morbidity and mortality. During the pandemic, knowledge, attitude, and practice (KAP) towards influenza virus and vaccination were less investigated among southern Chinese older adults. A cross-sectional study was conducted through the structured questionnaire among community healthcare centers in selected districts in Shenzhen, southern China from September to October 2021. KAP towards influenza virus and vaccination were analyzed. A multivariable logistic regression model was used to identify associated factors. Among 975 participants, 55.6% were reported to have received influenza vaccination ever, and 46.6% had taken influenza vaccination in 2020 during the pandemic. Only one-fifth of participants knew severe comorbidities happen among severe influenza cases. A total of 88.3% thought older adults should have influenza vaccination. COVID-19 vaccination history was associated with receiving influenza vaccination (OR 1.92, 95% CI 1.32–2.80). People with a high-level income had better KAP towards influenza virus and vaccination. COVID-19 vaccination history was associated with the positive actions of influenza vaccination during the pandemic. Efforts should be made to promote the free influenza vaccination program widely and launch health education events on influenza and its vaccination regularly to improve KAP among older adults.


Introduction
Influenza is prevalent globally, leading to severe morbidity and mortality [1,2]. It is estimated that worldwide influenza causes approximately 3 to 5 million cases of severe illness and up to 650,000 respiratory deaths every year [2]. Older adults and people with chronic physical conditions are deemed to be at an increased risk of infection and hospitalization due to influenza [2]. In China, it was estimated that roughly 80% of the excess respiratory deaths attributed to influenza were among people aged 60 years or above between 2010 and 2015 [1,3]. With the evolution of the circulating influenza virus, annual vaccination is recommended as the most effective tool to protect against influenza, as immunity is not lifelong [4,5]. WHO recommends the composition of the trivalent vaccine that targets the three most representative virus types in circulation (two subtypes of influenza A viruses and one influenza B virus) [2]. Hence, launching the influenza vaccination program among older adults is a significant approach to alleviating the influenza disease burden.
With the implementation of national medical reform in China in 2009, vaccination services were provided through community health centers (CHCs), including vaccines for influenza, hepatitis B, human papillomavirus, COVID-19, etc. [6,7]. People of all ages can have influenza vaccine uptakes with their out-of-pocket money of 11 to 49 US dollars (76-334 Chinese Yuan) yearly at widely distributed CHCs in urban areas. During the COVID-19 period, since March 2021, the Chinese government has started to offer the 2. 1

. Study Design and Participants
From 24 September to 20 October 2021, a cross-sectional survey was conducted on the demographic and socioeconomic information, disease and vaccination history, and KAP regarding influenza virus and vaccination in Shenzhen, China. Shenzhen is located in southern China, being one of the first-tier cities with more than 17 million residents. There are 10 districts with more than 700 community health centers in Shenzhen. Ten CHCs in two large districts (Nanshan and Guangming) of Shenzhen were randomly selected as our study sites.
Participants were included through convenient sampling in our study if they (1) were aged 60 years old and above before September 2021; (2) attended the above-included CHCs; and (3) were willing to complete the questionnaire. Considering the feasibility of the study design and the strong mobility of the population in the mega city of Shenzhen, as many participants were included as possible. Overall, 993 older adults were enrolled in our study. Of them, 975 participants had complete information and were valid for data analyses. A total of 18 participants were excluded because they did not state their influenza vaccination status, which was conducted as our primary outcome.

Data Collection
Trained interviewers administered the structured questionnaire to included participants, asked questions from the questionnaire to each participant, and wrote down the answers in person. Before this questionnaire was made available to all participants, a pilot study was conducted on a small sample of older participants (N = 30) to ensure that the questionnaire was easily understandable and completed. The structured questionnaire consisted of detailed questions on demographic and socioeconomic characteristics, health conditions, KAP on influenza and its vaccination, as well as health education on vaccination.
Demographic and socioeconomic characteristics were measured by sex (female and male), age (60-64, 65-75, and above 75 years old), education level (primary school and below, middle and high school, and college and above), marital status (unmarried and married), and monthly income (1000 and below Chinese Yuan (CNY), 1001-5000, and 5001 and above). Health conditions were assessed by self-awareness of health status (well, general, and worse), chronic disease history (yes and no), and COVID-19 vaccination history (yes and no).
The KAP questionnaire was a part of the structured questionnaire, including knowledge, attitude, and practice towards influenza virus and vaccine. The knowledge survey included influenza virus and vaccine items that were measured by influenza symptoms, prevention measures, vaccination-prioritized populations, vaccination frequencies, vaccination season, vaccine protection duration, the places to get vaccinated, and if they ever knew about influenza vaccine and vaccination policy. The attitude survey included opinions on whether older people and people with chronic diseases should have influenza vaccine uptake and thoughts about vaccination education. The practice survey included cues to actions, vaccine actions, and reasons for being unwilling to receive influenza vaccines. Cues to action consisted of recommendations from healthcare workers, previous vaccination awareness of people around, and participation in vaccine education programs. Actions included self-reported influenza vaccination history before the interview time and in the specific 2020 influenza season. Participants being stratified by influenza vaccination history at that time were categorized as vaccinated status and unvaccinated status as our primary outcome. In addition, participants stratified by influenza vaccination history in the 2020 influenza season were categorized as vaccinated status and unvaccinated status in 2020.

Statistical Analysis
Statistical analysis was performed with Stata version 17 (StataCorp Inc., Chicago, IL, USA). All categorical variables were described with frequencies (N) and percentages (%). Frequencies and proportions were used to describe the detailed information on knowledge of the influenza virus and vaccine (9 survey items), attitude towards influenza vaccination and its education program (3 survey items), and practice of influenza vaccination (6 survey items). The Chi-square test was used to evaluate the differences in knowledge, attitude, and practice towards influenza virus and vaccination between subgroups, with analyses stratified by age groups, education levels, and income levels. Statistically significant survey items among age groups, education levels, and income levels were included in the following multivariable logistic regression model to identify influenza-associated factors. Demographic and socioeconomic factors stratified by previous actions of influenza vaccine with a p value < 0.05 in the Chi-square test were further included in the same multivariable logistic regression model, where fully adjusted odds ratios (ORs) and their corresponding 95% CI were calculated after controlling for other covariates and associated factors.
Subgroup analysis was conducted among participants who reported as vaccinated in 2020. Statistically significant survey items among age groups, education levels, and income levels were included in the following multivariable logistic regression model to identify influenza-associated factors. Demographic factors stratified by ever received actions of influenza vaccine in 2020 with a p value < 0.05 in the Chi-square test were further included in the same multivariable logistic regression model, where ORs and 95% CIs were calculated. A two-sided p < 0.05 was considered statistically significant in multivariate analyses.

Ethical Statement
Our study was approved by the Shenzhen Center for Disease Control and Prevention. Oral informed consent was obtained from each participant before interviewers administered and distributed the structured questionnaire.

Characteristics of Participants
A total of 975 older participants were included in this analysis. In Table 1, it can be seen that more females (56.3%) than males (43.7%) were involved in this analysis. The mean age of participants was 69.4 years old, with a standard deviation of 6.4 years old, and 575 (59%) were between 65 and 75 years old. In total, 823 (87.4%) were married and more than half of the participants had middle and high school diplomas, followed by primary school and below. Overall, 429 (44.0%) had middle-income levels of 1000 to 5000 Chinese yuan (CNY), 592 (60.7%) considered their health well and 441 were diagnosed with chronic medical conditions by a doctor before, and 813 (83.4%) had received COVID-19 vaccine uptakes since the breakout of COVID-19 at the beginning of 2020.

Knowledge of Influenza Virus and Vaccination
In Table 2, only one-fifth of participants (N = 214) knew severe comorbidities would happen among severe cases affected by the influenza virus. Most participants knew about vaccination as the approach to protecting against influenza. In total, 75.6% thought people aged 60 years old and above, children aged 6 months to 5 years old, and patients with chronic conditions were the prioritized populations to take influenza vaccine uptakes, but only 13.1% knew that women who were pregnant or planned to become pregnant during flu season should take influenza vaccination. Overall, 64.2% participants knew the influenza vaccination frequency (once a year), 58.4% knew the influenza vaccination time frame (in autumn and winter), 58.4% knew the protection duration (six to eight months), and 74.1% knew the places to take influenza vaccination. Over 70% of participants have heard about influenza vaccination and knew about the free influenza vaccination program in Shenzhen. a The details of answers for "Q3. Who are the prioritypopulations that need to take influenza vaccination?" are shown below: healthcare workers, including clinicians, public health staff, and health and quarantine staff; vulnerable groups and employees include people in places where people gather, such as elderly care institutions, long-term care institutions, and welfare homes; people in key places include nursery institutions, primary and secondary schools, and prison institutions; risky populations include older people aged 60 and above, children aged 6 months to 5 years, and patients with specific chronic diseases; infants' caregivers include family members and caregivers of infants aged under 6 months; pregnant women include women who are pregnant or planning to become pregnant during flu season. b "Once a year" is the correct answer for Q4. c "In autumn and winter" is the correct answer for Q5. d "6-8 months" is the correct answer for Q6.
Most older people knew about vaccination as the method to prevent the influenza virus, the protection duration of influenza vaccine, and the places to take vaccination (p < 0.05 in three survey items in Table 3). Compared with participants with primary school or above education, participants with higher education levels had better knowledge of influenza symptoms, prioritized populations, vaccination frequency, places, protection duration, as well as vaccination policy (p < 0.05 for most survey items in Table 3). So did people who have higher monthly income (p < 0.05 for most survey items). The differences in vaccine protection duration and places existed in each age group, educational level, and income level (p < 0.05 in three subgroups).

Attitude towards Influenza Vaccination and Education Program
In Table 4, 861 (88.3%) participants thought older adults should take influenza vaccination and over half considered that older adults with chronic medical conditions were bound to take the vaccination. A total of 652 (65.9%) thought it beneficial to participate in the vaccination education program.
Most participants (58.9%) between 65 and 74 years old thought older adults diagnosed with chronic conditions should take influenza vaccination compared with the other two age groups (20.9% vs. 58.9% vs. 20.2%, p = 0.010 in Table 5). People with middle and high school education or middle level of income had a more positive attitude towards influenza vaccination and education programs, showing more agreement in three survey items (p < 0.05 in Table 5). The differences in attitudes towards vaccination among older adults with chronic diseases existed in each age group, educational level, and income level (p < 0.05 in three subgroups).  a p value is calculated from a Chi-square test. b The details of answers for "Q3. Who are the priority populations that need to take influenza vaccination?" are shown below: healthcare workers, including clinicians, public health staff, and health and quarantine staff; vulnerable groups and employees include people in places where people gather, such as elderly care institutions, long-term care institutions, and welfare homes; people in key places include nursery institutions, primary and secondary schools, and prison institutions; risky populations include older people aged 60 and above, children aged 6 months to 5 years, and patients with specific chronic diseases; infants' caregivers include family members and caregivers of infants aged under 6 months; pregnant women include women who are pregnant or planning to become pregnant during flu season. c "Once a year" is the correct answer for Q4. d "In autumn and winter" is the correct answer for Q5. e "6-8 months" is the correct answer for Q6. f The number inside of brackets indicates percentages and outside of brackets indicates frequency.

Practices of Influenza Vaccination
In Table 6, cues to actions of influenza vaccination included three items as follows: 653 (67.0%) participants were recommended the influenza vaccination by healthcare workers, but 542 (55.6%) reported to have received influenza vaccination and 454 (46.6%) have taken influenza vaccine uptakes in 2020 during the COVID-19 period. Around 60% of participants heard about people around who have taken influenza uptakes. One-third of participants have ever taken part in health education programs. In Table 7, additionally, the associations of vaccinated people around previous vaccination status and vaccination status in 2020 differed by age, education, and income levels (p < 0.05). Participants among 65 to 74 years old, holding middle and high school diplomas, or with higher income levels, were reported to have received influenza vaccination and taken influenza vaccine uptakes in 2020 (p < 0.05).

Reasons for Being Unwilling to Receive the Influenza Vaccines
Among 433 participants who reported not receiving influenza vaccination before, their reasons for being not vaccinated are presented in Table 6. The top three reasons were as follows: participants reported that they did not know about influenza vaccination (43.0%); they thought they stayed in good conditions and there was no need to take the influenza vaccine (27.5%); and they had no time to take the influenza vaccine (12.5%). It is worth noticing that only 2.8% of participants thought the influenza vaccine had no effect. Only 24 (5.5%) participants did not have the influenza vaccine because physicians have not ever recommended it, and another 23 (5.3%) considered it too much cost.

Multivariate Analysis
Using the actions of influenza vaccination as the primary outcome, a multivariate analysis was conducted to determine what variables were associated with our primary outcome. The differences in influenza vaccination status existed in knowledge items of influenza vaccination protective duration, the places to have influenza uptakes, and attitudes towards whether older adults with chronic conditions should take influenza vaccination. In Table 8, compared with younger participants less than 65 years old, participants aged above 65 years old were at higher odds of being vaccinated, with the odds ratio of 1.46 (95% CI 1.02-2.10) for the 65-75 age group and the odds ratio of 1.81 (95% CI 1.10-2.98) for the above 75 age group. Marital status and education levels were not associated with influenza vaccinated status after adjusting for other significant influenza-associated factors. Participants who had a high-level monthly income were associated with higher odds of being vaccinated (5001 and above CNY: OR 2.64, 95% CI 1.66-4.18). COVID-19 vaccination history was not statistically significantly associated with our primary outcome of previous vaccination status before the year 2020. Participants who answered correctly on vaccination protection duration were associated with having influenza vaccine uptakes (OR 2.76, 95% CI 1.99-3.84). Participants who knew about the places of vaccination were associated with the vaccinated status (OR 5.00, 95% CI 3.42-7.32). Moreover, participants who thought older adults with chronic conditions should take influenza vaccination were associated with having vaccination (OR 2.08, 95% CI 1.51-2.85).

Subgroup Analysis
In subgroup analysis, another multivariate regression model stratified by the actions of the influenza vaccine in 2020 was conducted. Identified influenza-associated factors were similar to the results stratified by previous actions of influenza vaccination, but during the COVID-19 period, COVID-19 vaccination history was associated with receiving influenza vaccine uptakes (OR 1.57, 95% CI 1.05-2.37). Participants who had a high-level monthly income were associated with higher odds of being vaccinated (5001 and above CNY: OR 1.69, 95% CI 1.10-2.61). Participants who answered correctly on vaccination protection duration were associated with having influenza vaccine uptakes (OR 2.15, 95% CI 1.58-2.93). Participants who knew about the places of vaccination were associated with the vaccinated status (OR 4.22, 95% CI 2.85-6.24). Moreover, participants who thought older adults with chronic conditions should take influenza vaccination were associated with having vaccination (OR 1.73, 95% CI 1.27-2.35).

Discussion
A cross-sectional survey was conducted to evaluate the knowledge, attitudes, and practices toward influenza virus and vaccination among 975 Chinese older adults aged 60 years and above and identify influenza vaccination-associated factors from September to October 2021 in southern China. The vaccination coverage was 55.6% among our participants. People with a higher education or income level had a better performance of knowledge, attitude, and practice towards influenza virus and vaccination. People with higher income levels and better knowledge and attitude were associated with the positive actions of influenza vaccination.
As a result of complex and diverse vaccination policies being implemented in different cities in China, the vaccination coverage rate showed differences among older populations, for example, 55.6% in this study, being much higher than those of previous studies among older adults, ranging from 4.3% to 40.0% [20], but lower than that of the US in 2022 [21]. This difference might be attributed to the fact that people living in Shenzhen are provided with fruitful medical resources and health information offerings from the high-quality primary healthcare system supported by the municipal government [22]. Additionally, evidence showed that health literacy was apparently higher among people in Shenzhen compared with the Chinese average level, which referred to the ability and basic diathesis to acquire and use health information and make health-associated associations, for example, vaccination in the present study [23,24]. Statistically significant influenza-associated factors in knowledge and attitude survey items were identified, which showed that people having sufficient and correct knowledge as well as positive attitude towards influenza vaccination were associated with having vaccination. However, four-fifths of participants were not aware of the occurrence of severe comorbidity, which made people look down upon influenza. A large proportion of them did not know pregnant women as one of the risky populations of infection, which potentially poses a threat to pregnant women and their babies. This reflected the knowledge barriers among our participants. Appropriate health education programs are urgently needed among older adults.
Previous studies focused on healthcare professionals, pregnant women, and travelers in different regions with the impact of vaccination policies [14,16,17]. Evidence showed that an appropriate vaccination policy indeed has a positive impact on the coverage rate [25], which indicated that a free vaccination policy might attract more attention. The study site, Shenzhen, as the first-tier city in China, has already provided free influenza vaccination among older permanent residents aged 60 years or above for 7 years. Previous studies also proved a positive influence on influenza vaccination coverage under the launch of free influenza vaccination programs for older adults [26]. Vaccination policy was considered one of the most significant vaccination-related factors [27]. Our study also affirmed this factor, stating that older adults who ever knew about the free vaccination program were associated with having the influenza vaccine uptake. This beneficial policy should be generalized among other capable cities to improve influenza vaccination coverage among older adults.
Almost 90% of participants agreed that older adults should take influenza vaccination, but only half of our participants had influenza vaccine uptakes before. The older partici-pants who were less educated were associated with not having influenza vaccination in this study compared with participants with higher education levels. It is consistent with previous studies, indicating that people with low literacy might ignore written information [28], for example, leaflets and posters on free influenza vaccination in CHCs. However, older participants with higher education or income levels in this study knew more about older adults who had influenza vaccination before. It is possible that they were influenced to have vaccine uptakes by their acquaintances, that is, the acquaintance effect. This factor needs to be explored in vaccination studies further.
The popularity of influenza vaccination was limited to some degree because almost half of the unvaccinated participants reported they did not know about the vaccination program as the top reason. This indicated that the influenza vaccination program should strengthen promotion among the public mass. A small proportion of people considered themselves healthy enough for it to be unnecessary to have influenza uptakes, which was the second reason. This demonstrated the misunderstanding of susceptible populations regarding influenza virus and the necessity of vaccination education programs widely and regularly. Despite the shortages of vaccination programs, a few people thought the influenza vaccine had no effect, which indicated that vaccination education played an important role in improving vaccine-associated knowledge. Several participants mentioned that they were not recommended to have influenza vaccine uptakes by their physicians, but recommending vaccination was supposed to be their work responsibility in our previous studies [26]. This reflected deficiencies in physicians' work to some degree.
COVID-19 vaccination history was found to be associated with influenza vaccination in 2020, which might be due to their good level of perception on both viruses and their vaccines, being consistent with a cross-sectional study focusing on the knowledge related to COVID-19 among the Italian elderly [18]. During the 2020 flu season with the pandemic, many people perceived the COVID-19 virus as the influenza virus mistakenly because of their similar symptoms, and people were willing to have influenza vaccination when there was no COVID-19 vaccine approved. Our findings suggested that participants with higher education and income levels are associated with having influenza vaccine uptake. Moreover, health and vaccine information on COVID-19 was gradually promoted widely and deeply during the pandemic [29]. The promotion of influenza education cannot reach the point of COVID-19, obviously. Nowadays, with the decreasing cases of COVID-19 daily, the new cases of type A influenza have started to increase and the positive rate is up to 25.1% [30]. Hence, it is urgent to promote influenza and influenza vaccination-related information in China, especially for older adults.
Physicians were reported as a significant factor in multiple studies [15,31]. In our study, similarly, 67% of participants were recommended the influenza vaccination by healthcare workers, and only a few participants stated their un-vaccination status was due to no recommendation from professionals, but half of them were influenza vaccinated. Hence, providing recommendations from professionals is the most convenient and reliable method to improve the influenza vaccination-associated information as well as coverage rate. However, vaccine hesitancy existed among both patients and healthcare professionals. Patients worry about the inefficacy of vaccines and the fear of adverse effects [32]. Professionals may have concerns about the responsibility of medical accidents if an allergy reaction or severe side effects appear after patients' follow the recommendation of vaccination from them, which needs further investigation as to the reason for not recommending vaccination. Hence, to eliminate vaccine hesitancy, proper and correct vaccination education is needed among healthcare professionals and patients regularly.
Several limitations of this study must be acknowledged. First, recall bias might exist when responding to past experiences. For example, previous vaccination status as our primary outcome was self-reported. Second, considering that the sample was from Shenzhen, where adults aged 60 and above take the proportion of 5.36% (0.95 million), compared with the national average of 18.7% [33,34], our study results might not be generalized to other Chinese cities. Moreover, Shenzhen, as one of four first-tier super cities with the top gross national product in China, is capable of offering financial support for multiple vaccination programs for specific populations. Hence, other governments should tailor their vaccination policy. Third, selection bias might exist, as only participants who visited the included CHCs were included. Fourth, because of the nature of study design, this survey was conducted at the beginning of the influenza season and the attitudes and practices only reflected the information available at a certain point. The actual KAP may have changed after our study period. Future study is needed to assess the KAP towards influenza virus and vaccination among risky populations after the COVID-19 pandemic for further vaccination policy making.

Conclusions
In conclusion, our study provided valuable insights into the free influenza vaccination policy, which played a significant role in improving vaccination coverage. A relatively high vaccination coverage was found among older adults in Shenzhen. People with higher income levels had a better performance of knowledge, attitude, and practice towards influenza virus and vaccination. COVID-19 vaccination history was associated with the actions of influenza vaccination during the pandemic. Therefore, more actions from the government should be taken to improve influenza vaccination coverage among older adults through providing health education regularly to improve knowledge and attitudes and delivering wide promotion of the free influenza vaccination program to facilitate older adults' practices.  Data Availability Statement: Data will be made available on request.