Characteristics and factors of repeated influenza vaccination among elderly individuals in Shanghai, China from 2020 to 2022

ABSTRACT

Elderly individuals face a high risk of hospitalization and death related to influenza, thus prioritizing them for influenza vaccination. Due to variations in the influenza virus and waning protective antibodies, annual influenza vaccination is recommended. However, research on repeated influenza vaccination among elderly individuals in China is limited. From 2020 to 2022, the average influenza vaccination coverage among registered elderly individuals in Shanghai was 4.1%, showing a declining trend over time. In 2020, the rate of repeated influenza vaccination among elderly individuals was 28.35%, which rose to almost two-thirds both in 2021 and 2022. No increased risk of adverse events following immunization was observed after repeated influenza vaccination during this period. Our study also found that elderly individuals with Shanghai household registration, managed by community clinics, and older age tended to receive more doses of repeated influenza vaccination throughout the period from 2020 to 2022. Increasing influenza vaccine coverage among elderly individuals in Shanghai is both urgent and challenging. Health authorities should intensify educational and promotional campaigns to encourage uptake of annual repeated influenza vaccination among elderly individuals.

KEYWORDS:

• Influenza vaccines
• vaccination coverage
• repeated vaccination
• safety
• COVID-19

Introduction

Influenza, an acute respiratory infectious disease caused by the influenza virus, poses a significant health threat worldwide, with up to 650,000 influenza-associated respiratory deaths estimated each year.¹ According to a systematic literature review, elderly individuals face a higher risk of influenza-associated hospitalization, intensive care unit admission, and mortality.² A study in China revealed that 71,000 individuals aged 60 and above die from influenza-related respiratory diseases annually, accounting for 80% of the excess mortality cases.³ The global aging population is rapidly increasing, with projections suggesting that by 2025, China will have over 300 million individuals aged 60 and above, comprising more than 20% of the population.⁴ This imposes a significant burden of influenza-related respiratory disease on China. Influenza vaccination is an effective measure to prevent the disease, reducing the burden of severe illness and death associated with it.⁵ The World Health Organization’s “Position Paper on Influenza Vaccines” recommends prioritizing elderly individuals for influenza vaccination.⁵

Due to the high likelihood of influenza virus mutation and the rapid decline in antibody levels induced by influenza vaccination over time, it is necessary to receive influenza vaccines annually.^5–7 Aging reduces antibody responses to both the influenza virus and the vaccine, highlighting the importance of annual influenza vaccination for elderly individuals.⁸ Several studies have confirmed that factors such as age, medical stability, health status, social interaction, cognitive decline, and smoking can influence elderly individuals’ decisions to receive influenza vaccination.⁹ Additionally, factors such as education level, place of residence, confidence in vaccine safety, perception of disease risk, and awareness of the importance of influenza vaccination impact vaccine hesitancy in elderly individuals.¹⁰ The benefits of seasonal influenza vaccination are short-term, as vaccine effectiveness is limited to the upcoming epidemic season, thus it is necessary to evaluate cost, vaccine safety, and effectiveness annually.

The controversy over the effectiveness of repeated influenza vaccination has continued for decades.¹¹ Research on repeated influenza vaccination primarily focuses on assessing its effectiveness.¹² Studies on factors influencing repeated vaccination have mainly been conducted in developed countries with free influenza vaccination policies.^13–16 In China, influenza vaccines are not included in the national immunization program (voluntary and self-payment vaccination), but the vaccination strategies vary across different regions. In the 2021–2022 period, 256 districts in China implemented free vaccination policies (covering 20.7 million people), 135 districts implemented medical insurance reimbursement policies (covering 31.1 million people), while the remaining areas implemented a self-payment policy (approximately 1360.9 million people).¹⁷ In China, influenza vaccination coverage under free vaccination, medical insurance reimbursement, and self-payment policies were 38.32%, 7.36%, and 1.81%, respectively.¹⁷ Currently, there is limited research on the characteristics and influencing factors of repeated influenza vaccination among elderly individuals in China. In this study, we observed the characteristics and factors associated with repeated influenza vaccination among the elderly population in Xuhui District, Shanghai, from 2020 to 2022, under the implementation of a self-payment policy. Furthermore, passive monitoring was conducted to assess the safety of repeated influenza vaccination. The aim of our study is to provide scientific data supporting future measures to enhance elderly individuals’ willingness to receive annual repeated influenza vaccination, thus improving influenza vaccination coverage among this demographic.

Methods

This study utilized convenience sampling to choose Xuhui District in Shanghai as the study location. Xuhui District, situated in the central area of Shanghai, spans an area of 547,600 square meters and had a population of 1,114,800 in 2022 (Table 1). All 13 community vaccination clinics and seven specialized vaccination clinics providing influenza vaccination services for elderly individuals in Xuhui District were chosen as research sites. Records of influenza vaccine for individuals aged 60 and above, including personal information and vaccination dates, were collected from these 20 clinics via the Shanghai Immunization Planning Information Management System (SIPIS). Adverse events following immunization (AEFI) records were obtained from the AEFI monitoring module of the Chinese Disease Prevention and Control Information System, containing personal information, vaccination information, AEFI symptoms, and reaction categorization. The AEFI reporting rate (per 100,000 doses) was calculated as the quotient of reported AEFI cases and doses administered, multiplied by 100,000. The number of registered residents aged 60 and above in Shanghai was sourced from the Shanghai Statistical Yearbook to calculate influenza vaccination coverage.¹⁸ From 2020 to 2021, the population of registered residents aged 60 and above in Xuhui District, Shanghai, was 327,700, 334,800, and 339,600, respectively, representing 35.41%, 36.00%, and 36.12% of the total registered population (Table 1). This study received approval from the Ethics Review Board of Xuhui District Center for Disease Control and Prevention (Approval No. XHLL202206).

Table 1. Distribution of influenza vaccination coverage among registered elderly individuals of different age groups in Shanghai, China, from 2020 to 2022.

Year	Total population	Registered population	Influenza vaccination among registered older individuals
			60–64			65–79			80+			Subtotal
			Population	Vaccination (%)	Coverage	Population	Vaccination (%)	Coverage	Population	Vaccination (%)	Coverage	Population	Vaccination	Coverage
2020	109.46	92.54	9.57	0.47 (26.04)	4.91	17.18	1.11 (61.65)	6.48	6.02	0.22 (12.32)	3.70	32.77	1.81	5.51
2021	111.47	92.99	9.11	0.27 (22.50)	2.99	18.29	0.77 (63.68)	4.21	6.09	0.17 (13.82)	2.75	33.48	1.21	3.61
2022	111.48	94.01	8.36	0.20 (18.25)	2.37	19.46	0.74 (67.67)	3.78	6.14	0.15 (14.09)	2.50	33.96	1.09	3.20

Units of population in ten thousand people; the numbers in parentheses represent the proportions.

The study cohort composed individuals aged 60 and above residing in Xuhui District, Shanghai, who received influenza vaccines from 2020 to 2022. According to the requirements of the specification of vaccination, their vaccination information is recorded in SIPIS. Age was determined by the date of the initial vaccination administered between 2020 and 2022. Repeated vaccination was defined as individuals who received the influenza vaccine in two consecutive years or in different influenza seasons within the same year. To determine individuals’ repeated vaccination status in 2020, their influenza vaccine history from 2019 was also collected.

Excel 2016 software was used for database management, encompassing records of influenza vaccine administration among individuals aged 60 and above, as well as AEFI case database. Data description and statistical analysis were performed using SPSS version 26.0. Descriptive statistics for continuous variables were presented as mean ± standard deviation (SD), whereas categorical variables were expressed as percentages. Categorical variables were compared using the chi-square test. Trend analysis was conducted using the Cochran-Armitage trend test. An ordered multinomial logistic regression model was employed to identify the factors influencing repeated influenza vaccination. The dependent variable included the number of repeated vaccinations (zero, one, two, or three times), while independent variables comprised gender, age, household registration, and type of clinic. A significance level of p < .05 indicates statistical significance. Graphs were generated using GraphPad Prism version 8.0.

Results

Between 2020 and 2022, a total of 29,200 elderly individuals aged 60 years and older in Xuhui District, Shanghai, received at least one dose of influenza vaccine. Among them 12,600 (43.15%) were male. The mean age was 70.51 ± 7.10 years. Of the vaccine recipients 24,400 (83.56%) were residents registered in Shanghai, and 24,200 (82.88%) were managed by community vaccination clinics. The number of elderly individuals receiving influenza vaccines each year gradually declined over the period, comprising 20,800, 14200, and 12,900 recipients in 2020, 2021, and 2022, respectively (Figure 1(a)).

Figure 1. Displays of the influenza vaccination, repeated vaccination, and AEFI among older individuals in Shanghai, China from 2020 to 2022. AEFI: adverse events following immunization.

(a) The number of older individuals who received influenza vaccines; (b) The rate of repeated influenza vaccination; (c) The reported incidence of adverse events following immunization.

From 2020 to 2022, the average influenza vaccination coverage among registered elderly individuals in Shanghai was 4.10%. Over these three years, the influenza vaccination coverage for registered elderly individuals was 5.51%, 3.61%, and 3.20% respectively, indicating a decreasing trend (p < .001), as shown in Table 1. Individuals aged 60–64 exhibited a declining trend in receiving influenza vaccines, decreasing from 26.04% in 2020 to 18.25% in 2022. Conversely, individuals aged 65–79 and those aged 80 and above exhibited an increasing trend (Table 1). For the year 2022, the influenza vaccination coverage among registered elderly individuals aged 60–64, 65–79, and 80 years and above was 2.37%, 3.78%, and 2.50%, respectively (Table 1). Across the three age groups in 2020 and 2021, the influenza vaccination coverage also exhibited an inverted U-shaped distribution.

Over the period of 2020–2022, of the 29,200 elderly individuals who had previously received the influenza vaccine 16,200 (55.48%) did not receive repeated vaccination, 6,000 (20.55%) received one repeat vaccination, 4,000 (13.70%) received two repeat vaccinations, and 3,000 (10.27%) received three repeat vaccinations. The rate of repeated vaccination among elderly individuals in 2020, 2021, and 2022 was 28.35% (5,900 out of 20,800), 63.53% (9,000 out of 14,200), and 64.38% (8,300 out of 12,900), respectively, as shown in (Figure 1(b)).

Among elderly individuals, the rate of repeated vaccination was higher in those managed through community vaccination clinics compared to those managed through special vaccination clinics (51.81% vs. 28.56%, χ² = 1279, p < .001). Registered residents of Shanghai exhibited a higher rate of repeated vaccination compared to non-Shanghai registered residents (51.20% vs. 31.66%, χ² = 885, p < .001). Males had a slightly higher rate of repeated vaccination compared to females (49.13% vs. 47.92%, χ² = 6.81, p = .009). Repeated vaccination rates among elderly individuals increased with age, with rates of 44.41%, 51.75%, and 60.06% in the 60–69, 70–79, and 80 years and above age groups, respectively, demonstrating an upward trend (p < .001), as shown in Table 2. The results of ordered multinomial logistic regression model showed that elderly individuals with Shanghai household registration (OR = 1.80, 95%CI: 1.68–1.93) and those vaccinated in community clinics (OR = 2.10, 95%CI: 1.96–2.26) exhibited a higher likelihood of repeated influenza vaccinations. Individuals aged 70–79 (OR = 1.18, 95%CI: 1.12–1.24) and those aged ≥ 80 (OR = 1.48, 95%CI: 1.38–1.60) were more likely to receive repeated influenza vaccinations compared to those aged 60–69. There was no observed correlation between gender and the frequency of repeated influenza vaccinations among elderly individuals (OR = 1.02, 95%CI: 0.97–1.07), as shown in Table 3.

Table 2. Distribution of repeated influenza vaccination among elderly individuals in Shanghai, China, from 2020 to 2022.

Variable Group	2020 (n = 2.08)		2021 (n = 1.42)		2022 (n = 1.29)		Total (N = 4.78)
	Non-repeated vaccination	Repeated vaccination	Non-repeated vaccination	Repeated vaccination	Non-repeated vaccination	Repeated vaccination	Non-repeated vaccination	Repeated vaccination
Type of vaccination clinic
Special clinics	0.26 (90.22)	0.03 (9.78)	0.14 (62.14)	0.08 (37.86)	0.10 (52.70)	0.09 (47.30)	0.49 (71.44)	0.20 (28.56)
Community clinics	1.23 (68.64)	0.56 (31.36)	0.38 (31.82)	0.82 (68.18)	0.36 (32.77)	0.74 (67.23)	1.97 (48.19)	2.12 (51.81)
Gender
Female	0.85 (72.16)	0.33 (27.84)	0.29 (36.86)	0.50 (63.14)	0.26 (36.19)	0.46 (63.81)	1.41 (52.08)	1.30 (47.92)
Male	0.64 (70.99)	0.26 (29.01)	0.22 (35.97)	0.40 (64.03)	0.19 (34.86)	0.36 (65.14)	1.05 (50.87)	1.02 (49.13)
Household registration
Non-shanghai	0.24 (86.20)	0.04 (13.80)	0.12 (59.44)	0.08 (40.56)	0.10 (52.70)	0.09 (47.30)	0.46 (68.34)	0.21 (31.66)
Shanghai	1.25 (69.45)	0.55 (30.55)	0.39 (32.55)	0.82 (67.45)	0.35 (32.56)	0.73 (67.44)	2.00 (48.80)	2.10 (51.20)
Age group
60–69	0.92 (77.23)	0.27 (22.77)	0.33 (40.02)	0.49 (59.98)	0.28 (37.70)	0.46 (62.30)	1.53 (55.59)	1.22 (44.41)
70–79	0.44 (67.64)	0.21 (32.36)	0.15 (33.47)	0.30 (66.53)	0.14 (33.66)	0.27 (66.34)	0.72 (48.25)	0.78 (51.75)
≥80	0.13 (54.39)	0.11 (45.61)	0.04 (26.81)	0.12 (73.19)	0.04 (29.99)	0.09 (70.01)	0.21 (39.94)	0.32 (60.06)
Total	1.49 (71.65)	0.59 (28.35)	0.52 (36.47)	0.90 (63.53)	0.46 (35.62)	0.83 (64.38)	2.46 (51.55)	2.32 (48.45)

Units of population in ten thousand people; the numbers in parentheses represent the proportions.

Table 3. Ordered multinomial logistic regression analysis on the factors influencing the number of repeated influenza vaccination among elderly individuals in Shanghai.

Variable Group	β	Waldχ^2	OR (95%CI)	P
Type of vaccination clinic
Special clinics			Reference
Community clinics	0.744	0.674	2.10 (1.96–2.26)	<.001
Gender
Female			Reference
Male	0.018	−0.027	1.02 (0.97–1.07)	.440
Household registration
Non-shanghai			Reference
Shanghai	0.588	0.518	1.80 (1.68–1.93)	<.001
Age group
60–69			Reference
70–79	0.165	0.115	1.18 (1.12–1.24)	<.001
≥80	0.394	0.322	1.48 (1.38–1.60)	<.001

Between 2020 and 2022, AEFIs were reported in 58 elderly individuals after receiving the influenza vaccine. Among these cases, 57 were categorized as common reactions, while one was characterized as a rare reaction – an anaphylactic rash, which resolved post-administration of allergy treatment. The reported incidence of AEFI in 2020, 2021, and 2022 were 134.62 cases per 100,000 doses, 105.88 cases per 100,000 doses, and 116.99 cases per 100,000 doses, respectively (Figure 1(c)). Among the 58 AEFI cases, 30 occurred in individuals who received repeated vaccination, all of which were common reactions. The remaining 28 cases occurred in individuals who did not receive repeated vaccination, including one case of anaphylactic rash. There was no statistically significant difference in the reported incidence of AEFI between the two groups (129.58 cases per 100,000 doses vs. 113.65 cases per 100,000 doses; χ² = 0.250, p = .617).

Discussion

During the period of 2020–2022, the influenza vaccination coverage among elderly individuals registered in Shanghai under the self-payment policy was below 5%, much lower than the coverage under the free policy during the same period in China, which ranged from 32.94% to 45.71%.¹⁷ Our study also identified a decreasing trend in influenza vaccination coverage among elderly individuals from 2020 to 2022, a phenomenon observed in studies conducted in China and the United States.^17,19 The period of 2020–2022 coincided with the COVID-19 pandemic, which may have contributed to the decline in influenza vaccination coverage. Firstly, there was a significant increase in willingness to be vaccinated against influenza before the availability of COVID-19 vaccines.²⁰ Secondly, the strict public health interventions during the COVID-19 pandemic led to a notable decrease in influenza prevalence,²¹ reducing the perceived risk of influenza among the public, thus diminishing the importance of influenza vaccines.²² Additionally, the mass vaccination campaigns for COVID-19 in China, starting in 2021, resulted in a shortage of vaccination personnel,²³ oversaturation due to an excessive of COVID-19 vaccine doses,²⁴ and concerns regarding potential interactions between influenza and COVID-19 vaccines,^25,26 all of which could have decreased willingness to receive influenza vaccines. Considering the heavy burden of influenza on elderly individuals and the extremely low vaccination coverage, the Shanghai municipal government should consider implementing strategies such as free vaccinations or medical insurance reimbursement as soon as possible.

Despite the recommendation for annual influenza vaccination among older adults, only 10% of elderly individuals in Shanghai, China received influenza vaccines annually during the period of 2020–2021. This is notably lower compared to older women in France, where 43% are vaccinated annually.¹⁴ This discrepancy may lie in France’s policy of free influenza vaccination, significantly boosting vaccination coverage.²⁰ Moreover, the French study primarily focused on female participants, 62% of whom were teachers and 82% possessed higher education, potentially contributing to the observed difference.¹⁴ Our study indicates a declining trend in influenza vaccination coverage overall, yet there was a notable rise in repeated vaccination rates among elderly individuals in 2021 and 2022 compared to 2020. The lower rate of repeated vaccination among elderly individuals in 2020 might be related to the absence of COVID-19 vaccines during the initial pandemic year, prompting more elderly individuals, especially those aged 60–64, to receive their first influenza vaccination. This phenomenon can also be explained by the declining trend in the proportion of influenza vaccination among individuals aged 60–64 years during 2020–2021. Previous researches have demonstrated that influenza vaccination history is a strong predictor of future vaccination,^27,28 likely contributing to the increased rate of repeated vaccination among elderly individuals in 2021 and 2022. The National Advisory Committee on Immunization in Canada has recommended that influenza vaccination should be given annually, regardless of previous vaccination status.²⁹ Therefore, to enhance influenza vaccine coverage among the older population, government departments should intensify efforts to promote the necessity of annual influenza vaccination and increase the proportion of repeated vaccination.

Previous studies have identified several factors influencing individuals’ likelihood of receiving repeated influenza vaccinations, such as age, gender, history of chronic illnesses, smoking habits, marital status, level of education, racial, and frequency of hospital visits.^13–16 Our study also confirmed that age was a determinant factor in repeated influenza vaccination. Furthermore, our study identified two additional factors influencing repeated influenza vaccination: elderly individuals with Shanghai household registration and those managed by community vaccination clinics exhibit a higher propensity for repeat influenza vaccinations. Measures such as family physicians, annual health checkups, and chronic disease management provide elderly individuals with more opportunities to learn about influenza and influenza vaccination. Therefore, government agencies can implement more targeted measures to increase the frequency of repeated influenza vaccination among elderly individuals. For example, focusing on health education and incentives for younger elderly individuals and those not registered in Shanghai.

Previous studies have shown an inverse relationship between the levels of confidence in the safety of influenza vaccines among elderly individuals and their tendency toward vaccine hesitancy.¹⁰ Our safety surveillance findings showed that the reporting rate of AEFI among elderly individuals who received repeat influenza vaccinations was similar to those who did not, and there was no increased likelihood of severe adverse effects. Post-marketing safety surveillance data on influenza vaccines confirm the safety of administering these vaccines to elderly individuals.^30–32 Therefore, to address the safety concerns of the elderly individuals regarding influenza vaccines, government agencies should strengthen public awareness efforts to reduce vaccine hesitancy among this population.

Our study had several limitations. Firstly, given the variation in influenza vaccination strategies across different regions in China, the generalizability of our findings to the entire nation may be limited. However, the population covered by the implementation of the free influenza vaccine policy reached 96.3%. Secondly, due to inadequate population data, approximately 15% of non-registered elderly individuals were excluded from the calculation of influenza vaccine coverage. Shanghai, being a densely populated megacity with significant population mobility, hinders our understanding of influenza vaccine coverage across the entire population. Thirdly, present post-market vaccine safety monitoring predominantly relies on passive surveillance, potentially leading to underreporting of severe adverse reactions among older individuals following repeat vaccinations. Nonetheless, the incidence of serious adverse events remain consistent between the repeat and non-repeat vaccination cohorts. Lastly, our study focused on the initial three years of the COVID-19 pandemic. Differences in epidemic severity and control measures between countries may affect the comparability of findings.

In conclusion, influenza vaccination coverage among older residents registered in Shanghai was remarkably low, with a declining trend observed from 2020 to 2022. Nevertheless, the rate of repeated influenza vaccination among elderly individuals increased in 2021 and 2022 more than doubling that of 2020 and reaching nearly two-thirds. Moreover, repeated influenza vaccination has shown no increased risk of adverse events following immunization. Increasing influenza vaccination coverage among elderly individuals in Shanghai is both urgent and challenging. Health authorities should intensify educational and promotional campaigns to encourage uptake of annual repeated influenza vaccination among elderly individuals. Subsequent steps involve conducting real-world studies to evaluate the effectiveness of repeated influenza vaccination among elderly individuals, aimed at reducing concerns regarding the efficacy of repeat vaccination. Government departments should promptly implement free vaccination or medical insurance reimbursement policies for key populations, especially elderly individuals, to significantly increase influenza vaccination coverage.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was financially supported by grants from the Medical Research Project in Xuhui District, Shanghai [SHXH202212].