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Perceptions of measles, pneumonia, and meningitis vaccines among caregivers in Shanghai, China, and the health belief model: a cross-sectional study

  • Abram L. Wagner1Email author,
  • Matthew L. Boulton1,
  • Xiaodong Sun2,
  • Bhramar Mukherjee3,
  • Zhuoying Huang2,
  • Irene A. Harmsen4,
  • Jia Ren2 and
  • Brian J. Zikmund-Fisher5
BMC PediatricsBMC series – open, inclusive and trusted201717:143

DOI: 10.1186/s12887-017-0900-2

Received: 17 November 2015

Accepted: 5 June 2017

Published: 12 June 2017

Abstract

Background

In China, the measles vaccine is offered for free whereas the pneumococcal vaccine is a for-fee vaccine. This difference has the potential to influence how caregivers evaluate whether a vaccine is important or necessary for their child, but it is unclear if models of health behavior, such as the Health Belief Model, reveal the same associations for different diseases. This study compares caregiver perceptions of different diseases (measles, pneumonia and meningitis); and characterizes associations between Health Belief Model constructs and both pneumococcal vaccine uptake and perceived vaccine necessity for pneumonia, measles, and meningitis.

Methods

Caregivers of infants and young children between 8 months and 7 years of age from Shanghai (n = 619) completed a written survey on their perceptions of measles, pneumonia, and meningitis. We used logistic regression models to assess predictors of pneumococcal vaccine uptake and vaccine necessity.

Results

Only 25.2% of children had received a pneumococcal vaccine, although most caregivers believed that pneumonia (80.8%) and meningitis (92.4%), as well as measles (93.2%), vaccines were serious enough to warrant a vaccine. Perceived safety was strongly associated with both pneumococcal vaccine uptake and perceived vaccine necessity, and non-locals had 1.70 times higher odds of pneumonia vaccine necessity than non-locals (95% CI: 1.01, 2.88).

Conclusions

Most factors had a similar relationship with vaccine necessity, regardless of disease, indicating a common mechanism for how Chinese caregivers decided which vaccines are necessary. Because more caregivers believed meningitis needed a vaccine than pneumonia, health care workers should emphasize pneumococcal vaccination’s ability to protect against meningitis.

Keywords

Health belief model Immunization coverage China Measles Pneumococcus

Background

The World Health Organization promotes the global adoption of new vaccines through its Expanded Program on Immunization (EPI) [1, 2], although individual countries decide which vaccines to include based on local epidemiological, financial, and other considerations. The EPI in China started in 1978 and included the tuberculosis, polio, measles, and diphtheria-tetanus-pertussis (DTP) vaccines. Since then, it has expanded to include hepatitis A and B, meningococcal, Japanese encephalitis, rubella, and mumps vaccines [1]. All EPI vaccines in China are free and mandatory for school entry.

Immunization clinics in China also offer non-EPI vaccines to children for a fee (and not covered by insurance programs), including influenza, varicella, Haemophilus influenzae type b (Hib), rotavirus, and pneumococcal vaccines, among others. The pneumococcal vaccine, in particular, is a prime candidate for inclusion on the EPI schedule given the substantial burden of pneumococcal disease in China [3]. It has been introduced in many low-income countries with support from Gavi, the Vaccine Alliance [4], and it could prevent some of the 261,000 cases and 11,000 deaths due to pneumococcal pneumonia and meningitis in Chinese children under 5 years of age annually [5]. These figures are greater than, for example, the number of measles cases in China, which have fluctuated between 2005 and 2013 from a high of 123,136 in 2005 to a low of 6183 in 2012 [6].

Non-EPI vaccines have lower childhood coverage than EPI vaccines in China; for example, coverage of the 7-valent pneumococcal conjugate vaccine (PCV7) is 10.1% and coverage of the 23-valent pneumococcal polysaccharide vaccine (PPSV23) is 29.8% in Shanghai, which are both non-EPI vaccines, compared to >97% for DTP, an EPI vaccine [7, 8]. This disparity arises in part because of their expense [9]; for example, PCV7 costs approximately $135 per dose and PPSV23 is approximately $24 per dose. A study from 2013 in Jiangsu, Hubei, and Gansu provinces, found that the median amount that caregivers were willing to pay for the pneumococcal vaccine was between 150 and 200 RMB ($20–$30) [10]. Given the current lack of government funding for pneumococcal vaccination, understanding Chinese caregivers’ perceptions about this non-EPI vaccine and the diseases it prevents is key to developing effective interventions to increase vaccine uptake. And, if pneumococcal vaccine is added to the EPI schedule, understanding these perceptions will be important for developing effective programs to increase people’s acceptance of the vaccine.

Vaccine decision-making can be explained by health behavior models like the Health Belief Model (HBM) [11], which conceives of vaccination behaviors as an output of an individual’s perceptions of both a disease and its related vaccine [12]. These constructs specifically include people’s perceived susceptibility or vulnerability to the disease (i.e., the subjective perception of the risk associated with getting the disease), their understanding of disease severity (which could include medical consequences like disability and death or social consequences such as limited social interactions), a sense of the potential benefits of vaccination (e.g., effectiveness of vaccines), and anticipated barriers to vaccination (financial and temporal cost, side effects, unpleasant/painful injection) [12, 13]. Vaccine decision-making can also be influenced by demographic characteristics, such as residency and urbanicity. Non-locals, or migrants from rural areas to urban cities [14], have less access to governmental entitlement programs than locals [14, 15]. but still receive EPI vaccines for free; and urban districts represent historical business areas, whereas suburban districts are more industrial and have less access to public services [16, 17].

Although previous studies in China have shown the usefulness of an HBM framework for understanding perceived dysentery vaccine need [18], influenza vaccination intent [19], and influenza vaccine uptake among healthcare workers [20], no previous study in China has contrasted perceptions between EPI and non-EPI vaccines among caregivers using the HBM. It may be that people think differently about vaccines, such as the measles and pneumococcal vaccines, which have divergent payment mechanisms, which vary by length of time on the market, and for which people plausibly have different levels of personal experience. In this study, we compare perceptions of measles, pneumonia, and meningitis vaccines among caregivers in Shanghai; we characterize the associations between HBM constructs and pneumococcal vaccine uptake; and we contrast the associations between HBM constructs and perceived vaccine necessity of measles, pneumonia, and meningitis.

Methods

Study population

In this cross-sectional study which was completed during May and June of 2014, we invited caregivers (i.e., parents or grandparents) of young children at immunization clinics in Shanghai to participate in a survey that focused on their perceptions of vaccines for measles, pneumonia, and meningitis. We selected caregivers into the study through a two-stage, stratified, cluster sampling. The sample size was based on another aim of the project (to discriminate between measles vaccination timeliness of 81% in non-locals and 91% in locals), which required a simple random size of 208 per group or 416 total. Using another dataset on measles vaccination timeliness [21], we estimated an intracluster correlation coefficient of 0.024, and with a desired sample of 20 per cluster, we estimated a design effect of 1.456 for an effective sample size of 606. Clusters in this sample refer to townships, administrative regions in China which have an immunization clinic. There were 230 townships in Shanghai listed in the Census; we excluded 21 from Chongming county—islands off the coast of Shanghai which are distant from the other counties in the city, for a total of 209 townships in our selection. Townships were selected by a probability proportionate to size (PPS) systematic selection procedure with population of children 0 to 14 years of age from the China 2010 Census as the population size.

Within each township immunization clinic (where individuals obtain EPI and non-EPI vaccines), we selected a convenience sample, in person, of at least 20 caregivers who accompanied their child for a vaccination visit. The sole eligibility criterion was that the child was between 8 months and 7 years of age, which made them eligible for receipt of the measles and pneumococcal vaccines. We attempted to sample an equal number of locals and non-locals at each clinic because of hypothesized differences in experience with disease between the two groups. All potential participants gave informed consent prior to completing the paper survey at the immunization clinic. The survey was in Chinese and took approximately 20 min to complete, and participants were given an incentive of 30 renminbi ($5). An English version of the questionnaire is available in Additional file 1. The analysis included 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 structure of locals and non-locals in Shanghai.

Questionnaire

The questionnaire collected information on caregiver perceptions of pediatric vaccines, in general, and measles and pneumococcal vaccines, more specifically. The questions were informed by previous literature on beliefs and perceptions of vaccine-preventable diseases [2227], in addition to a qualitative, pilot research project undertaken by the lead author on 23 parents and grandparents at immunization clinics in Tianjin, China, during the summer of 2013 [28]. Prior to data collection, the questionnaire underwent pre-testing with 10 native Chinese speakers in the United States and 9 parents living in China. The questionnaire was also piloted in one township clinic in Shanghai. Questions were revised based on feedback in these pre-test settings. For a portion of the questionnaire, the same questions were asked about all three diseases (hereafter indicated as [disease type]): measles, pneumonia, or meningitis.

Outcome variables

The first outcome considered was pneumococcal vaccine uptake, which was administration of at least one dose of pneumococcal conjugate vaccine or pneumococcal polysaccharide vaccine, as documented in the child’s vaccination booklet. Because coverage of measles vaccine, which is part of the EPI, approaches 100% in China, we chose another outcome to allow us to compare how people make decisions about both measles and pneumococcal vaccines. This outcome, “vaccine necessity,” was the response to the question “Do you think that [disease type] is a serious enough disease to warrant a vaccine?”

Predictor variables

Local or non-local status was based on a previously completed field in the child’s vaccination booklet. Urbanicity was based on the location of the clinic: the urban districts include Huangpu, Xuhui, Changning, Jing’an, Putuo, Zhabei, Hongkou, Yangpu; and the suburban districts are Minhang, Baoshan, Jiading, Pudong, Jinshan, Songjiang, Qingpu, Fengxian. We did not include socioeconomic variables in the model over concerns that they would be mediators of the relationship between residency or urbanicity and the outcome, but a sensitivity analysis with education included did not significantly change any parameter estimates.

We included one question to measure each HBM construct, which were measured on a 5-point Likert scale. Perceived prevalence of the disease from the question “How common is [disease type] in your community?”. We measured perceived prevalence instead of the typical construct of perceived susceptibility because of feedback from the qualitative interviews. Previous studies have also made this substitution [29, 30], and have found strong correlations between these two concepts [31, 32].

The vaccine-related questions were asked twice, once for the measles vaccine and once for the pneumococcus vaccine (hereafter indicated as [measles / pneumococcus]). Perceived effectiveness of vaccine from the question, “How effective do you think the [measles/pneumococcus] vaccine is in preventing all cases of [disease type]?”; and perceived safety of the vaccine from the question, “How safe is the [measles/pneumococcus] vaccine?”. Perceived effectiveness of vaccine and perceived safety of vaccine represent the HBM constructs of perceived benefits and barriers to a health-related action, respectively.

We also included questions on disease experience and descriptive norm of vaccination, which are not HBM constructs but which were identified as important in the qualitative research project [28]. Experience with the disease was a binary variable, with the “yes” option being a positive response to any of the following questions: “Have you ever personally contracted [disease type]?”; “Has your child ever contracted [disease type]?”; and “Has any close family member of friend of yours ever contracted [disease type]?”. Finally, perceived norm of vaccination was derived from the question, “Among your social group, how many children do you think are vaccinated against [measles/pneumococcus]?”.

Statistical analysis

For a descriptive analysis, we used the non-parametric Kruskal-Wallis one-way analysis of variance to test for a significant difference in means for the Likert scale variables across the three disease types (degrees of freedom (df) =2). A Chi-Square test of independence, with the Rao-Scott adjustment to account for the survey design, compared proportions for categorical variables (df = 2, except for caregiver relation, which had df = 4).

For pneumococcal vaccine uptake, two logistic regression models with survey adjustments were run—one for pneumonia-specific perceptions and the other for meningitis-specific perceptions.

To compare how perceptions about measles, pneumonia, and meningitis were differently associated with the outcome vaccine necessity, we created a long-form dataset wherein each individual had 3 observations, one for their perception of each of the three diseases assessed. To account for possible dependence due to each individual yielding three separate observations, we used a generalized estimating equation (GEE) with a binomial distribution and logit link and specified an unstructured within-subject correlation. An interaction term of each predictor variable and a dummy variable for the disease type corresponding to that particular observation was also entered into this model. Significance of the interaction across the 3 disease types was assessed by a Wald chi-square test (df = 2, except for caregiver relation, which had df = 4). Significance was assessed at an α level of 0.05 for all tests, and the precision of odds ratios (OR) was evaluated with 95% confidence intervals (CI). All analyses were weighted based on participants’ probability of selection with respect to urbanicity and residency, and we used SAS version 9.3 (SAS Institute Inc., Cary, North Carolina).

Results

Out of 734 caregivers approached, 619 caregivers (84.3%) of children who were between 8 months and 7 years of age participated in the survey; nearly two-thirds (64.5%) were mothers of the child, one-quarter (27.6%) were fathers; and 7.8% were other family members, mostly grandmothers. Slightly more than half of the children (51.3%) were male; and 31.3% resided in Shanghai’s urban districts (Table 1). Approximately one-quarter (25.2%) of children had received a pneumococcal vaccine, and nearly all (98.8%) had been administered a measles vaccine.
Table 1

Demographic characteristics of 619 children and their caregivers from Shanghai, 2014

Characteristic

Category

Unweighted Count

Weighted proportion (95% CI)

Caregiver relation

Mother

405

64.5 (59.8, 69.3)

Father

156

27.6 (23.1, 32.2)

Other

57

7.8 (5.5, 10.1)

Parent’s agea

<28 years

105

23.1 (18.3, 27.9)

28 to <31 years

142

28.0 (23.3, 32.8)

31 to <34 years

129

24.5 (19.9, 29.1)

≥35 years

144

24.3 (19.9, 28.8)

Caregiver’s education

≤Middle school

142

24.2 (19.9, 28.6)

≤High school

93

17.8 (13.8, 21.8)

Some college

153

23.3 (19.4, 27.3)

College graduate

227

34.6 (30.1, 39.2)

Family monthly income

<4000 RMB

109

19.1 (15.1, 23.1)

4000 to <6000 RMB

142

23.9 (19.6, 28.2)

6000 to <10,000 RMB

156

26.8 (22.4, 31.2)

≥10,000 RMB

208

30.2 (25.9, 34.5)

Child’s sex

Male

324

51.3 (46.4, 56.2)

Female

292

48.7 (43.8, 53.6)

Child’s residency

Local

315

43.2 (38.5, 47.8)

Non-local

303

56.8 (52.2, 61.5)

Township urbanicity

Urban

203

31.3 (26.9, 35.7)

Suburban

415

68.7 (64.3, 73.1)

Pneumococcal vaccination

Yes

170

25.2 (21.0, 29.3)

No

448

74.8 (70.7, 79.0)

Measles vaccination

Yes

609

98.8 (98.0, 99.7)

No

9

1.2 (0.3, 2.0)

CI confidence interval

aOnly for mothers and fathers

All caregiver perception and experience variables were significantly different across the three diseases (Table 2). Most caregivers judged measles (93.2%) and meningitis (92.4%) serious enough to warrant a vaccine, whereas 80.8% thought pneumonia warranted a vaccine. More caregivers (43.3%) had personal experience with pneumonia, compared with 18.6% for measles and only 7.1% for meningitis. Caregivers believed that meningitis was more severe (mean 4.35) than measles (4.07) or pneumonia (4.11); and the perceived prevalence of disease was higher for pneumonia (3.15) than measles (2.30) or meningitis (2.28).
Table 2

Perceptions of measles, pneumonia, and meningitis disease and vaccination among caregivers in Shanghai, 2014

 

Measles

Pneumonia

Meningitis

P-value*

Mean (SE)

Mean (SE)

Mean (SE)

Vaccine necessity (%)

93.2 (1.15)

80.8 (1.89)

92.4 (1.34)

<0.0001

Perceived prevalence

2.30 (0.043)

3.15 (0.047)

2.28 (0.037)

<0.0001

Disease experience (%)

18.6 (1.96)

43.3 (2.44)

7.1 (1.40)

<0.0001

Perceived norm

4.03 (0.045)

3.35 (0.051)

3.35 (0.051)

<0.0001

Perceived effectiveness

3.81 (0.033)

3.58 (0.032)

3.56 (0.035)

<0.0001

Perceived safety

3.92 (0.036)

3.81 (0.034)

3.81 (0.034)

0.0404

SE standard error

*For Likert scale variables, the P-value is the Kruskal-Wallis test. For dichotomous variables, the P-value is from the Rao-Scott Chi-Square Test

Perceived necessity of a pneumonia vaccine was the strongest predictor of pneumococcal vaccine uptake in the model with pneumonia-specific perceptions (OR: 2.67, 95% CI: 1.27, 5.63) (Table 3). Perceived safety of vaccination was a significant predictor in the models for both pneumonia-specific (OR: 2.39, 95% CI: 1.57, 3.63) and meningitis-specific perceptions (OR: 2.12, 95% CI: 1.24, 3.63).
Table 3

Pneumonia- or meningitis-specific perceptions and pneumococcal vaccine uptake among 602 caregivers in Shanghai, 2014

 

Pneumonia

Meningitis

OR (95% CI)

OR (95% CI)

Perceived vaccine necessity

2.67 (1.27, 5.63)

1.45 (0.52, 3.99)

Perceived prevalence

1.10 (0.84, 1.44)

0.97 (0.73, 1.31)

Disease experience

 Yes vs No

1.16 (0.70, 1.94)

1.32 (0.55, 3.17)

Perceived norm

1.16 (0.92, 1.46)

1.21 (0.96, 1.53)

Perceived effectiveness

0.91 (0.61, 1.35)

0.95 (0.61, 1.47)

Perceived safety

2.39 (1.57, 3.63)

2.12 (1.24, 3.63)

Residency

 Non-local vs local

1.01 (0.63, 1.60)

0.97 (0.62, 1.52)

Urbanicity

 Outer vs inner district

1.10 (0.69, 1.78)

1.31 (0.82, 2.08)

Caregiver relation

 Father vs mother

0.71 (0.41, 1.24)

0.67 (0.39, 1.17)

 Other vs mother

1.54 (0.71, 3.32)

1.20 (0.56, 2.53)

OR odds ratio, CI confidence interval

Results from the multivariable model of vaccine necessity are shown in Table 4. An increase in perceived norm of vaccination was associated with 1.97 times greater odds of measles vaccine necessity (95% CI: 1.50, 2.59) and 1.53 times greater odds of pneumonia vaccine necessity (95% CI: 1.23, 1.91). Perceived safety of vaccination was positively associated with measles (OR: 2.35; 95% CI: 1.26, 4.38), pneumonia (OR: 1.62; 95% CI: 1.04, 2.52), and meningitis vaccine necessity (OR: 2.11, 95% CI: 1.31, 3.40). Perceived prevalence of disease was not associated with necessity for vaccination against measles, pneumonia, or meningitis.
Table 4

Predictors of vaccine necessity for three diseases among 602 caregivers in Shanghai, 2014

 

Measles

Pneumonia

Meningitis

P-valuea

OR (95% CI)

OR (95% CI)

OR (95% CI)

Perceived prevalence

1.25 (0.85, 1.83)

1.18 (0.91, 1.53)

1.08 (0.65, 1.80)

0.9022

Disease experience

   

0.2576

 Yes vs No

1.48 (0.58, 3.78)

0.76 (0.46, 1.26)

0.34 (0.10, 1.10)

 

Perceived norm

1.97 (1.50, 2.59)

1.53 (1.23, 1.91)

1.13 (0.80, 1.61)

0.0753

Perceived effectiveness

1.31 (0.69, 2.49)

4.05 (2.61, 6.31)

1.17 (0.57, 2.42)

0.0088

Perceived safety

2.35 (1.26, 4.38)

1.62 (1.04, 2.52)

2.11 (1.31, 3.40)

0.5349

Residency

   

0.4511

 Non-local vs local

1.77 (0.84, 3.73)

1.70 (1.01, 2.88)

1.06 (0.48, 2.36)

 

Urbanicity

   

0.0016

 Suburban vs urban

0.37 (0.15, 0.92)

1.74 (1.01, 3.00)

0.79 (0.32, 1.95)

 

Caregiver relation

   

0.1886

 Father vs mother

0.38 (0.17, 0.84)

1.21 (0.64, 2.27)

1.07 (0.44, 2.56)

 

 Other vs mother

0.20 (0.06, 0.65)

0.50 (0.21, 1.17)

0.45 (0.14, 1.48)

 

OR odds ratio, CI confidence interval

aWald chi-square test for overall interaction (df = 2, except for caregiver relation, which had df = 4). Results in this table are from a single, multivariable logistic regression model

The strength of the associations between most explanatory variables and vaccine necessity did not vary significantly by disease. However, the relationship between perceived effectiveness of vaccination and necessity of vaccination did vary by disease (P = 0.0088); for pneumonia this was a positive association (OR: 4.05; 95% CI: 2.61, 6.31), whereas for measles and meningitis there was no association. There was also a significant interaction between urbanicity and disease (P = 0.0016); people living in suburban districts were more likely to consider the pneumonia vaccine necessary (OR: 1.74; 95% CI: 1.01, 3.00), whereas the opposite relationship (OR: 0.37; 95% CI: 0.15, 0.92) was found for the measles vaccine. Additionally, although the interaction term for residency was not significant, non-locals had higher odds of pneumonia vaccine necessity than locals (OR: 1.70; 95% CI: 1.01, 2.88), whereas there was not a significant association between residency and either measles (OR: 1.77; 95% CI: 0.84, 3.73) or meningitis vaccine necessity (OR: 1.06; 95% CI: 0.48, 2.36).

Discussion

In order to increase coverage of newer, pediatric vaccines in middle income countries, it is necessary to develop a better understanding of the relationships between caregiver perceptions of a disease and its vaccine. In this cross-sectional survey of parents and grandparents in Shanghai, only a minority of children had been administered a pneumococcal vaccine, even though most of their caregivers believed that pediatric pneumonia and meningitis vaccines were necessary. Moreover, whereas the vast majority of caregivers thought measles and meningitis were serious enough to warrant a vaccine, a lesser amount held similar beliefs for pneumonia. Previous studies have also shown that parents generally do not consider pneumonia vaccines as important as other vaccines. In the Netherlands, Hak et al. found that fewer parents had a positive attitude towards pneumonia vaccines than other vaccines, such as those for hepatitis B or tuberculosis [33]. Bedford and Lansley similarly reported that fewer British parents would accept a pneumococcal vaccine than a meningococcal vaccine. They postulated that this difference in acceptance came from parents associating meningococcus with meningitis and pneumococcus with pneumonia, and subsequently believing that meningitis was more clinically severe than pneumonia [34], which is corroborated by our study in comparing perceptions of pneumococcal meningitis and pneumococcal pneumonia.

In this study, perceived vaccine necessity but not perceived prevalence of pneumonia, was positively associated with pneumococcal vaccine uptake. Both our study and a study on pediatric dysentery vaccination by Chen et al. did not observe a relationship between perceived prevalence and vaccine need [18], suggesting that, for Chinese parents, perceptions about a disease’s threat primarily derive from concerns about severity and is not necessarily based on their understanding of how common the disease is within the community. It is possible that Chinese caregivers may view the threat of diseases in a fundamentally different way compared to caregivers in other countries because the one-child policy likely results in heightened focus from parents on one child [35]. Chinese caregivers’ high investment in their child’s safety may explain why pneumonia vaccine necessity, a measure of disease severity, was a strong predictor of pneumococcal vaccine uptake and why perceived vaccine safety was strongly and positively associated with all vaccine outcomes that we considered.

Besides perceived safety of vaccination, necessity of pneumonia vaccination was also associated with pneumococcal vaccine uptake. Vaccine necessity could be an important mediator in the pathway between disease perceptions and vaccine uptake, and we may observe stronger associations between disease perceptions and vaccine necessity than disease perceptions and vaccine uptake because vaccine necessity is more proximal to these perceptions. The lack of significant associations between perceptions of meningitis and pneumococcal vaccination could result from caregivers not being aware that pneumococcal vaccines can protect against some forms of meningitis.

Most of the HBM constructs and other beliefs under consideration had a similar relationship with vaccine necessity, regardless of disease. Because we saw consistent associations between HBM constructs and vaccine necessity, we conclude there was a common mechanism underlying how Chinese parents decided which vaccines are necessary, in the context of their perceptions about the disease and the vaccine. However, the strength of the relationship between perceived effectiveness of vaccination and vaccine necessity did differ by disease. For measles, perceived effectiveness of vaccination was not an important determinant of vaccine necessity, perhaps because measles vaccine is mandatory. In contrast, because the pneumococcal vaccine requires payment from caregivers, they may only feel their children need it if the vaccine is effective. We may not see any association for meningitis because the pneumococcal vaccine in China is marketed as a pneumonia vaccine, not a meningitis vaccine, and we conjecture that caregivers have little understanding of how the pneumococcal vaccine can prevent some forms of meningitis.

Given the high uptake of EPI vaccines in China, adding pneumococcal vaccination to the EPI schedule will undoubtedly increase coverage, however, we have no indication when or if this will happen, especially since PCV7 was taken off the market in China in 2015 [36]. Measles vaccine is an EPI vaccine but pneumococcal vaccine is not, and this difference prevented us from considering other factors that influence vaccine uptake in other countries. First, measles vaccine is free in Shanghai but pneumococcal vaccine requires payment. This could significantly impact decisions; in a 7-country survey of parents, support for a vaccine decreased by 14% if the vaccine required payment [37]. Second, China has focused tremendous efforts on measles elimination, and hundreds of millions of children have been vaccinated against measles during supplementary immunization activities within the past decade [38]. There has not been a comparable effort for pneumococcal vaccination. Therefore, the Chinese public is receiving more information about measles than about pneumonia or meningitis.

Non-locals and suburban dwellers have a number of different experiences and attributes which distinguish them from their local or urban counterparts. They may have different experiences with disease, given disparities in treatment or ability to interface with health care providers. Notably, quality and density of health care diminishes outside of urban areas in cities [16], and non-locals access health care services much less than locals [15]. Previous studies have shown that non-locals have lower vaccination coverage than locals, and suburban children have worse vaccination outcomes than those in urban districts, for both EPI and non-EPI vaccines [7, 39, 40]. Yet we found that non-locals and suburban dwellers had greater odds of considering pneumonia vaccines as necessary compared to locals and urban dwellers. That these subpopulations think that pneumonia vaccines are necessary but do not receive them could result from the cost, and financial incentives from the government may be necessary to increase vaccination coverage, particularly in these poorer populations where there is a demand for vaccination.

This study provides a framework for developing a better understanding of the context driving demand for a vaccine. As Nichter notes, there is a difference between passive acceptance of and active demand for vaccinations [41]. With passive acceptance, the populace attains high vaccination coverage only after the public health sector devotes intensive resources towards promoting a certain vaccine. By contrast, in the latter, a well-informed public perceives the need for vaccination and drives demand for immunization services. In our survey, perceived necessity of vaccination by caregivers was higher for measles and meningitis than it was for pneumonia. This implies that even if pneumonia vaccination were added to the EPI schedule, active demand could be lower than for other vaccines. Thus, uptake would be driven by pressure from the public health sector and not from caregivers demanding the vaccine.

Strengths and limitations

The study has both important strengths and limitations. One strength was the purposeful sampling of people by residency to account for an important demographic group in Shanghai. However, within each township’s immunization clinic, we selected a convenience sample. This means that the study population is biased towards a population with more positive views towards immunization services. Additionally, we only used one item to measure each HBM construct, and therefore could not minimize measurement error by formulating latent constructs.

This study evaluated perceptions of meningitis and pneumococcal vaccinations, but a Hib vaccine and meningococcal vaccine are also available in China to protect against these diseases. The etiology of pneumonia and meningitis in China is poorly understood [5, 42, 43], but it is likely that Hib results in comparable rates of pneumonia morbidity and mortality as pneumococcus [5, 44], and that the cause of meningitis morbidity in China is somewhat equally divided between meningococcus and pneumococcus [5, 45]. A caregiver’s perception of vaccine necessity could therefore be colored by the other vaccines already on the market, and we hypothesize that caregivers would be less apt to consider a vaccine necessary if they also thought that that disease could be caused by a number of different infections.

Conclusions

Given the enormous toll of pneumococcal disease in China [3, 5], widespread pneumococcal vaccination could improve child health and save lives. China has spent tremendous resources on measles elimination [38], but measles elimination efforts should could be combined with other immunization initiatives [46], such as educating caregivers about the benefits of other vaccines. In particular, because more people thought that a meningitis vaccine was necessary than a pneumonia vaccine, promotional materials for pneumococcal vaccines could focus disease severity and on meningitis, the more severe clinical presentation of pneumococcal disease.

Future studies could take a longitudinal look at attitudes towards a disease, the desire to obtain a vaccine, and, finally, actual vaccination. Additionally, both the relationship between the patient and the provider and how the provider approaches talking about vaccination are important [47], warranting further research on health care workers in China. As more vaccines are introduced into the EPI schedule in China, providers will be an important conduit of information about the risk of disease and the safety and effectiveness of vaccination.

Abbreviations

CI: 

confidence interval

df: 

degrees of freedom

DTP: 

diphtheria-tetanus-pertussis vaccine

EPI: 

Expanded Program on Immunization

GEE: 

Generalized Estimating Equations

HBM: 

Health Belief Model

Hib: 

Haemophilus influenzae type b

OR: 

Odds ratio

PCV7: 

7-valent pneumococcal conjugate vaccine

PPS: 

Probability proportionate to size

PPSV23: 

23-valent pneumococcal polysaccharide vaccine

RMB: 

Renminbi

SE: 

standard error

Declarations

Acknowledgements

This study was possible thanks to the local Centers for Disease Control and Prevention staff who coordinated site visits and interviews.

Funding

This research was funded by the University of Michigan Office of Global Public Health and by a Rackham International Research Award. The funders had no role in the design of the study, data collection, analysis, interpretation of data, manuscript writing, or manuscript submission.

Availability of data and materials

The datasets generated and analyzed during the current study are available in the ResearchGate repository, http://dx.doi.org/10.13140/RG.2.2.11521.86886.

Authors’ contributions

AW conceived of the study design, led data analysis, and wrote the first draft of the paper. MB contributed to the study design and interpretation of data, and revised the manuscript critically for content. XS, ZY, and JR supervised field work, contributed to interpretation of data, and revised the manuscript critically for content. BM contributed to study design, data analysis, and interpretation of data; she also revised the manuscript critically for content. IA contributed to study design and interpretation of data, and revised the manuscript critically for content. BZ supervised data analysis and interpretation, and revised the manuscript critically for content. All authors have given final approval of the version to be published and agree to be accountable for the work.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The study protocol was approved by the Health Sciences Behavioral Sciences Institutional Review Board at the University of Michigan (#HUM00087564) and the Shanghai CDC Ethics Review Committee (#2014–10).

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Epidemiology, University of Michigan
(2)
Department of Immunization Programs, Shanghai Centers for Disease Control and Prevention
(3)
Department of Biostatistics, University of Michigan
(4)
Department of Epidemiology and Health Promotion, Public Health Service of Amsterdam
(5)
Department of Health Behavior and Health Education, University of Michigan

References

  1. Zheng J, Zhou Y, Wang H, Liang X. The role of the China experts advisory committee on immunization program. Vaccine. 2010;28S:A84–7. doi:10.1016/j.vaccine.2010.02.039.View ArticleGoogle Scholar
  2. Wang L, Wang Y, Jin S, Wu Z, Chin D. Emergence and control of infectious diseases in China. Lancet. 2008;372:34–41. doi:10.1016/S0140-6736(08)61365-3.View ArticleGoogle Scholar
  3. Yu H, Yang W, Varma JK. To save children’s lives, China should adopt an initiative to speed introduction of pneumonia vaccines. Health Aff. 2012;31:2545–53. doi:10.1377/hlthaff.2011.1272.View ArticleGoogle Scholar
  4. GAVI Alliance. Vaccine goal indicators. GAVI 2015. http://www.gavi.org/results/goal-level-indicators/vaccine-goal-indicators/ (accessed June 2, 2016).Google Scholar
  5. Chen Y, Deng W, Wang S-M, Mo Q-M, Jia H, Wang Q, et al. Burden of pneumonia and meningitis caused by Streptococcus Pneumoniae in China among children under 5 years of age: a systematic literature review. PLoS One. 2011;6:e27333. doi:10.1371/journal.pone.0027333.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Ma C, Hao L, Zhang Y, Su Q, Rodewald L, An Z, et al. Monitoring progress towards the elimination of measles in China: an analysis of measles surveillance data. Bull World Health Organ. 2014;92:340–7. doi:10.2471/BLT.13.130195.View ArticlePubMedPubMed CentralGoogle Scholar
  7. Wagner AL, Sun X, Montgomery JP, Huang Z, Boulton ML. The impact of residency and Urbanicity on Haemophilus influenzae type b and pneumococcal immunization in Shanghai children: a retrospective cohort study. PLoS One. 2014;9:e97800. doi:10.1371/journal.pone.0097800.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Boulton ML, Ravi NS, Sun X, Huang Z, Wagner AL. Trends in childhood pneumococcal vaccine coverage in Shanghai, China, 2005-2011: a retrospective cohort study. BMC Public Health. 2016;16:109. doi:10.1186/s12889-016-2785-7.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Xie J, Dow WH. Longitudinal study of child immunization determinants in China. Soc Sci Med. 2005;61:601–11. doi:10.1016/j.socscimed.2004.12.016.View ArticlePubMedGoogle Scholar
  10. Hou Z, Chang J, Yue D, Fang H, Meng Q, Zhang Y. Determinants of willingness to pay for self-paid vaccines in China. Vaccine. 2014;32:4471–7. doi:10.1016/j.vaccine.2014.06.047.View ArticlePubMedGoogle Scholar
  11. Janz NK, Becker MH. The health belief model: a decade later. Health Educ Q. 1984;11:1–47.View ArticlePubMedGoogle Scholar
  12. Rosenstock IM, Strecher VJ, Becker MH. Social learning theory and the health belief model. Health Educ Q. 1988;15:175–83.View ArticlePubMedGoogle Scholar
  13. LaMorte WW. Behavioral change models. Bost Univ Sch Public Heal. 2016; http://sphweb.bumc.bu.edu/otlt/MPH-Modules/SB/BehavioralChangeTheories/ (accessed May 19, 2017
  14. Chan K. China: internal migration. In: ness I, Bellwood P, editors. Encycl. Glob. Hum. Migr. Wiley-Blackwell: Hoboken, NJ; 2012. doi:10.1002/9781444351071.Google Scholar
  15. Gong P, Liang S, Carlton EJ, Jiang Q, Wu J, Wang L, et al. Urbanisation and health in China. Lancet. 2012;379:843–52. doi:10.1016/S0140-6736(11)61878-3.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Li H, Wang Q, Shi W, Deng Z, Wang H. Residential clustering and spatial access to public services in Shanghai. Habitat Int. 2015;46:119–29. doi:10.1016/j.habitatint.2014.11.003.View ArticleGoogle Scholar
  17. Yang S, Wang C, Wang M. Synergistic evolution of Shanghai urban economic development transition and social spatial structure. In: Wang MY, Kee P, Gao J, editors. Transform. Chinese Cities, New York, NY: Routledge; 2014. p. 48–74.Google Scholar
  18. Chen X, Stanton B, Wang X, Nyamette A, Pach A, Kaljee L, et al. Differences in perception of dysentery and enteric fever and willingness to receive vaccines among rural residents in China. Vaccine. 2006;24:561–71. doi:10.1016/j.vaccine.2005.08.060.View ArticlePubMedGoogle Scholar
  19. Mok E, Yeung SH, Chan MF. Prevalence of influenza vaccination and correlates of intention to be vaccinated among Hong Kong Chinese. Public Heal Nurs. 2006;23:506–15.View ArticleGoogle Scholar
  20. Seale H, Kaur R, Wang Q, Yang P, Zhang Y, Wang X, et al. Acceptance of a vaccine against pandemic influenza a (H1N1) virus amongst healthcare workers in Beijing, China. Vaccine. 2011;29:1605–10. doi:10.1016/j.vaccine.2010.12.077.View ArticlePubMedGoogle Scholar
  21. Wagner AL, Sun X, Huang Z, Ren J, Mukherjee B, Wells EV, et al. On-time measles and pneumococcal vaccination of Shanghai children: the impact of individual- and neighborhood-level factors. Pediatr Infect Dis J. 2016;35:e311–7. doi:10.1097/INF.0000000000001267.View ArticlePubMedGoogle Scholar
  22. Bond L, Nolan T. Making sense of perceptions of risk of diseases and vaccinations: a qualitative study combining models of health beliefs, decision-making and risk perception. BMC Public Health. 2011;11:943. doi:10.1186/1471-2458-11-943.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Smith PJ, Humiston SG, Marcuse EK, Zhao Z, Dorell CG, Howes C, et al. Parental delay or refusal of vaccine doses, childhood vaccination coverage at 24 months of age, and the health belief model. Public Heal Rep. 2011;126:135–46.View ArticleGoogle Scholar
  24. Timmermans DRM, Henneman L, Hirasing RA, van der Wal G. Parents’ perceived vulnerability and perceived control in preventing meningococcal C infection: a large-scale interview study about vaccination. BMC Public Health. 2008;8:45. doi:10.1186/1471-2458-8-45.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Ruijs WLM, Hautvast JLA, van Ansem WJC, van Ijzendoorn G, van der Velden K, Hulscher ME. How orthodox protestant parents decide on the vaccination of their children: a qualitative study. BMC Public Health. 2012;12:408. doi:10.1186/1471-2458-12-408.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Harmsen IA, Mollema L, Ruiter RA, Paulussen TG, de Melker HE, Kok G. Why parents refuse childhood vaccination: a qualitative study using online focus groups. BMC Public Health. 2013;13:1183. doi:10.1186/1471-2458-13-1183.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Harmsen IA, Doorman GG, Mollema L, Ruiter RA, Kok G, de Melker HE. Parental information-seeking behaviour in childhood vaccinations. BMC Public Health. 2013;13:1219. doi:10.1186/1471-2458-13-1219.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Wagner AL. Attitudes towards pediatric vaccines among caregivers in Tianjin, China: a qualitative study. 2015. doi:10.13140/RG.2.1.2862.2881.
  29. Butraporn P, Pach A. The health belief model and factors relating to potential use of a vaccine for shigellosis in Kaeng koi district, Saraburi province, Thailand. J Health Popul Nutr. 2004;22:170–81.PubMedGoogle Scholar
  30. Brown A, Moodie C. The influence of tobacco marketing on adolescent smoking intentions via normative beliefs. Health Educ Res. 2009;24:721–33. doi:10.1093/her/cyp007.View ArticlePubMedGoogle Scholar
  31. Park JS, Grow JM. The social reality of depression : DTC advertising of antidepressants and perceptions of the prevalence and lifetime risk of depression. J Bus Ethics. 2008;79:379–93. doi:10.1007/sl0551-007-9403-7.View ArticleGoogle Scholar
  32. Windschitl PD, Martin R, Flugstad AR. Context and the interpretation of likelihood information: the role of intergroup comparisons on perceived vulnerability. J Pers Soc Psychol. 2002;82:742–55. doi:10.1037//0022-3514.82.5.742.View ArticlePubMedGoogle Scholar
  33. Hak E, Schönbeck Y, De Melker H, Van Essen GA, Sanders EAM. Negative attitude of highly educated parents and health care workers towards future vaccinations in the Dutch childhood vaccination program. Vaccine. 2005;23:3103–7. doi:10.1016/j.vaccine.2005.01.074.View ArticlePubMedGoogle Scholar
  34. Bedford H, Lansley M. More vaccines for children? Parents’ views. Vaccine. 2007;25:7818–23. doi:10.1016/j.vaccine.2007.08.057.View ArticlePubMedGoogle Scholar
  35. Gong Y, Stanton BF, Von Seidlen L, Feng X, Nyamette A. Perceptions of Shigella and of Shigella vaccine among rural Chinese: compatibility with western models of behavioral change. Southeast Asian J Trop Med Public Health. 2004;35:97–108.Google Scholar
  36. Burkitt L. Pfizer to cease vaccine sales business in China. Wall Str J. 2015; http://www.wsj.com/articles/pfizer-to-cease-vaccine-sales-business-in-china-1427965438 (accessed April 19, 2015
  37. Bakhache P, Rodrigo C, Davie S, Ahuja A, Sudovar B, Crudup T, et al. Health care providers’ and parents’ attitudes toward administration of new infant vaccines--a multinational survey. Eur J Pediatr. 2013;172:485–92. doi:10.1007/s00431-012-1904-4.View ArticlePubMedGoogle Scholar
  38. World Health Organization. News in brief. Measles-Rubella Bull. 2011;5:1–9.Google Scholar
  39. Sun M, Ma R, Zeng Y, Luo F, Zhang J, Hou W. Immunization status and risk factors of migrant children in densely populated areas of Beijing, China. Vaccine. 2010;28:1264–74. doi:10.1016/j.vaccine.2009.11.015.View ArticlePubMedGoogle Scholar
  40. Li Q, Hu Y, Zhong Y, Chen Y, Tang X, Guo J, et al. Using the immunization information system to determine vaccination coverage rates among children aged 1-7 years: a report from Zhejiang Province, China. Int J Environ Res Public Health. 2014;11:2713–28. doi:10.3390/ijerph110302713.View ArticlePubMedPubMed CentralGoogle Scholar
  41. Nichter M. Vaccinations in the third world: a consideration of community demand. Soc Sci Med. 1995;41:617–32.View ArticlePubMedGoogle Scholar
  42. Che D, Zhou H, He J, Wu B. Modeling the impact of the 7-valent pneumococcal conjugate vaccine in Chinese infants: an economic analysis of a compulsory vaccination. BMC Health Serv Res. 2014;14:56. doi:10.1186/1472-6963-14-56.View ArticlePubMedPubMed CentralGoogle Scholar
  43. Yang Y-H, Fu S-G, Peng H, Shen A-D, Yue S-J, Go Y-F, et al. Abuse of antibiotics in China and its potential interference in determining the etiology of pediatric bacterial diseases. Pediatr Infect Dis J. 1993;12:986–7. doi:10.1097/00006454-199312000-00004.View ArticlePubMedGoogle Scholar
  44. Watt JP, Wolfson LJ, O’Brien KL, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Haemophilus influenzae type b in children younger than 5 years: global estimates. Lancet. 2009;374:903–11. doi:10.1016/S0140-6736(09)61203-4.View ArticlePubMedGoogle Scholar
  45. Zhang X, Shao Z, Zhu Y, Xu L, Xu X, Mayer LW, et al. Genetic characteristics of serogroup a meningococci circulating in China, 1956-2005. Clin Microbiol Infect. 2008;14:555–61.View ArticlePubMedGoogle Scholar
  46. Griffiths UK, Mounier-Jack S, Oliveira-Cruz V, Balabanova D, Hanvoravongchai P, Ongolo P. How can measles eradication strengthen health care systems? J Infect Dis. 2011;204:S78–81. doi:10.1093/infdis/jir090.View ArticlePubMedGoogle Scholar
  47. Benin AL, Wisler-Scher DJ, Colson E, Shapiro ED, Holmboe ES. Qualitative analysis of mothers’ decision-making about vaccines for infants: the importance of trust. Pediatrics. 2006;117:1532–41. doi:10.1542/peds.2005-1728.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2017