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Parents’ concerns about vaccine scheduling in Shanghai, China
Vaccine xxx (2017) xxx–xxx
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Parents’ concerns about vaccine scheduling in Shanghai, China Abram L. Wagner a,⇑, Matthew L. Boulton a,b, Xiaodong Sun c, Zhuoying Huang c, Irene A. Harmsen d, Jia Ren c, Brian J. Zikmund-Fisher e a
Department of Epidemiology, School of Public Health, University of Michigan, 1415 Washington Heights, Ann Arbor, MI 48109, USA Department of Internal Medicine, Division of Infectious Diseases, University of Michigan Medical School, 1500 East Medical Center Drive, Ann Arbor, MI 48109, USA c Department of Immunization Program, Shanghai Municipal Centers for Disease Control & Prevention, NO. 1380, West Zhongshan Road, 200336 Shanghai, China d Department of Epidemiology and Health Promotion, Public Health Service of Amsterdam, Amsterdam, The Netherlands e Department of Health Behavior & Health Education, School of Public Health, University of Michigan, 1415 Washington Heights, Ann Arbor, MI 48109, USA b
a r t i c l e
i n f o
Article history: Received 1 February 2017 Received in revised form 21 June 2017 Accepted 23 June 2017 Available online xxxx Keywords: Anti-vaccination movement Vaccine hesitancy China Immunization schedule Vaccine refusal
a b s t r a c t Background: Several new vaccines have been introduced into China in recent years, but some parents in China have shown concerns about the scheduling of vaccinations for young infants. This study explores caregiver concerns about children receiving multiple vaccines during a single visit and about vaccine administration in infants <6 months, and assesses the degree to which these concerns are associated with ratings of the importance of different sources of vaccine information in Shanghai. Methods: Caregivers of children 8 months to 7 years presenting at immunization clinics in Shanghai completed a survey about vaccine co-administration and vaccine administration <6 months of age. Respondents provided ratings of information from different sources (Internet, family/friends, other parents) and trust in doctors. We analyzed vaccine concerns using linear regression analyses that included these information sources after adjusting for socioeconomic variables. Results: Among 618 caregivers, 64% were concerned about vaccine co-administration and 31% were concerned about vaccine administration to infants <6 months of age. Higher ratings of Internet as an important source of information were associated with greater concern about co-administration (b = 0.11, 95% CI: 0.00, 0.22) and concern about administration at <6 months of age (b = 0.17, 95% CI: 0.05, 0.28). Higher ratings given to information from other parents corresponded to 0.24 points greater concern about vaccine co-administration (95% CI: 0.04, 0.44). More trust in doctors and ratings of information from friends and family were not associated with vaccine concerns. Conclusions: Caregiver concerns about vaccine scheduling may limit China’s flexibility to add vaccines to its official immunization schedule. Reporting information about vaccine safety on the Internet and bringing groups of parents together to discuss vaccines might help to ameliorate concerns about vaccine scheduling. Ó 2017 Elsevier Ltd. All rights reserved.
1. Introduction Sustained investments in vaccine research have led to a steady increase in the number of vaccines introduced into national immunization programs. Currently, the World Health Organization (WHO) recommends that countries immunize infants under 12 months of age with 9 vaccines as part of its Expanded Program on Immunization (EPI) [1]. Many of these vaccines involve multiple doses for series completion and the schedule necessitates vaccine ⇑ Corresponding author. E-mail addresses: [email protected] (A.L. Wagner), [email protected] (M.L. Boulton), [email protected] (X. Sun), [email protected] (Z. Huang), [email protected] (I.A. Harmsen), [email protected] (J. Ren), bzikmund@ umich.edu (B.J. Zikmund-Fisher).
co-administration—the administration of multiple vaccines on the same day—to ensure timely administration and to minimize risk of disease. Co-administration of vaccines limits the number of clinic visits while also inducing immunity against vaccinepreventable diseases at an early age [2]. Decades of research have shown that vaccines are highly safe [3], and concurrent administration has a minimal impact on safety [4] or effectiveness of the separate vaccine components [5]. Many parents, politicians, and others have expressed concerns and hesitancy surrounding vaccination, especially towards the perceived ‘‘crowding” of the vaccination schedule [6,7]. Vaccine hesitancy in its full range of expression—from refusal of all vaccines to preferences for alternative vaccination schedules—has mostly been studied in developed countries [8,9]. The prevailing paradigm is that the poor in developing countries cannot access healthcare
http://dx.doi.org/10.1016/j.vaccine.2017.06.077 0264-410X/Ó 2017 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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services and therefore have lower immunization coverage [10,11]. By contrast, individuals of higher socioeconomic status (SES) in developed countries reject or delay vaccination [12,13]. Thus, there remains a need to understand the patterns and correlates of vaccine hesitancy in newly industrialized countries like China. Within developed countries, altering parents’ beliefs about vaccination has proven difficult [14,15], and about half of parents seek out information about vaccination beyond what is provided by the doctor or national public health agencies [16]. How these information sources affect concerns about vaccination are little known in developing countries such as China, which has a rapidly expanding middle class, but which also has a large, and socio-economically disadvantaged, non-local population, i.e. migrants often from rural regions of the country who move into cities [17], and who are more likely to have a delayed administration of vaccines [18]. We have previously identified through qualitative research that Chinese parents worry about vaccine co-administration and administration of ‘‘too many” vaccines for children <6 months [19]. In this study, we estimate the degree to which parents in Shanghai, China, expressed concerns about vaccine coadministration and vaccine administration among children <6 months of age. Subsequently, we assess the association between parents’ stated importance of different information sources (Internet, family and friends, and other parents) and these vaccine concerns.
asked about how worried they were with giving their child two or more vaccines at the same time and then, about giving their child vaccines when the child is under 6 months. Participants responded to all these questions using a 5-point Likert scale from 1 to 5, with 1 being ‘‘not at all worried” and 5 being ‘‘extremely worried.” To describe the prevalence of worry within the population, we created a dichotomous variable, where caregivers with a 4 or 5 on the Likert scale were considered to be ‘‘concerned.” For all other analyses, these questions were analyzed as continuous variables. These variables were never combined and were analyzed separately, but are referred to together as ‘‘concerns about vaccine scheduling.”
2. Methods
2.2.3. Source of information Each question about the source of information on vaccines was prefaced with the phrase ‘‘When deciding on whether to get a vaccine you must pay for,” and subsequently, participants were asked: ‘‘how trustworthy are recommendations from your doctors at the immunization clinic,” ‘‘how important is it for you to look online for information about vaccines yourself,” ‘‘how important is it for you to consult family and friends,” and ‘‘how important is it for you to consult parents in your social group?”
2.1. Study population Caregivers of children aged 8 months to 7 years were invited to participate in this cross-sectional study during May and June of 2014. Details about this sample are available elsewhere [20]. Briefly, we selected caregivers (mothers, fathers, or others – typically grandmothers) into the study through a two-stage, stratified, cluster sampling. The clusters were township immunization clinics. The sample size was based on the aims of another study, and necessitated choosing 31 township immunization clinics and interviewing 20 caregivers at each clinic. Townships were selected by a probability proportionate to size (PPS) systematic selection procedure based on the population of children 0–14 years of age listed in the China 2010 Census. Within each clinic, we selected a convenience sample of at least 20 caregivers who accompanied their child for a vaccination visit and whose sole eligibility criterion was that the child was between 8 months and 7 years of age. Potential participants gave informed consent prior to completing the survey at the immunization clinic. The written survey was in Chinese language and took approximately 20 min to complete; participants were given an incentive of 30 renminbi ($5 USD). The study protocol was approved by the Institutional Review Board at the University of Michigan and an ethical review committee at the Shanghai Centers for Disease Control and Prevention. 2.2. Study measures The questionnaire collected information on caregiver perceptions of pediatric vaccines which were largely derived from questions utilized in previous literature on vaccine hesitancy [16,21– 25], and augmented with additional information drawn from a qualitative, pilot research project on vaccine perceptions (technical report available online [19]).
2.2.2. Numbers of vaccines Additionally, participants were asked what was the largest number of shots they would be willing to give their child during the same clinic visit, how often were they willing to come to the immunization clinic, and how would they describe their willingness to pay for vaccines. The answer choices for these questions were categorical. Because very few parents mentioned that they would be willing to give their child ‘‘3” or ‘‘4” shots, we combined this with the category ‘‘as many as recommended by the doctor.” And because few parents responded that they were willing to come to the clinic ‘‘once a week,” we combined this category with ‘‘a couple of times each month.”
2.3. Statistical analysis First, we described the demographic distribution of participants across demographic groups. Next, we presented mean scores and standard errors (SE) for the stated importance of different informational sources and vaccine concerns. These variables were also stratified by residency status, and the scores between locals and non-locals were compared through a non-parametric Wilcoxon rank-sum test. Finally, we assessed the association between the stated importance of informational sources and concerns about vaccine coadministration and vaccine administration <6 months using two separate multivariable linear regression models adjusted for SES. The b estimates represent the absolute change in the outcome (vaccine concern) on the Likert scale, for a one-unit increase in the predictor variable. Significance was assessed at an a level of 0.05, and precision of results evaluated through 95% confidence intervals (CI). We used survey procedures in the analysis, specifying clusters at the township level and using sampling weights derived from the township selection probability and the proportion of non-locals and locals in the township so that our study population resembled the population distribution by residency status in Shanghai. All analyses were conducted in SAS version 9.4 (SAS Institute, Cary, NC, USA). 3. Results
2.2.1. Vaccine concerns Vaccine concerns were assessed with two separate questions measuring parents’ worries about vaccines. First, parents were
Out of 734 caregivers of children between 8 months and 7 years of age who were approached about the study, 618 (84%) agreed to
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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participate in the survey. Most participants (65%) were mothers of the child, and the rest were either fathers (28%) or other family members (8%), usually grandmothers (Table 1). Overall, 64% of parents were concerned about vaccine coadministration and 31% were concerned about vaccine administration of a child <6 months of age. Only 19% of caregivers indicated that they were willing to receive all non-EPI vaccines at the earliest recommended time (Table 2). Results from the multivariable linear regression models are shown in Table 3. Monthly family income was not a significant predictor of concern about vaccine administration <6 months of age, Table 1 Demographic characteristics of caregivers of young children, Shanghai, 2014. Count Overall Respondent’s relation to child
Weighted proportion (95% CI)
Mother Father Other
618 405 156 57
Sex of child
Male Female Missing
324 292 2
51% (46%, 56%) 49% (44%, 54%)
Residency status
Local Non-local Missing
312 304 2
44% (39%, 48%) 56% (52%, 61%)
Urbanicity
Urban Suburban
338 280
42% (38%, 47%) 58% (53%, 62%)
Respondent’s education
High school or less Some post-secondary education College graduate Missing
235 153
42% (37%, 47%) 23% (19%, 27%)
227 3
35% (30%, 39%)
Monthly family income
<6000 RMB 6 to <10,000 RMB 10,000 RMB Missing
251 156 208 3
43% (38%, 48%) 27% (22%, 31%) 30% (26%, 35%)
Age of child
8 months to <1 year 1 to <2 years 2 to <4 years 4 years
103 198 195 122
17% 32% 32% 19%
65% (60%, 69%) 28% (23%, 32%) 8% (6%, 10%)
(14%, (27%, (27%, (15%,
21%) 36%) 37%) 22%)
but individuals in families that made 6 to <10,000 RMB each year had less concern about vaccine co-administration (b = 0.39, 95% CI: 0.70, 0.08) than families with higher incomes. Education of the caregiver did not impact concern about vaccine coadministration, but individuals with some post-secondary education had more concerns about vaccine administration <6 months of age than college graduates ((b = 0.28, 95% CI: 0.06, 0.50). Stated importance of vaccine information from the Internet was associated with changes in concern about vaccine coadministration (b = 0.11, 95% CI: 0.00, 0.22) and concern about vaccine administration < 6 months of age (b = 0.17, 95% CI: 0.05, 0.28). A 1-point increase in the stated importance of information from other parents corresponded to 0.24 points greater concern about vaccine co-administration (95% CI: 0.04, 0.44), but a marginally nonsignificant association with concern about vaccine administration <6 months of age (b = 0.13, 95% CI: 0.01, 0.28). We did not find significant differences in vaccine concerns between locals and non-locals in the multivariable model, but stated importance of different information sources differed by residency (Table 2). Compared to non-locals, it was more important for locals to obtain information from the Internet, from friends and family, and from other parents. Non-locals were more likely to be willing to come to the clinic as often as needed (44% vs 32% of locals, P = 0.0288), and they were more likely to be willing to receive as many shots as was recommended by the doctor (45% vs 32% of locals, P = 0.0046).
4. Discussion The introduction of new vaccines throughout the world has decreased deaths and disability from vaccine-preventable diseases [26]. However, increasingly complex immunization schedules have prompted greater levels of parental scrutiny and, ultimately, controversy in developed countries [27]. In this cross-sectional study of caregivers of young children in Shanghai, a large majority expressed concerns about vaccine co-administration, while slightly less than a third were concerned about vaccine administration in infants <6 months of age. Higher income, rating vaccine information from the Internet as important, and attaching greater
Table 2 Vaccine concerns and sources of information about vaccines among local and non-local caregivers of young children, Shanghai, 2014.
Trustworthiness of doctor, mean ± SE Importance of information from internet, mean ± SE Importance of information from friends and family, mean ± SE Importance of information from other parents, mean ± SE Concern about vaccine co-administration, mean ± SE Concern about vaccine administration < 6 months, mean ± SE Maximum number of shots willing to give child, count (%) 1 2 As many as recommended Frequency of time willing to come to clinic, count (%) As often as needed A couple of times each month Once a month Every other month A few times a year Willingness to pay for vaccines, count (%) Receive all for-fee vaccines at the earliest recommended time Receive all for-fee vaccines, but some delayed Refuse some for-fee vaccines Refuse all for-fee vaccines
Overall
Locals
Non-locals
P-valuea
4.11 ± 0.04 3.66 ± 0.07 3.75 ± 0.09 3.57 ± 0.09 3.32 ± 0.12 2.48 ± 0.08
4.14 ± 0.05 3.85 ± 0.06 3.84 ± 0.06 3.73 ± 0.07 3.22 ± 0.11 2.40 ± 0.12
4.09 ± 0.06 3.52 ± 0.11 3.68 ± 0.14 3.45 ± 0.13 3.42 ± 0.19 2.54 ± 0.12
0.2255 0.0007 0.0381 0.0024 0.0125 0.0762 0.0046
185 (30%) 188 (31%) 241 (39%)
106 (34%) 98 (34%) 107 (32%)
79 (27%) 90 (28%) 134 (45%)
224 (39%) 98 (16%) 202 (32%) 38 (5%) 53 (8%)
107 (32%) 50 (19%) 104 (32%) 21 (7%) 30 (10%)
117 (44%) 48 (14%) 98 (32%) 17 (4%) 23 (6%)
109 (19%) 131 (21%) 344 (55%) 29 (4%)
52 (16%) 65 (21%) 178 (58%) 15 (5%)
57 (22%) 66 (21%) 166 (53%) 14 (4%)
0.0288
0.3741
Notes: SE, standard error (from the Taylor series variance estimation method). a Significance of the value for locals compared to the value for non-locals, from the Wilcoxon rank-sum test (for continuous variables) or Rao-Scott chi-square test (for categorical variables).
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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Table 3 The association between information source and vaccine concerns according to linear regression models, caregivers of young children, Shanghai, 2014.
Intercepta Relation to child Mother Father Other Child’s sex (female vs male) Non-local vs local Suburban vs urban dweller Respondent’s education High school or less Some post-secondary education College graduate Monthly family income <6000 RMB 6 to <10,000 RMB 10,000 RMB Age of child 8 months to <1 year 1 to <2 years 2 to <4 years 4 years Trustworthiness of doctor Importance of information from internet Importance of information from friends and family Importance of information from other parents
Concern about vaccine co-administration b (95% CI)
Concern about vaccine administration < 6 months b (95% CI)
2.90 (2.46, 3.34)*
1.96 (1.49, 2.44)*
Ref 0.12 ( 0.04 ( 0.16 ( 0.23 ( 0.11
Ref 0.20 ( 0.09 0.19 ( 0.21 ( 0.20
0.09, 0.32) 0.45, 0.53) 0.08, 0.41) 0.11, 0.56) ( 0.46, 0.25)
0.05, 0.44) ( 0.63, 0.44) 0.01, 0.38) 0.07, 0.49) ( 0.50, 0.09)
0.41 ( 0.07, 0.90) 0.33 (0.00, 0.65) Ref
0.24 ( 0.11, 0.59) 0.28 (0.06, 0.50)* Ref
0.21 ( 0.56, 0.14) 0.39 ( 0.70, 0.08)* Ref
0.08 ( 0.45, 0.28) 0.06 ( 0.31, 0.19) Ref
0.32 (0.00, 0.63)* 0.01 ( 0.26, 0.24) 0.07 ( 0.15, 0.28) Ref 0.13 ( 0.28, 0.02) 0.11 (0.00, 0.22)* 0.06 ( 0.13, 0.25) 0.24 (0.04, 0.44)*
0.24 ( 0.14, 0.62) 0.08 ( 0.28, 0.44) 0.08 ( 0.22, 0.37) Ref 0.09 ( 0.20, 0.03) 0.17 (0.05, 0.28)* 0.09 ( 0.03, 0.21) 0.13 ( 0.01, 0.28)
Notes: CI: confidence interval. a Intercept is the mean value when all trust and information variables were set to a value of ‘‘3”. * P < 0.05.
importance to information from other parents were all associated with more concerns about vaccine scheduling. With the world’s second largest birth cohort, China’s government is tasked with initiating vaccination of 18 million new babies each year. Unlike many other countries, China has instituted a twotier vaccination system [28,29]. Vaccines that are part of the EPI (e.g., Bacillus Calmette-Guérin, polio vaccine, diphtheria-tetanuspertussis vaccine (DTP), and measles vaccine), are given for free to children (both local and non-local) with the recommended schedules provided by the Chinese Government’s Experts Advisory Committee on Immunization Program [29]. Non-EPI vaccines, (such as Haemophilus influenzae type b vaccine or rotavirus vaccine), are administered in the same clinics as EPI vaccines, but require payment. For these non-EPI vaccines, the Chinese government does not make official recommendations for vaccination age beyond what is explicitly stated in the manufacturer’s instructions, and in actual practice these non-EPI vaccines are often only administered when the child is over 1 or 2 years of age [28]. In contrast to many countries, which have vaccination schedules requiring administration of several pediatric vaccines during the same visit (e.g., at 2, 4, and 6 months of age), Chinese infants <6 months of age following the official EPI schedule will usually receive only 2 vaccines, at most, during one office visit [29]. Official guidelines, however, allow for co-administration if the vaccines are injected on different anatomical sites [30]. One study of electronic vaccination records in Shanghai found that only 10.3% of DTP1 doses were co-administered with any other vaccine [31]. Consequently, Chinese families have to return to immunization clinics more frequently to complete a given multi-dose vaccination series. Previous studies in developed countries have found that it is wealthier and more educated groups of people who are more likely to actively choose to reject or delay vaccination [12,13]. We found very few SES factors that were significantly related to vaccine concerns other than that more income was related to greater concerns about vaccine co-administration. Conversely, we also found that
more education was related to less concern about vaccine administration <6 months of age, opposite trends in developing countries. It is perhaps not surprising that China, as a rapidly developing economy, reflects some, but not all, of the trends in vaccine hesitancy seen in developing countries. More research is needed on how rapidly growing numbers of middle class parents from middle income countries like China make decisions about vaccinating their children [32], and what sources of information could make them more positively view vaccinations. Armed with such information, public health would be better able to preemptively address issues arising around vaccine hesitancy which have now become entrenched and difficult to respond to among the affluent in high income countries. Consulting a wide range of information sources was important for caregivers in this study. A study by Freed et al. about vaccine information sources in the US also found that American adults utilize several sources to obtain information about vaccine safety [33]. Other studies have shown the importance of healthcare providers in particular; one survey in the US found a high degree of concordance in positive vaccine beliefs (such as belief in the community benefit of vaccination or that vaccines were safe) between parents and providers [34]. Providers often overestimate parental concerns about vaccines, including co-administration [35], and can mitigate delays in vaccination through the use of communication which is presumptive and confident (e.g., ‘‘Today your child will be receiving four vaccines”) and not participative (e.g., ‘‘How many vaccines will your child be receiving today?”) [36]. In Freed et al.’s study, parents trusted information from websites of doctor groups more than any other website, including government websites, websites from vaccine manufacturers, and websites from anti-vaccine groups [33]. Future research in China could also tease out how parents view websites from different sources, especially as the exact methods for how people obtain health information online, including how they perform searches, what websites they view, and when they performed searches
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(relative to clinic appointments) is unclear [37]. Health care workers should also become familiar with material put forward by antivaccine movements on the internet in order to counter it within their own practice [38]. However, we did not measure beliefs that vaccination providers in China have regarding vaccine coadministration, and we caution against the direct application of studies about health messaging in Western countries onto the Chinese context. The importance of information from the Internet, from friends and family, and from other parents, was greater for locals than non-locals. Other studies have confirmed that migrants have less access to healthcare information online [39]. Non-locals could be less familiar with the Internet as a source of information about health. We also found that non locals were more likely to follow directions from doctors (specifically – obtain the number of shots recommended by the doctor and come to the clinic more often than locals). This suggests that the non-local migrants place greater trust in authorities than locals. Other research, for example, at three different sites in southern and eastern China found that migrants placed greater trust in police than local urbanites [40]. 4.1. Policy implications This study did not measure parents’ adherence to alternative vaccination schedules. Previous research in developed countries has shown that a substantial minority of parents choose to intentionally delay vaccination. In New York state, 25% of children were on a delayed vaccination schedule [7]. Because delayed vaccination can negatively impact up-to-date vaccination status and, therefore, the timely development of immunity, physicians typically recommend a compact schedule of vaccination for infants. It is interesting that China’s official immunization schedule has some similarities to Robert Sears’s popular alternative immunization schedule [41], in that typically only 2 vaccines will be administered at each clinic visit. However, there are also differences: infants are vaccinated at birth, and by having more frequent visits to the clinic than recommended in Sears’s alternative schedule, Chinese children can complete the primary series of DTP, polio vaccine, and hepatitis B vaccine around the same time as children in the US. Even so, more immunization appointments could be burdensome to Chinese parents. Interestingly, the manufacturer’s instructions for 7-valent pneumococcal conjugate vaccine, which was on the market between 2008 and 2015 [42], stated that it should not be co-administered with other vaccines, even though it is in other countries. And a new enterovirus 71 vaccine to be introduced in China has been given the recommendation for no coadministration, although there is no evidence for this guidance [43]. More transparency is needed on how the immunization schedule is constructed and on how manufacturers’ instructions inform this schedule. 4.2. Strengths and limitations Because our study is cross-sectional, we cannot infer causality, or even temporality, between people’s stated importance of various information sources (the main explanatory variables) and their concerns about vaccination (the outcomes). Additionally, by sampling individuals at immunization clinics, we are biasing our sample towards individuals with positive vaccination beliefs. However, vaccination in China is mandatory for school entry, and participation in immunization clinics has remained high. In a study of nonlocal families in Beijing, only 12% had not visited an immunization clinic [44]. The strengths of our study were that we drew from a sample of 31 clinics throughout the city and used survey procedures in the analysis, and therefore are able to make generalizations about the state of vaccine confidence within Shanghai.
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5. Conclusions This study found that most caregivers of young children in China are concerned about vaccine co-administration and that attaching greater importance to information from the Internet or from other parents was associated with more concerns about vaccine scheduling. Concerns about vaccine scheduling in the populace may limit China’s flexibility in the future to add vaccines to its official immunization schedule, especially given that China has already prioritized a slightly extended vaccination schedule over fewer visits to immunization clinics with more doses administered per visit [29]. Conflicts of interest We declare no conflicts of interest. Author contributions AW contributed to data analysis and drafting of the article. MB contributed to design of the study, interpretation of the data, and revision of the manuscript for important intellectual content. XS supervised data collection, contributed to interpretation of the data, and revision of the manuscript for important intellectual content. HR and ZH contributed to acquisition of data, interpretation of data, and revision of the manuscript for important intellectual content. IH contributed to questionnaire design, data interpretation, and revision of the manuscript for important intellectual content. BZ contributed to design of the study, data analysis and interpretation, and revision of the manuscript for important intellectual content. Acknowledgements This research was funded by the University of Michigan Office of Global Public Health and by a University of Michigan Rackham International Research Award. We appreciate the local Centers for Disease Control and Prevention staff and immunization clinic staff who coordinated site visits and interviews. References [1] Advisory Committee on Immunization Practices. Recommended Immunization Schedules for Persons Aged 0 — Through 18 Years: UNITED STATES, 2016 2016. [accessed November 10, 2016]. [2] CDC. General Recommendations on Immunization. Epidemiol. Prev. VaccinePreventable Dis. 13th ed., Washington, DC: Public Health Foundation; 2012, p. 9–30. [3] Maglione MA, Das L, Raaen L, Smith A, Chari R, Newberry S, et al. Safety of vaccines used for routine immunization of us children: a systematic review. Pediatrics 2014;134:325–37. http://dx.doi.org/10.1542/peds.2014-1079. [4] Tse A, Tseng HF, Greene SK, Vellozzi C, Lee GM. Signal identification and evaluation for risk of febrile seizures in children following trivalent inactivated influenza vaccine in the Vaccine Safety Datalink Project, 2010–2011. Vaccine 2012;30:2024–31. http://dx.doi.org/10.1016/j.vaccine.2012.01.027. [5] Klugman KP, Black S, Dagan R, Malley R, Whitney CG. Pneumococcal conjugate vaccine and pneumococcal common protein vaccines. In: Plotkin SA, Orenstein WA, Offit PA, editors. Vaccines. Philadelphia, PA: Elsevier; 2013. p. 504–41. [6] Larson HJ, Jarrett C, Eckersberger E, Smith DMD, Paterson P. Understanding vaccine hesitancy around vaccines and vaccination from a global perspective: A systematic review of published literature, 2007–2012. Vaccine 2014;32:2150–9. http://dx.doi.org/10.1016/j.vaccine.2014.01.081. [7] Nadeau JA, Bednarczyk RA, Masawi MR, Meldrum MD, Santilli L, Zansky SM, et al. Vaccinating my way - use of alternative vaccination schedules in New York State. J Pediatr 2015;166(151–156):e1. http://dx.doi.org/10.1016/j. jpeds.2014.09.013. [8] Larson HJ, Schulz W. The state of vaccine confidence 2015. London: London School of Hygiene and Tropical Medicine; 2015. [9] Cobos Munoz D, Monzon Llamas L, Bosch-Capblanch X. Exposing concerns about vaccination in low- and middle-income countries: a systematic review. Int J Public Health 2015;60:767–80. http://dx.doi.org/10.1007/s00038-0150715-6.
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Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Parents’ concerns about vaccine scheduling in Shanghai, China Abram L. Wagner a,⇑, Matthew L. Boulton a,b, Xiaodong Sun c, Zhuoying Huang c, Irene A. Harmsen d, Jia Ren c, Brian J. Zikmund-Fisher e a
Department of Epidemiology, School of Public Health, University of Michigan, 1415 Washington Heights, Ann Arbor, MI 48109, USA Department of Internal Medicine, Division of Infectious Diseases, University of Michigan Medical School, 1500 East Medical Center Drive, Ann Arbor, MI 48109, USA c Department of Immunization Program, Shanghai Municipal Centers for Disease Control & Prevention, NO. 1380, West Zhongshan Road, 200336 Shanghai, China d Department of Epidemiology and Health Promotion, Public Health Service of Amsterdam, Amsterdam, The Netherlands e Department of Health Behavior & Health Education, School of Public Health, University of Michigan, 1415 Washington Heights, Ann Arbor, MI 48109, USA b
a r t i c l e
i n f o
Article history: Received 1 February 2017 Received in revised form 21 June 2017 Accepted 23 June 2017 Available online xxxx Keywords: Anti-vaccination movement Vaccine hesitancy China Immunization schedule Vaccine refusal
a b s t r a c t Background: Several new vaccines have been introduced into China in recent years, but some parents in China have shown concerns about the scheduling of vaccinations for young infants. This study explores caregiver concerns about children receiving multiple vaccines during a single visit and about vaccine administration in infants <6 months, and assesses the degree to which these concerns are associated with ratings of the importance of different sources of vaccine information in Shanghai. Methods: Caregivers of children 8 months to 7 years presenting at immunization clinics in Shanghai completed a survey about vaccine co-administration and vaccine administration <6 months of age. Respondents provided ratings of information from different sources (Internet, family/friends, other parents) and trust in doctors. We analyzed vaccine concerns using linear regression analyses that included these information sources after adjusting for socioeconomic variables. Results: Among 618 caregivers, 64% were concerned about vaccine co-administration and 31% were concerned about vaccine administration to infants <6 months of age. Higher ratings of Internet as an important source of information were associated with greater concern about co-administration (b = 0.11, 95% CI: 0.00, 0.22) and concern about administration at <6 months of age (b = 0.17, 95% CI: 0.05, 0.28). Higher ratings given to information from other parents corresponded to 0.24 points greater concern about vaccine co-administration (95% CI: 0.04, 0.44). More trust in doctors and ratings of information from friends and family were not associated with vaccine concerns. Conclusions: Caregiver concerns about vaccine scheduling may limit China’s flexibility to add vaccines to its official immunization schedule. Reporting information about vaccine safety on the Internet and bringing groups of parents together to discuss vaccines might help to ameliorate concerns about vaccine scheduling. Ó 2017 Elsevier Ltd. All rights reserved.
1. Introduction Sustained investments in vaccine research have led to a steady increase in the number of vaccines introduced into national immunization programs. Currently, the World Health Organization (WHO) recommends that countries immunize infants under 12 months of age with 9 vaccines as part of its Expanded Program on Immunization (EPI) [1]. Many of these vaccines involve multiple doses for series completion and the schedule necessitates vaccine ⇑ Corresponding author. E-mail addresses: [email protected] (A.L. Wagner), [email protected] (M.L. Boulton), [email protected] (X. Sun), [email protected] (Z. Huang), [email protected] (I.A. Harmsen), [email protected] (J. Ren), bzikmund@ umich.edu (B.J. Zikmund-Fisher).
co-administration—the administration of multiple vaccines on the same day—to ensure timely administration and to minimize risk of disease. Co-administration of vaccines limits the number of clinic visits while also inducing immunity against vaccinepreventable diseases at an early age [2]. Decades of research have shown that vaccines are highly safe [3], and concurrent administration has a minimal impact on safety [4] or effectiveness of the separate vaccine components [5]. Many parents, politicians, and others have expressed concerns and hesitancy surrounding vaccination, especially towards the perceived ‘‘crowding” of the vaccination schedule [6,7]. Vaccine hesitancy in its full range of expression—from refusal of all vaccines to preferences for alternative vaccination schedules—has mostly been studied in developed countries [8,9]. The prevailing paradigm is that the poor in developing countries cannot access healthcare
http://dx.doi.org/10.1016/j.vaccine.2017.06.077 0264-410X/Ó 2017 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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services and therefore have lower immunization coverage [10,11]. By contrast, individuals of higher socioeconomic status (SES) in developed countries reject or delay vaccination [12,13]. Thus, there remains a need to understand the patterns and correlates of vaccine hesitancy in newly industrialized countries like China. Within developed countries, altering parents’ beliefs about vaccination has proven difficult [14,15], and about half of parents seek out information about vaccination beyond what is provided by the doctor or national public health agencies [16]. How these information sources affect concerns about vaccination are little known in developing countries such as China, which has a rapidly expanding middle class, but which also has a large, and socio-economically disadvantaged, non-local population, i.e. migrants often from rural regions of the country who move into cities [17], and who are more likely to have a delayed administration of vaccines [18]. We have previously identified through qualitative research that Chinese parents worry about vaccine co-administration and administration of ‘‘too many” vaccines for children <6 months [19]. In this study, we estimate the degree to which parents in Shanghai, China, expressed concerns about vaccine coadministration and vaccine administration among children <6 months of age. Subsequently, we assess the association between parents’ stated importance of different information sources (Internet, family and friends, and other parents) and these vaccine concerns.
asked about how worried they were with giving their child two or more vaccines at the same time and then, about giving their child vaccines when the child is under 6 months. Participants responded to all these questions using a 5-point Likert scale from 1 to 5, with 1 being ‘‘not at all worried” and 5 being ‘‘extremely worried.” To describe the prevalence of worry within the population, we created a dichotomous variable, where caregivers with a 4 or 5 on the Likert scale were considered to be ‘‘concerned.” For all other analyses, these questions were analyzed as continuous variables. These variables were never combined and were analyzed separately, but are referred to together as ‘‘concerns about vaccine scheduling.”
2. Methods
2.2.3. Source of information Each question about the source of information on vaccines was prefaced with the phrase ‘‘When deciding on whether to get a vaccine you must pay for,” and subsequently, participants were asked: ‘‘how trustworthy are recommendations from your doctors at the immunization clinic,” ‘‘how important is it for you to look online for information about vaccines yourself,” ‘‘how important is it for you to consult family and friends,” and ‘‘how important is it for you to consult parents in your social group?”
2.1. Study population Caregivers of children aged 8 months to 7 years were invited to participate in this cross-sectional study during May and June of 2014. Details about this sample are available elsewhere [20]. Briefly, we selected caregivers (mothers, fathers, or others – typically grandmothers) into the study through a two-stage, stratified, cluster sampling. The clusters were township immunization clinics. The sample size was based on the aims of another study, and necessitated choosing 31 township immunization clinics and interviewing 20 caregivers at each clinic. Townships were selected by a probability proportionate to size (PPS) systematic selection procedure based on the population of children 0–14 years of age listed in the China 2010 Census. Within each clinic, we selected a convenience sample of at least 20 caregivers who accompanied their child for a vaccination visit and whose sole eligibility criterion was that the child was between 8 months and 7 years of age. Potential participants gave informed consent prior to completing the survey at the immunization clinic. The written survey was in Chinese language and took approximately 20 min to complete; participants were given an incentive of 30 renminbi ($5 USD). The study protocol was approved by the Institutional Review Board at the University of Michigan and an ethical review committee at the Shanghai Centers for Disease Control and Prevention. 2.2. Study measures The questionnaire collected information on caregiver perceptions of pediatric vaccines which were largely derived from questions utilized in previous literature on vaccine hesitancy [16,21– 25], and augmented with additional information drawn from a qualitative, pilot research project on vaccine perceptions (technical report available online [19]).
2.2.2. Numbers of vaccines Additionally, participants were asked what was the largest number of shots they would be willing to give their child during the same clinic visit, how often were they willing to come to the immunization clinic, and how would they describe their willingness to pay for vaccines. The answer choices for these questions were categorical. Because very few parents mentioned that they would be willing to give their child ‘‘3” or ‘‘4” shots, we combined this with the category ‘‘as many as recommended by the doctor.” And because few parents responded that they were willing to come to the clinic ‘‘once a week,” we combined this category with ‘‘a couple of times each month.”
2.3. Statistical analysis First, we described the demographic distribution of participants across demographic groups. Next, we presented mean scores and standard errors (SE) for the stated importance of different informational sources and vaccine concerns. These variables were also stratified by residency status, and the scores between locals and non-locals were compared through a non-parametric Wilcoxon rank-sum test. Finally, we assessed the association between the stated importance of informational sources and concerns about vaccine coadministration and vaccine administration <6 months using two separate multivariable linear regression models adjusted for SES. The b estimates represent the absolute change in the outcome (vaccine concern) on the Likert scale, for a one-unit increase in the predictor variable. Significance was assessed at an a level of 0.05, and precision of results evaluated through 95% confidence intervals (CI). We used survey procedures in the analysis, specifying clusters at the township level and using sampling weights derived from the township selection probability and the proportion of non-locals and locals in the township so that our study population resembled the population distribution by residency status in Shanghai. All analyses were conducted in SAS version 9.4 (SAS Institute, Cary, NC, USA). 3. Results
2.2.1. Vaccine concerns Vaccine concerns were assessed with two separate questions measuring parents’ worries about vaccines. First, parents were
Out of 734 caregivers of children between 8 months and 7 years of age who were approached about the study, 618 (84%) agreed to
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participate in the survey. Most participants (65%) were mothers of the child, and the rest were either fathers (28%) or other family members (8%), usually grandmothers (Table 1). Overall, 64% of parents were concerned about vaccine coadministration and 31% were concerned about vaccine administration of a child <6 months of age. Only 19% of caregivers indicated that they were willing to receive all non-EPI vaccines at the earliest recommended time (Table 2). Results from the multivariable linear regression models are shown in Table 3. Monthly family income was not a significant predictor of concern about vaccine administration <6 months of age, Table 1 Demographic characteristics of caregivers of young children, Shanghai, 2014. Count Overall Respondent’s relation to child
Weighted proportion (95% CI)
Mother Father Other
618 405 156 57
Sex of child
Male Female Missing
324 292 2
51% (46%, 56%) 49% (44%, 54%)
Residency status
Local Non-local Missing
312 304 2
44% (39%, 48%) 56% (52%, 61%)
Urbanicity
Urban Suburban
338 280
42% (38%, 47%) 58% (53%, 62%)
Respondent’s education
High school or less Some post-secondary education College graduate Missing
235 153
42% (37%, 47%) 23% (19%, 27%)
227 3
35% (30%, 39%)
Monthly family income
<6000 RMB 6 to <10,000 RMB 10,000 RMB Missing
251 156 208 3
43% (38%, 48%) 27% (22%, 31%) 30% (26%, 35%)
Age of child
8 months to <1 year 1 to <2 years 2 to <4 years 4 years
103 198 195 122
17% 32% 32% 19%
65% (60%, 69%) 28% (23%, 32%) 8% (6%, 10%)
(14%, (27%, (27%, (15%,
21%) 36%) 37%) 22%)
but individuals in families that made 6 to <10,000 RMB each year had less concern about vaccine co-administration (b = 0.39, 95% CI: 0.70, 0.08) than families with higher incomes. Education of the caregiver did not impact concern about vaccine coadministration, but individuals with some post-secondary education had more concerns about vaccine administration <6 months of age than college graduates ((b = 0.28, 95% CI: 0.06, 0.50). Stated importance of vaccine information from the Internet was associated with changes in concern about vaccine coadministration (b = 0.11, 95% CI: 0.00, 0.22) and concern about vaccine administration < 6 months of age (b = 0.17, 95% CI: 0.05, 0.28). A 1-point increase in the stated importance of information from other parents corresponded to 0.24 points greater concern about vaccine co-administration (95% CI: 0.04, 0.44), but a marginally nonsignificant association with concern about vaccine administration <6 months of age (b = 0.13, 95% CI: 0.01, 0.28). We did not find significant differences in vaccine concerns between locals and non-locals in the multivariable model, but stated importance of different information sources differed by residency (Table 2). Compared to non-locals, it was more important for locals to obtain information from the Internet, from friends and family, and from other parents. Non-locals were more likely to be willing to come to the clinic as often as needed (44% vs 32% of locals, P = 0.0288), and they were more likely to be willing to receive as many shots as was recommended by the doctor (45% vs 32% of locals, P = 0.0046).
4. Discussion The introduction of new vaccines throughout the world has decreased deaths and disability from vaccine-preventable diseases [26]. However, increasingly complex immunization schedules have prompted greater levels of parental scrutiny and, ultimately, controversy in developed countries [27]. In this cross-sectional study of caregivers of young children in Shanghai, a large majority expressed concerns about vaccine co-administration, while slightly less than a third were concerned about vaccine administration in infants <6 months of age. Higher income, rating vaccine information from the Internet as important, and attaching greater
Table 2 Vaccine concerns and sources of information about vaccines among local and non-local caregivers of young children, Shanghai, 2014.
Trustworthiness of doctor, mean ± SE Importance of information from internet, mean ± SE Importance of information from friends and family, mean ± SE Importance of information from other parents, mean ± SE Concern about vaccine co-administration, mean ± SE Concern about vaccine administration < 6 months, mean ± SE Maximum number of shots willing to give child, count (%) 1 2 As many as recommended Frequency of time willing to come to clinic, count (%) As often as needed A couple of times each month Once a month Every other month A few times a year Willingness to pay for vaccines, count (%) Receive all for-fee vaccines at the earliest recommended time Receive all for-fee vaccines, but some delayed Refuse some for-fee vaccines Refuse all for-fee vaccines
Overall
Locals
Non-locals
P-valuea
4.11 ± 0.04 3.66 ± 0.07 3.75 ± 0.09 3.57 ± 0.09 3.32 ± 0.12 2.48 ± 0.08
4.14 ± 0.05 3.85 ± 0.06 3.84 ± 0.06 3.73 ± 0.07 3.22 ± 0.11 2.40 ± 0.12
4.09 ± 0.06 3.52 ± 0.11 3.68 ± 0.14 3.45 ± 0.13 3.42 ± 0.19 2.54 ± 0.12
0.2255 0.0007 0.0381 0.0024 0.0125 0.0762 0.0046
185 (30%) 188 (31%) 241 (39%)
106 (34%) 98 (34%) 107 (32%)
79 (27%) 90 (28%) 134 (45%)
224 (39%) 98 (16%) 202 (32%) 38 (5%) 53 (8%)
107 (32%) 50 (19%) 104 (32%) 21 (7%) 30 (10%)
117 (44%) 48 (14%) 98 (32%) 17 (4%) 23 (6%)
109 (19%) 131 (21%) 344 (55%) 29 (4%)
52 (16%) 65 (21%) 178 (58%) 15 (5%)
57 (22%) 66 (21%) 166 (53%) 14 (4%)
0.0288
0.3741
Notes: SE, standard error (from the Taylor series variance estimation method). a Significance of the value for locals compared to the value for non-locals, from the Wilcoxon rank-sum test (for continuous variables) or Rao-Scott chi-square test (for categorical variables).
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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Table 3 The association between information source and vaccine concerns according to linear regression models, caregivers of young children, Shanghai, 2014.
Intercepta Relation to child Mother Father Other Child’s sex (female vs male) Non-local vs local Suburban vs urban dweller Respondent’s education High school or less Some post-secondary education College graduate Monthly family income <6000 RMB 6 to <10,000 RMB 10,000 RMB Age of child 8 months to <1 year 1 to <2 years 2 to <4 years 4 years Trustworthiness of doctor Importance of information from internet Importance of information from friends and family Importance of information from other parents
Concern about vaccine co-administration b (95% CI)
Concern about vaccine administration < 6 months b (95% CI)
2.90 (2.46, 3.34)*
1.96 (1.49, 2.44)*
Ref 0.12 ( 0.04 ( 0.16 ( 0.23 ( 0.11
Ref 0.20 ( 0.09 0.19 ( 0.21 ( 0.20
0.09, 0.32) 0.45, 0.53) 0.08, 0.41) 0.11, 0.56) ( 0.46, 0.25)
0.05, 0.44) ( 0.63, 0.44) 0.01, 0.38) 0.07, 0.49) ( 0.50, 0.09)
0.41 ( 0.07, 0.90) 0.33 (0.00, 0.65) Ref
0.24 ( 0.11, 0.59) 0.28 (0.06, 0.50)* Ref
0.21 ( 0.56, 0.14) 0.39 ( 0.70, 0.08)* Ref
0.08 ( 0.45, 0.28) 0.06 ( 0.31, 0.19) Ref
0.32 (0.00, 0.63)* 0.01 ( 0.26, 0.24) 0.07 ( 0.15, 0.28) Ref 0.13 ( 0.28, 0.02) 0.11 (0.00, 0.22)* 0.06 ( 0.13, 0.25) 0.24 (0.04, 0.44)*
0.24 ( 0.14, 0.62) 0.08 ( 0.28, 0.44) 0.08 ( 0.22, 0.37) Ref 0.09 ( 0.20, 0.03) 0.17 (0.05, 0.28)* 0.09 ( 0.03, 0.21) 0.13 ( 0.01, 0.28)
Notes: CI: confidence interval. a Intercept is the mean value when all trust and information variables were set to a value of ‘‘3”. * P < 0.05.
importance to information from other parents were all associated with more concerns about vaccine scheduling. With the world’s second largest birth cohort, China’s government is tasked with initiating vaccination of 18 million new babies each year. Unlike many other countries, China has instituted a twotier vaccination system [28,29]. Vaccines that are part of the EPI (e.g., Bacillus Calmette-Guérin, polio vaccine, diphtheria-tetanuspertussis vaccine (DTP), and measles vaccine), are given for free to children (both local and non-local) with the recommended schedules provided by the Chinese Government’s Experts Advisory Committee on Immunization Program [29]. Non-EPI vaccines, (such as Haemophilus influenzae type b vaccine or rotavirus vaccine), are administered in the same clinics as EPI vaccines, but require payment. For these non-EPI vaccines, the Chinese government does not make official recommendations for vaccination age beyond what is explicitly stated in the manufacturer’s instructions, and in actual practice these non-EPI vaccines are often only administered when the child is over 1 or 2 years of age [28]. In contrast to many countries, which have vaccination schedules requiring administration of several pediatric vaccines during the same visit (e.g., at 2, 4, and 6 months of age), Chinese infants <6 months of age following the official EPI schedule will usually receive only 2 vaccines, at most, during one office visit [29]. Official guidelines, however, allow for co-administration if the vaccines are injected on different anatomical sites [30]. One study of electronic vaccination records in Shanghai found that only 10.3% of DTP1 doses were co-administered with any other vaccine [31]. Consequently, Chinese families have to return to immunization clinics more frequently to complete a given multi-dose vaccination series. Previous studies in developed countries have found that it is wealthier and more educated groups of people who are more likely to actively choose to reject or delay vaccination [12,13]. We found very few SES factors that were significantly related to vaccine concerns other than that more income was related to greater concerns about vaccine co-administration. Conversely, we also found that
more education was related to less concern about vaccine administration <6 months of age, opposite trends in developing countries. It is perhaps not surprising that China, as a rapidly developing economy, reflects some, but not all, of the trends in vaccine hesitancy seen in developing countries. More research is needed on how rapidly growing numbers of middle class parents from middle income countries like China make decisions about vaccinating their children [32], and what sources of information could make them more positively view vaccinations. Armed with such information, public health would be better able to preemptively address issues arising around vaccine hesitancy which have now become entrenched and difficult to respond to among the affluent in high income countries. Consulting a wide range of information sources was important for caregivers in this study. A study by Freed et al. about vaccine information sources in the US also found that American adults utilize several sources to obtain information about vaccine safety [33]. Other studies have shown the importance of healthcare providers in particular; one survey in the US found a high degree of concordance in positive vaccine beliefs (such as belief in the community benefit of vaccination or that vaccines were safe) between parents and providers [34]. Providers often overestimate parental concerns about vaccines, including co-administration [35], and can mitigate delays in vaccination through the use of communication which is presumptive and confident (e.g., ‘‘Today your child will be receiving four vaccines”) and not participative (e.g., ‘‘How many vaccines will your child be receiving today?”) [36]. In Freed et al.’s study, parents trusted information from websites of doctor groups more than any other website, including government websites, websites from vaccine manufacturers, and websites from anti-vaccine groups [33]. Future research in China could also tease out how parents view websites from different sources, especially as the exact methods for how people obtain health information online, including how they perform searches, what websites they view, and when they performed searches
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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(relative to clinic appointments) is unclear [37]. Health care workers should also become familiar with material put forward by antivaccine movements on the internet in order to counter it within their own practice [38]. However, we did not measure beliefs that vaccination providers in China have regarding vaccine coadministration, and we caution against the direct application of studies about health messaging in Western countries onto the Chinese context. The importance of information from the Internet, from friends and family, and from other parents, was greater for locals than non-locals. Other studies have confirmed that migrants have less access to healthcare information online [39]. Non-locals could be less familiar with the Internet as a source of information about health. We also found that non locals were more likely to follow directions from doctors (specifically – obtain the number of shots recommended by the doctor and come to the clinic more often than locals). This suggests that the non-local migrants place greater trust in authorities than locals. Other research, for example, at three different sites in southern and eastern China found that migrants placed greater trust in police than local urbanites [40]. 4.1. Policy implications This study did not measure parents’ adherence to alternative vaccination schedules. Previous research in developed countries has shown that a substantial minority of parents choose to intentionally delay vaccination. In New York state, 25% of children were on a delayed vaccination schedule [7]. Because delayed vaccination can negatively impact up-to-date vaccination status and, therefore, the timely development of immunity, physicians typically recommend a compact schedule of vaccination for infants. It is interesting that China’s official immunization schedule has some similarities to Robert Sears’s popular alternative immunization schedule [41], in that typically only 2 vaccines will be administered at each clinic visit. However, there are also differences: infants are vaccinated at birth, and by having more frequent visits to the clinic than recommended in Sears’s alternative schedule, Chinese children can complete the primary series of DTP, polio vaccine, and hepatitis B vaccine around the same time as children in the US. Even so, more immunization appointments could be burdensome to Chinese parents. Interestingly, the manufacturer’s instructions for 7-valent pneumococcal conjugate vaccine, which was on the market between 2008 and 2015 [42], stated that it should not be co-administered with other vaccines, even though it is in other countries. And a new enterovirus 71 vaccine to be introduced in China has been given the recommendation for no coadministration, although there is no evidence for this guidance [43]. More transparency is needed on how the immunization schedule is constructed and on how manufacturers’ instructions inform this schedule. 4.2. Strengths and limitations Because our study is cross-sectional, we cannot infer causality, or even temporality, between people’s stated importance of various information sources (the main explanatory variables) and their concerns about vaccination (the outcomes). Additionally, by sampling individuals at immunization clinics, we are biasing our sample towards individuals with positive vaccination beliefs. However, vaccination in China is mandatory for school entry, and participation in immunization clinics has remained high. In a study of nonlocal families in Beijing, only 12% had not visited an immunization clinic [44]. The strengths of our study were that we drew from a sample of 31 clinics throughout the city and used survey procedures in the analysis, and therefore are able to make generalizations about the state of vaccine confidence within Shanghai.
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5. Conclusions This study found that most caregivers of young children in China are concerned about vaccine co-administration and that attaching greater importance to information from the Internet or from other parents was associated with more concerns about vaccine scheduling. Concerns about vaccine scheduling in the populace may limit China’s flexibility in the future to add vaccines to its official immunization schedule, especially given that China has already prioritized a slightly extended vaccination schedule over fewer visits to immunization clinics with more doses administered per visit [29]. Conflicts of interest We declare no conflicts of interest. Author contributions AW contributed to data analysis and drafting of the article. MB contributed to design of the study, interpretation of the data, and revision of the manuscript for important intellectual content. XS supervised data collection, contributed to interpretation of the data, and revision of the manuscript for important intellectual content. HR and ZH contributed to acquisition of data, interpretation of data, and revision of the manuscript for important intellectual content. IH contributed to questionnaire design, data interpretation, and revision of the manuscript for important intellectual content. BZ contributed to design of the study, data analysis and interpretation, and revision of the manuscript for important intellectual content. Acknowledgements This research was funded by the University of Michigan Office of Global Public Health and by a University of Michigan Rackham International Research Award. We appreciate the local Centers for Disease Control and Prevention staff and immunization clinic staff who coordinated site visits and interviews. References [1] Advisory Committee on Immunization Practices. Recommended Immunization Schedules for Persons Aged 0 — Through 18 Years: UNITED STATES, 2016 2016.
Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077
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Please cite this article in press as: Wagner AL et al. Parents’ concerns about vaccine scheduling in Shanghai, China. Vaccine (2017), http://dx.doi.org/ 10.1016/j.vaccine.2017.06.077