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Preplanned Studies: Hesitancy to Receive the Booster Doses of COVID-19 Vaccine Among Cancer Patients in China: A Multicenter Cross-Sectional Survey — Four PLADs, China, 2022

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  • Summary

    What is already known about this topic?

    Cancer patients are more vulnerable and have higher mortality rates from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) than the general population; however, coverage for booster doses of the coronavirus disease 2019 (COVID-19) vaccine was low among cancer patients in China.

    What is added by this report?

    Overall, 32.0% and 56.4% of cancer patients from four Provincial Level Administrative Divisions (PLADs) expressed hesitancy toward the first and second booster doses, respectively. Factors negatively associated with hesitancy to receive booster doses included positive attitudes, perceived support, and higher exposure to COVID-19 vaccination information. Conversely, postvaccination fatigue was positively associated with vaccine hesitancy.

    What are the implications for public health practice?

    Improved COVID-19 vaccination coverage is needed to promote health for cancer patients.

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  • Funding: This study was supported by the National Natural Science Foundation of China (81872674), the Joint Foundation of Innovative Environment Construction of Autonomous Region of Xinjiang (#2019D01C326), and the Four “Batches” Innovation Project of Invigorating Medical Cause through Science and Technology of Shanxi Province (2022XM45), Shenzhen Science and Technology Innovation Committee Projects (No. JCYJ20220818102817038), the Scientific Research Foundation of Peking University Shenzhen Hospital (No. KYQD2022216)
  • [1] Menni C, May A, Polidori L, Louca P, Wolf J, Capdevila J, et al. COVID-19 vaccine waning and effectiveness and side-effects of boosters: a prospective community study from the ZOE COVID study. Lancet Infect Dis 2022;22(7):1002 − 10. http://dx.doi.org/10.1016/S1473-3099(22)00146-3CrossRef
    [2] Zhao Y, Du J, Li Z, Xu Z, Wu YX, Duan WS, et al. It is time to improve the acceptance of COVID-19 vaccines among people with chronic diseases: a systematic review and meta-analysis. J Med Virol 2023;95(2):e28509. http://dx.doi.org/10.1002/jmv.28509CrossRef
    [3] National Health Commission of the People’s Republic of China. COVID-19 vaccination boosters. 2022. http://www.nhc.gov.cn/xcs/fkdt/202301/34d7d68ed30a4d249be6da9a43e6a8d7.shtml. [2023-2-1]. (In Chinese). http://www.nhc.gov.cn/xcs/fkdt/202301/34d7d68ed30a4d249be6da9a43e6a8d7.shtml
    [4] Chun JY, Kim SI, Park EY, Park SY, Koh SJ, Cha YJ, et al. Cancer patients’ willingness to take COVID-19 vaccination: a nationwide multicenter survey in Korea. Cancers (Basel) 2021;13(15):3883. http://dx.doi.org/10.3390/cancers13153883CrossRef
    [5] Su ZH, Cheshmehzangi A, McDonnell D, da Veiga CP, Xiang YT. Mind the “vaccine fatigue”. Front Immunol 2022;13:839433. http://dx.doi.org/10.3389/fimmu.2022.839433CrossRef
    [6] Ajzen I. The theory of planned behavior. Organ Behav Hum Decis Process 1991;50(2):179 − 211. http://dx.doi.org/10.1016/0749-5978(91)90020-TCrossRef
    [7] Wang ZX, Fang Y, Yu FY, Chan PSF, Chen SY, Sun FH. Facilitators and barriers to take up a COVID-19 vaccine booster dose among community-dwelling older adults in Hong Kong: a population-based random telephone survey. Vaccines (Basel) 2022;10(6):966. http://dx.doi.org/10.3390/VACCINES10060966CrossRef
    [8] Zhang KC, Fang Y, Chan PSF, Cao H, Chen HB, Hu T, et al. Behavioral intention to get a booster dose of COVID-19 vaccine among Chinese factory workers. Int J Environ Res Public Health 2022;19(9):5245. http://dx.doi.org/10.3390/ijerph19095245CrossRef
    [9] Qin CY, Wang RT, Tao LY, Liu M, Liu J. Acceptance of a third dose of COVID-19 vaccine and associated factors in China based on health belief model: a national cross-sectional study. Vaccines (Basel) 2022;10(1):89. http://dx.doi.org/10.3390/VACCINES10010089CrossRef
  • FIGURE 1.  The data collection procedures of this study.

    TABLE 1.  Background characteristics of 525 participants who completed the primary COVID-19 vaccination series.

    Background characteristicNo. of participantsPercentage (%)
    Sociodemographic characteristics
    Age group in years
    18–458716.6
    46–6021941.7
    61–7519437.0
    >75254.8
    Gender
    Male29355.8
    Female23244.2
    Ethnicity
    Han majority42681.1
    Other ethnic minority groups9918.9
    Education level
    Junior high school and below33864.4
    High school education or equivalent10219.4
    College-level and above8516.2
    Relationship status
    Single/divorced/widowed397.4
    Married48692.6
    Employment status
    Full-time13826.3
    Part-time/self-employed/unemployed/retired/students38773.7
    Characteristics of cancer
    Type of cancer
    Lung cancer10920.8
    Gastric cancer6612.6
    Liver cancer152.9
    Breast cancer305.7
    Colorectal cancer9718.5
    Esophageal cancer265.0
    Ovarian cancer438.2
    Other types of cancer13926.5
    Metastatic cancers
    No49093.3
    Yes356.7
    Current treatment for cancer
    Untreated patients173.2
    Chemotherapy only33864.4
    Radiotherapy only8917.0
    Immunotherapy only122.3
    Chemotherapy and radiotherapy346.5
    Immunotherapy and chemotherapy/radiotherapy152.9
    Treatment completion203.8
    Presence of other chronic diseases
    Diabetes mellitus305.7
    Hypertension and/or hyperlipidemia7313.9
    Chronic cardiovascular diseases132.5
    Chronic respiratory diseases40.8
    Chronic liver and/or kidney diseases71.3
    Other chronic diseases152.9
    Download: CSV

    TABLE 2.  Factors associated with hesitancy to receive the first and second booster doses of the COVID-19 vaccine (N=525).

    CharacteristicHesitancy to receive the
    third dose of COVID-19 vaccine
    Hesitancy to receive the
    fourth dose of COVID-19 vaccine
    OR (95% CI)P valueAOR*
    (95% CI)
    P valueOR (95% CI)P valueAOR*
    (95% CI)
    P value
    Individual-level variables
    Positive attitude scale0.83
    (0.76, 0.92)
    <0.0010.83
    (0.76, 0.92)
    <0.0010.65
    (0.60, 0.74)
    <0.0010.66
    (0.60, 0.74)
    <0.001
    Negative attitude scale1.01
    (0.97, 1.06)
    0.5531.01
    (0.97, 1.06)
    0.5601.03
    (0.99, 1.08)
    0.1471.03
    (0.99, 1.08)
    0.195
    Perceived subjective norms0.54
    (0.43, 0.67)
    <0.0010.55
    (0.44, 0.69)
    <0.0010.39
    (0.30, 0.49)
    <0.0010.40
    (0.31, 0.51)
    <0.001
    Perceived behavioral control0.54
    (0.43, 0.67)
    <0.0010.51
    (0.40, 0.63)
    <0.0010.25
    (0.19, 0.34)
    <0.0010.25
    (0.19, 0.34)
    <0.001
    Vaccination fatigue (tired of receiving COVID-19 vaccination over and over again)1.34
    (1.18, 1.58)
    <0.0011.36
    (1.18, 1.58)
    <0.0011.48
    (1.28, 1.71)
    <0.0011.52
    (1.31, 1.78)
    <0.001
    Hesitancy to receive the third dose of COVID-19 vaccineNANANANA14.05
    (7.94, 24.79)
    <0.00114.05
    (8.05, 24.52)
    <0.001
    Interpersonal variables
    Media exposure scale0.93
    (0.89, 0.99)
    0.0120.94
    (0.89, 0.99)
    0.0330.90
    (0.85, 0.95)
    <0.0010.90
    (0.85, 0.95)
    <0.001
    Frequency of thoughtful consideration about veracity of COVID-19-specific information0.64
    (0.53, 0.77)
    <0.0010.65
    (0.54, 0.79)
    <0.0010.51
    (0.42, 0.62)
    <0.0010.52
    (0.43, 0.64)
    <0.001
    Abbreviation: OR=crude odds ratio; AOR=adjusted odds ratio; CI=confidence interval; NA=not applicable.
    * Adjusted for significant background characteristics listed in Supplementary Table S2.
    Download: CSV

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Hesitancy to Receive the Booster Doses of COVID-19 Vaccine Among Cancer Patients in China: A Multicenter Cross-Sectional Survey — Four PLADs, China, 2022

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Summary

What is already known about this topic?

Cancer patients are more vulnerable and have higher mortality rates from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) than the general population; however, coverage for booster doses of the coronavirus disease 2019 (COVID-19) vaccine was low among cancer patients in China.

What is added by this report?

Overall, 32.0% and 56.4% of cancer patients from four Provincial Level Administrative Divisions (PLADs) expressed hesitancy toward the first and second booster doses, respectively. Factors negatively associated with hesitancy to receive booster doses included positive attitudes, perceived support, and higher exposure to COVID-19 vaccination information. Conversely, postvaccination fatigue was positively associated with vaccine hesitancy.

What are the implications for public health practice?

Improved COVID-19 vaccination coverage is needed to promote health for cancer patients.

  • 1. Clinical Research Academy, Peking University Shenzhen Hospital, Shenzhen Peking University-The Hong Kong University of Science and Technology Medical Center, Shenzhen City, Guangdong Province, China
  • 2. Department of Radiotherapy, Peking University Shenzhen Hospital, Peking University, Shenzhen City, Guangdong Province, China
  • 3. JC School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, China
  • 4. Department of Epidemiology, China Medical University, Shenyang City, Liaoning Province, China
  • 5. Clinical Research Academy, Peking University Shenzhen Hospital, Shenzhen City, Guangdong Province, China
  • 6. Cancer Center at Inner Mongolia People’s Hospital, Hohhot City, Inner Mongolia Autonomous Region, China
  • 7. John Hopkins Bloomberg School of Public Health, Baltimore, United States
  • 8. Department of Public Health and Preventive Medicine, Changzhi Medical College, Changzhi City, Shanxi Province, China
  • Corresponding authors:

    Jianzhou Yang, jzyang@aliyun.com

    Zixin Wang, wangzx@cuhk.edu.hk

    Junjie Xu, xjjcmu@163.com

  • Funding: This study was supported by the National Natural Science Foundation of China (81872674), the Joint Foundation of Innovative Environment Construction of Autonomous Region of Xinjiang (#2019D01C326), and the Four “Batches” Innovation Project of Invigorating Medical Cause through Science and Technology of Shanxi Province (2022XM45), Shenzhen Science and Technology Innovation Committee Projects (No. JCYJ20220818102817038), the Scientific Research Foundation of Peking University Shenzhen Hospital (No. KYQD2022216)
  • Online Date: March 10 2023
    Issue Date: March 10 2023
    doi: 10.46234/ccdcw2023.041
  • Recent concerns have been raised about waning protection against coronavirus disease 2019 (COVID-19) after completing the two-dose primary vaccination series (1). Cancer patients have been found to have higher mortality from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) than the general population, but only 52% [95% confidence interval (CI): 35%–70%] of this population were willing to accept the COVID-19 vaccine (2). To date, no study has evaluated the hesitancy of cancer patients to receive the booster doses of the COVID-19 vaccines in China. A multicenter cross-sectional study was conducted in four Chinese cities. Medical staff approached all cancer inpatients aged 18 years or above, and 893 patients completed a face-to-face interview. This study was based on a sub-sample of 525 participants who completed the primary vaccination series. Logistic regression models were fitted to identify the factors associated with vaccine hesitancy. Among the participants, 32.0% and 56.4% were hesitant to receive the first and second COVID-19 vaccine booster doses. Positive attitudes, perceived support from significant others and perceived behavioral control related to the booster dose, higher exposure to COVID-19 vaccination information, and thoughtful consideration about the veracity of COVID-19-specific information were associated with lower hesitancy to receive the booster doses. Vaccination fatigue was positively associated with vaccine hesitancy. Cancer patients in China were more hesitant than the general population to receive COVID-19 vaccine booster doses. Health sectors should advocate the benefits of vaccination with COVID-19 booster doses to cancer patients, which would improve the coverage and promote health.

    In Chinese mainland, the National Guideline recommends a third dose of COVID-19 vaccine as a booster for cancer patients six months after completing the two-dose primary vaccination series (3). Many cancer patients may be hesitant to receive the booster doses. A previous study identified some factors associated with hesitancy to complete the primary vaccination series among cancer patients (4). Vaccine fatigue, which is defined as people’s inaction towards vaccine instruction due to perceived burden and burnout (5), could be a factor in this hesitancy. Thoughtful consideration of the veracity of the information may mitigate the negative impact of misinformation related to COVID-19 and COVID-19 vaccination. This study examined the effects of sociodemographics, cancer-related characteristics, perceptions, vaccine fatigue, and media influences associated with vaccine hesitancy.

    This was a multicenter, cross-sectional study of cancer patients in four Chinese cities from four Provincial Level Administrative Divisions (PLADs) (Changzhi, Hohhot, Urumqi, and Shenzhen) conducted between May and June 2022. All study sites adhered to the national guideline and recommended a third dose of the COVID-19 vaccine as a booster for cancer patients (3).

    Participants of the original study were included if they met the following criteria: 1) cancer patients who were hospitalized in the four participating hospitals during the study period, 2) aged 18 years or above, and 3) willing to provide written informed consent to complete the survey. Exclusion criteria included: 1) critical illness or intensive care unit admission, 2) a diagnosis of lymphoma, leukemia, mental illness, or taking medication for mental illness, or 3) dementia or inability to communicate effectively with the investigators. Medical staff from the selected hospitals approached all cancer inpatients, screened their eligibility, briefed them about the study, and invited them to participate in a face-to-face interview. No incentives were provided. The data collection procedures are shown in Figure 1. Ethics approval was obtained from the Institutional Review Board of Changzhi Medical College (reference: RT2022027).

    Figure 1. 

    The data collection procedures of this study.

    Participants reported sociodemographic information, and medical staff extracted cancer-related characteristics and presence of other chronic diseases from medical records. We first asked whether participants had received the first booster dose, and for those who had not, we further asked their likelihood of receiving it (response categories: 1=very unlikely, 2=unlikely, 3=neutral, 4=likely, and 5=very likely). Since China has not yet provided the second booster dose, we asked all participants their likelihood of receiving it if it is available (response categories: 1=very unlikely, 2=unlikely, 3=neutral, 4=likely, and 5=very likely). Vaccine hesitancy was defined as “very unlikely,” “unlikely,” or “neutral.” We used the Theory of Planned Behavior (TPB) to measure perceptions related to COVID-19 vaccine booster dose (6). We used the 3-item Positive Attitude Scale and modified the 5-item Negative Attitude Scale, both of which were validated in older Chinese adults (7). In addition, perceived subjective norm and perceived behavioral control were measured by two single-item scales validated in the Chinese population (8). Vaccine fatigue was measured by a single item (“You are tired of receiving COVID-19 vaccination over and over again”). We adopted four items validated in the Chinese population to measure media influences related to COVID-19 and COVID-19 vaccination (8). A validated single item assessed the frequency of thoughtful consideration about the veracity of COVID-19 specific information. The Cronbach’s alpha of the Positive Attitude Scale, Negative Attitude Scale, and the Media Exposure Scale was 0.90, 0.84, and 0.90, respectively.

    Frequency distributions of all variables were measured, and the mean and standard deviation (SD) of the scale and item scores were presented. Reliability tests were used to obtain the Cronbach's alpha for the scales. Hesitancy to receive the first and second COVID-19 vaccine booster doses were used as dependent variables, and univariate logistic regression models were used to examine significant associations between background characteristics and dependent variables. Perceptions, vaccine fatigue, and media influence were used as independent variables, and associations between one of these independent variables and the dependent variables with adjustments for significant background characteristics were assessed using adjusted odds ratios (AORs) and their corresponding CIs. There were no missing values for the participants who completed the primary vaccination series. Data analysis was conducted using IBM SPSS Statistics (version 26.0, IBM Corp., Armonk, NY, USA) and P<0.05 was considered statistically significant.

    A total of 893 participants provided written informed consent and completed the interview. Of the 525 eligible cancer patients who completed primary COVID-19 vaccination, 41.8% were over 60 years old and 55.8% were male. The most common type of cancer was lung cancer (20.8%), followed by colorectal cancer (18.5%), and 6.7% had metastatic cancers. Most participants (93.0%) were under cancer treatment. In addition to cancers, 21.5% had at least one other chronic disease (Table 1). Of the participants, 49.9% had received the first COVID-19 booster dose. Of those who had not yet received the first booster dose, 36.1% intended to get vaccinated. The prevalence of hesitancy to receive the first and the second booster doses was 32.0% and 56.4%, respectively (Supplementary Table S1).

    Background characteristicNo. of participantsPercentage (%)
    Sociodemographic characteristics
    Age group in years
    18–458716.6
    46–6021941.7
    61–7519437.0
    >75254.8
    Gender
    Male29355.8
    Female23244.2
    Ethnicity
    Han majority42681.1
    Other ethnic minority groups9918.9
    Education level
    Junior high school and below33864.4
    High school education or equivalent10219.4
    College-level and above8516.2
    Relationship status
    Single/divorced/widowed397.4
    Married48692.6
    Employment status
    Full-time13826.3
    Part-time/self-employed/unemployed/retired/students38773.7
    Characteristics of cancer
    Type of cancer
    Lung cancer10920.8
    Gastric cancer6612.6
    Liver cancer152.9
    Breast cancer305.7
    Colorectal cancer9718.5
    Esophageal cancer265.0
    Ovarian cancer438.2
    Other types of cancer13926.5
    Metastatic cancers
    No49093.3
    Yes356.7
    Current treatment for cancer
    Untreated patients173.2
    Chemotherapy only33864.4
    Radiotherapy only8917.0
    Immunotherapy only122.3
    Chemotherapy and radiotherapy346.5
    Immunotherapy and chemotherapy/radiotherapy152.9
    Treatment completion203.8
    Presence of other chronic diseases
    Diabetes mellitus305.7
    Hypertension and/or hyperlipidemia7313.9
    Chronic cardiovascular diseases132.5
    Chronic respiratory diseases40.8
    Chronic liver and/or kidney diseases71.3
    Other chronic diseases152.9

    Table 1.  Background characteristics of 525 participants who completed the primary COVID-19 vaccination series.

    In the univariate analysis, cancer patients who were ethnic minorities had lower hesitancy to receive the first COVID-19 vaccine booster dose (Supplementary Table S2). After adjusting for significant background characteristics listed in Supplementary Table S2, positive attitudes toward the booster dose (AOR: 0.83 & 0.66), perceived higher support from significant others (AOR: 0.55 & 0.40), perceived higher behavioral control to take up the booster dose (AOR: 0.51 & 0.25), higher exposure to information related to COVID-19 vaccination (AOR: 0.94 & 0.90), and thoughtful consideration about the veracity of COVID-19-specific information (AOR: 0.65 & 0.52) were associated with lower hesitancy to receive the first and the second booster doses (Table 2). Vaccination fatigue was also positively associated with hesitancy to receive the first and second booster doses (AOR: 1.36 & 1.52). Additionally, hesitancy to receive the first booster dose was associated with higher hesitancy for the second booster dose (AOR: 14.05).

    CharacteristicHesitancy to receive the
    third dose of COVID-19 vaccine
    Hesitancy to receive the
    fourth dose of COVID-19 vaccine
    OR (95% CI)P valueAOR*
    (95% CI)
    P valueOR (95% CI)P valueAOR*
    (95% CI)
    P value
    Individual-level variables
    Positive attitude scale0.83
    (0.76, 0.92)
    <0.0010.83
    (0.76, 0.92)
    <0.0010.65
    (0.60, 0.74)
    <0.0010.66
    (0.60, 0.74)
    <0.001
    Negative attitude scale1.01
    (0.97, 1.06)
    0.5531.01
    (0.97, 1.06)
    0.5601.03
    (0.99, 1.08)
    0.1471.03
    (0.99, 1.08)
    0.195
    Perceived subjective norms0.54
    (0.43, 0.67)
    <0.0010.55
    (0.44, 0.69)
    <0.0010.39
    (0.30, 0.49)
    <0.0010.40
    (0.31, 0.51)
    <0.001
    Perceived behavioral control0.54
    (0.43, 0.67)
    <0.0010.51
    (0.40, 0.63)
    <0.0010.25
    (0.19, 0.34)
    <0.0010.25
    (0.19, 0.34)
    <0.001
    Vaccination fatigue (tired of receiving COVID-19 vaccination over and over again)1.34
    (1.18, 1.58)
    <0.0011.36
    (1.18, 1.58)
    <0.0011.48
    (1.28, 1.71)
    <0.0011.52
    (1.31, 1.78)
    <0.001
    Hesitancy to receive the third dose of COVID-19 vaccineNANANANA14.05
    (7.94, 24.79)
    <0.00114.05
    (8.05, 24.52)
    <0.001
    Interpersonal variables
    Media exposure scale0.93
    (0.89, 0.99)
    0.0120.94
    (0.89, 0.99)
    0.0330.90
    (0.85, 0.95)
    <0.0010.90
    (0.85, 0.95)
    <0.001
    Frequency of thoughtful consideration about veracity of COVID-19-specific information0.64
    (0.53, 0.77)
    <0.0010.65
    (0.54, 0.79)
    <0.0010.51
    (0.42, 0.62)
    <0.0010.52
    (0.43, 0.64)
    <0.001
    Abbreviation: OR=crude odds ratio; AOR=adjusted odds ratio; CI=confidence interval; NA=not applicable.
    * Adjusted for significant background characteristics listed in Supplementary Table S2.

    Table 2.  Factors associated with hesitancy to receive the first and second booster doses of the COVID-19 vaccine (N=525).

    • This is the first study to investigate hesitancy to receive the first and second COVID-19 vaccine booster doses among cancer patients. This study has several strengths, including its coverage of different geographic regions in China, its large sample size, and its examination of potential determinants at different levels. The level of hesitancy to receive the first COVID-19 vaccine booster dose among our participants was much higher than that of the general population in China (9).

      This study provided practical implications for developing health promotion. Addressing vaccination fatigue may be beneficial for future health promotion for cancer patients. Rapid changes in policies and recommendations related to COVID-19 booster doses caused confusion among the general public (5). This confusion was further exacerbated when health authorities recommended the second booster dose. Modifying perceptions related to COVID-19 vaccine booster doses is also important. Updated evidence of booster doses in reducing mortality and severe consequences caused by COVID-19 among cancer patients should be disseminated in an accessible manner. Future programs might consider involving significant others of cancer patients to create a subjective norm favoring COVID-19 vaccine booster doses uptake. Healthcare workers may facilitate cancer patients to form a plan to receive a booster dose during clinical visits, which may help to improve perceived behavioral control. Higher exposure to topics related to COVID-19 vaccination and the Omicron variant was associated with lower hesitancy to receive booster doses. Health authorities should consider using these mass media channels to disseminate messages promoting booster doses. Similar to the findings among the general population in China, thoughtful consideration played an essential role in reducing hesitancy to receive booster doses. Thoughtful consideration could mitigate the negative impacts of misinformation on vaccine hesitancy (8).

      This study has several limitations. First, our findings could not be generalized to all cancer patients, as we only targeted inpatients. Second, the sample was selected conveniently and could not represent all cancer patients in China. Third, we could not obtain the characteristics of cancer patients who refused to join the study, leading to selection bias. Additionally, this was a cross-sectional survey and could not establish a causal relationship. To address vaccination fatigue, modify perceptions related to booster doses, disseminate booster dose promotion messages through mass media, and improve thoughtful consideration of the veracity of COVID-19-related information might be helpful strategies.

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