On-time Measles and Pneumococcal Vaccination of Shanghai Children: The Impact of Individual-level and Neighborhood-level Factors : The Pediatric Infectious Disease Journal

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On-time Measles and Pneumococcal Vaccination of Shanghai Children

The Impact of Individual-level and Neighborhood-level Factors

Wagner, Abram L. PhD, MD; Sun, Xiaodong PhD; Huang, Zhuoying MPH; Ren, Jia BMed; Mukherjee, Bhramar PhD; Wells, Eden V. MD, MPH; Boulton, Matthew L. MD, MPH

Author Information
The Pediatric Infectious Disease Journal: October 2016 - Volume 35 - Issue 10 - p e311-e317
doi: 10.1097/INF.0000000000001267
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Measles and pneumococcal pneumonia have historically been major causes of childhood illness and were exceeded only by tuberculosis and malaria as the leading causes of infectious disease mortality worldwide as recently as 1990.1 In the ensuing 2 decades, annual mortality from invasive pneumococcal disease (IPD) comprising pneumonia, meningitis and septicemia has remained relatively stable at over 900,000 deaths per year, in contrast to substantial decreases in measles mortality, from 631,200 deaths in 1990 to 125,400 deaths in 2010.1 Although the global epidemiology of these 2 vaccine-preventable diseases are markedly different,2 the World Health Organization recommends inclusion of vaccines for both diseases in all countries’ national immunization programs.3 In China, measles vaccinations are publically funded under the Expanded Program on Immunization (EPI) and have high coverage,4 whereas pneumococcal vaccines are not included on the EPI and, therefore, require out-of-pocket payment and are characterized by substantially lower coverage.5,6Table 1 shows current pediatric vaccination schedule in Shanghai.

Table 1:
The Pediatric Immunization Schedule in China as of 2012

China approved the use of a measles vaccine in 1966,8 and 2 doses of measles-containing vaccine (MCV) are administered free to children before their second birthday: MCV1 is given at 8 months and MCV2 at 18–24 months.7,9 As a result of increasing MCV coverage, measles incidence in China declined from over 1000 cases per 100,000 in the 1960s to 5.7 cases per 100,000 in the late 1990s.10 Subsequently, incidence of measles has declined more slowly, even though China has mobilized significant resources and heavily promoted measles vaccination in pursuit of measles elimination. As a result, the original goal of measles elimination by 2012 was pushed back to 2020.11,12 China’s difficulty in controlling measles has been attributed to low vaccination coverage among adults, late or untimely vaccination and increasing numbers of internal migrants whose relocation facilitates ongoing transmission.10,13 Although almost 100% of children in China are eventually vaccinated against measles, previous studies have found that <90% of children have an on-time administration of MCV1.14,15 Given systematic delays in vaccination for a substantial number of children in China, vaccine timeliness may better represent population-level immunity to measles compared with simple estimates of vaccination coverage which do not consider timing of administration.16 Studies in the United States have suggested that delayed measles vaccination17 and delayed pertussis vaccination18 have been linked to outbreaks of these vaccine-preventable diseases. In Tianjin, China, 24% of measles cases between 2005 and 2014 were under the age of 1 year, whereas only 0.6% of the population was in this age group,19 further indicating that there is a need in China for children to receive the first dose of measles vaccine as early as indicated. In contrast to the measles vaccine, the 7-valent pneumococcal conjugate vaccine (PCV) was approved for use in China only in 2008,5 although it was taken off the market in 2015.20 It is relatively expensive (USD135/dose), and 1 to 4 doses are required to elicit long-term immunity, depending on the age at first dose of administration. As a result, PCV coverage is relatively low in China—just over 10%,6 and the promotion of pneumococcal vaccination does not currently appear to be a government priority despite evidence that the vaccine could reduce the substantial burden of related disease among children in China.5 Chen et al21 estimated that in 2000 there were 384.45 cases of pneumococcal pneumonia per 100,000 children <5 years old and 1.33 cases of pneumococcal meningitis per 100,000 children <5 years old. Because young children of <2 years of age have the highest case-fatality ratio from IPD of any age group,22 vaccinating infants at the earliest-recommended age is an important public health objective.

Several studies have shown that coverage for many vaccines in China is lower in nonlocals, migrants from rural to urban areas, than locals, including coverage for pneumococcus and measles.6,14,23 Of China’s 1.3 billion people, 260 million are nonlocals, and in Shanghai, 9 of 23 million residents are nonlocals. These nonlocals do not have official residency papers, or hukou, which accord Chinese citizens access to local government entitlement programs24,25; however, children are offered EPI vaccines for free in China regardless of their residency status.

Nonlocals often group together in neighborhoods,26 and this demographic clustering, along with other social characteristics associated with neighborhoods, could influence an individual’s attitudes toward vaccination through a variety of mechanisms. Neighborhoods represent the environment in which the disease spreads and in which health care facilities provide preventive care. Previous studies in the Netherlands27 and Hawaii28 have found important links between neighborhood-level socioeconomic status and immunization uptake. Shanghai’s townships, a neighborhood administrative division that has on average over 100,000 people, have distinguishing demographic characteristics, and people within a township typically attend the same immunization clinic.

The influence of township-level traits on vaccination behaviors has not been well studied in China. Quantifying vaccination disparities between nonlocals and locals within the context of the township where they actually live is important for identifying pockets of susceptible populations and evaluating whether immunization programs are equitably reaching diverse groups of people. Moreover, public health programs targeting different vaccinations are not equally successful when they are subject to varying levels of governmental promotion, national attention and cost, as is true of the measles and pneumococcal vaccines. Accordingly, this study explores both MCV and PCV administration at 2 milestone ages: 9 and 24 months. These vaccines were chosen because they both historically have been responsible for a large burden of disease, but they are funded, and promoted, differently in China, with subsequent consequences that we wanted to quantify. Specifically, we estimate the proportion of children in Shanghai with these vaccination outcomes, compare vaccination outcomes between nonlocals and locals and assess the impact of township-level characteristics on vaccination outcomes.


Study Population

We used a single-stage cluster design to explore vaccination outcomes among children aged 9 months to 14 years in Shanghai. Townships were selected by a probability proportionate to size systematic selection procedure using population of children 0 to 14 years of age from the China 2010 Census as the population size. In each selected township, we sampled every child born between January 1, 2000, and July 4, 2014. From a preliminary analysis of older data, we determined that 24 clusters were needed to discriminate between proportions of 92.4% and 79.5%, the estimated values of MCV2 timeliness for locals and nonlocals, respectively, given an intracluster correlation coefficient of 0.133 calculated from an older dataset.

We examined MCV and PCV timeliness at 2 milestone ages. For the outcomes of MCV1 and PCV1 by (the start of) 9 months, only children ≥9 months were included. We excluded any child without a record of a measles vaccination because measles vaccination coverage is very high in China,14,15 and lack of a MCV1 record could be indicative of attrition from the dataset or a contraindication to vaccination. Similarly, for MCV2 and PCV1 by 24 months, we only included children ≥24 months who had a record of MCV2 administration.

Data Sources

This study uses individual-level data from a cohort in the Shanghai Immunization Program Information System (SIPIS) in addition to township-level data from the 2010 China Census. SIPIS includes information on children’s birthdate, sex, residency status (local vs. nonlocal), the township where they received their latest vaccination and individual dates of any vaccinations; no other individual-level information was available from the dataset. Urbanicity was defined by the district where the township was located; Huangpu, Xuhui, Changning, Jing’an, Putuo, Zhabei, Hongkou and Yangpu comprise the urban districts; the suburban districts are Minhang, Baoshan, Jiading, Pudong, Jinshan, Songjiang, Qingpu, Fengxian and Chongming. At the time of the study, Minhang used a separate, district-specific immunization information system. The database from Minhang contains similar information to SIPIS, and it was combined with the data from the other districts in SIPIS for the analysis.

The derivation of the vaccination outcomes was based on recommended ages at administration in Shanghai and the manufacturer’s instructions about how early the doses could be administered.9 The outcome MCV1 by 9 months was defined as a measles or measles-rubella vaccine administered when the child was between 8 and 9 months of age. Any administration before or after this age was considered not on-time. Similarly, MCV2 by 24 months was calculated as any measles-mumps-rubella (MMR) vaccine dose between the child’s 12th and 24th month, and doses administered before or after those ages were not on-time. Because PCV coverage is so low, we only considered dose 1 administration at both milestone ages. For PCV1 by 9 months, the dose could be administered when the child was 6 weeks to 9 months of age, and PCV1 by 24 months was any dose administered to the child between 6 weeks to 24 months of age.

The China 2010 Census provided information about township residency composition and child dependency ratio (CDR). The township residency composition was derived from the proportion of nonlocals living in the township, that is, 1 minus the proportion of the total population of registered permanent residents in the total resident population of the township. The CDR was calculated as the total population between the ages of 0 and 14 years divided by the total population between the ages of 15 and 65, multiplied by 100. The CDR estimates the density of children within the population of a township. In the multivariable regressions, the township residency composition was categorized based on which residency group, local or nonlocal, formed the majority of the population. The CDR was dichotomized at the median.

Statistical Analysis

Frequencies and proportions were calculated for each of the individual-level explanatory and outcome variables, and these proportions were compared by residency status. The mean and median were used to describe the distribution of the township-level variables before categorization.

For each analysis, we fit a multilevel model through a generalized estimating equation framework with a binomial distribution and logit link to account for the nested structure of individuals within a township. To account for intratownship correlation, we specified an exchangeable correlation matrix at the township level. The explanatory variables in each model were specified a priori and were the same for each outcome in order to facilitate comparisons across different vaccinations. These variables included residency, urbanicity, township proportion nonlocal and township CDR. To evaluate trends over time and to account for more complete records in SIPIS in recent years, both birth year centered at 2008 and a piecewise linear term after birth year 2008 were included in the models. Interactions were included for residency and 3 other variables: birth year, the piecewise linear term with changing slopes after birth year 2008 and township residency composition in order to examine changes over time by residency and differential impacts of township residency composition on nonlocals versus locals. Because of the differential probabilities of selection based on population size, we included population of children aged between 0 and 14 years in the township as quartiles in the regression. We calculated estimates and standard errors for the odds ratios (ORs) of locals compared with nonlocals in different strata by combining main and interaction coefficients. Plots of joint ORs comparing nonlocals to locals by township residency composition and at different birth years were constructed to facilitate interpretation of models. The precision of results was evaluated through 95% confidence intervals (CIs). The regression analyses were performed with R version 3.0.3,29 with additional packages geepack,30plotrix31 and ggplot2.32 To visualize age at vaccine uptake, we constructed cumulative vaccination curves stratified by residency and township residency composition for children in the dataset born in 2008 or after, using the cumulative incidence function macro in Statistical Analysis System.33

We also examined other indicators of immunization system functioning, including the interval in days between MCV1 and MCV2 and between PCV1 and PCV2. Doses with intervals less than 4 weeks were categorized as invalid. Vaccination before 6 weeks (for PCV1), 8 months (for MCV1) or 12 months (for MCV2) was categorized as invalid because of administration earlier than recommended. In line with guidance from the US Centers for Disease Control and Prevention and previous research, vaccine doses administered ≤4 days before the minimum age or minimum interval were still considered valid.34 We compared the proportion of invalid doses between locals and nonlocals with a χ2 test of independence.

Ethics Statement

This study was exempted from ethical approval by the University of Michigan Institutional Review Board and a Shanghai Centers for Disease Control and Prevention ethics committee because it was limited to analysis of previously de-identified data collected for public health purposes.


A sample of 416,750 children born between January 1, 2000, and July 4, 2014, was drawn from SIPIS for the study. The majority of children in the sample were nonlocals (61.2%), male (53.1%) and lived in Shanghai’s suburban districts (87.9%) (Table 2). The CDR ranged from 7.9 to 15.5 in the sample, with a median of 10.6. The proportion of nonlocals in the townships varied between 17% and 74%, and the median was 66%.

Table 2:
Distribution of Demographic Characteristics Overall and by Residency Status in a Sample of Children From the SIPIS, July 2014

From the initial sample of 416,750 children, we have drawn 2 separate samples. For analyses involving MCV1 or PCV1 by 9 months we have limited our sample to the 341,134 children who had a record of MCV1 in SIPIS. For analyses involving MCV2 or PCV1 by 24 months, our sample is limited to the 276,544 children who have a record of MCV2 in SIPIS. Table 3 shows the distribution of vaccination outcomes in the total sample and by residency. The proportion of children with MCV1 by 9 months was 82.5% and with MCV2 by 24 months was 86.0%. Very few children had PCV1 administered by 9 months (2.9%) or by 24 months (3.8%). Locals had more on-time administration of MCV and higher PCV coverage than nonlocals. There was a trend of increasing uptake for each vaccine dose across birth years (Fig. 1).

Table 3:
Distribution of Vaccination Outcomes Overall and by Residency Status in a Sample of Children From the SIPIS, July 2014
Proportion of children with PCV1 by 9 and 24 months and who have MCV1 by 9 months and MCV2 by 24 months.

Findings from the multivariable regressions are shown in Table 4. For children born in 2008 who lived in local-majority townships, nonlocals had lower odds of any vaccination outcomes. Local children had worse vaccination outcomes in nonlocal-majority townships than in local-majority townships, and the interaction terms between individual residency status and township residency composition reveal that living in nonlocal-majority townships leads to differentially worse vaccination outcomes for nonlocals than locals. For instance, from the regression model’s main effects, we estimate that the odds of administration of MCV1 by 9 months is 0.50 times as high for nonlocals compared with locals (95% CI: 0.47, 0.53). Because we have included an interaction term between individual residency status and township residency composition, this estimate refers solely to nonlocals in local-majority townships. In nonlocal-majority townships, the odds of MCV1 administration by 9 months, comparing nonlocals to locals, is 0.84 times (95% CI: 0.80, 0.88) as the OR estimate in local-majority townships.

Table 4:
Odds Ratios and 95% CIs of 5 Different Vaccination Outcomes According to Generalized Estimating Equations Regressions in a Sample of Children From the SIPIS, July 2014

The ORs comparing nonlocals and locals across select birth years and different township settings are graphically depicted in Figure 2. Except for MCV2 timeliness, the disparity in vaccination outcomes between nonlocals and locals decreased over time, with no significant difference in the odds of PCV administration between locals and nonlocals for children born in 2012. Additionally, there is less disparity between nonlocals and locals in local-majority townships than in nonlocal-majority townships.

ORs and 95% CIs comparing vaccination outcomes in nonlocals versus locals by birth year and township residency composition (black boxes indicate local-majority townships, and white boxes nonlocal-majority townships).

People living in townships with an above-median CDR had lower odds of MCV1 by 9 months (OR: 0.93; 95% CI: 0.91, 0.95) and MCV2 by 24 months (OR: 0.92; 95% CI: 0.89, 0.95) than those from townships with a below-median CDR. The opposite direction of association was seen for pneumococcal vaccinations. The odds of PCV1 by 9 months of age (OR: 1.21, 95% CI: 1.15, 1.27) and PCV1 by 24 months (OR: 1.13, 95% CI: 1.07, 1.19) were higher for those living in townships with an above-median CDR compared with those from townships with a below-median CDR.

Figure 3 shows the cumulative vaccination coverage for the vaccines under consideration: MCV1, MCV2 and PCV1. For MCV1 and MCV2, there is rapid uptake of the vaccine after 8 and 18 months, respectively, the ages at which the vaccine is first recommended. For PCV1, uptake begins at 3 months, at which age it typically starts being promoted for use, but the uptake is much slower over time. For all 3 vaccine doses, nonlocals living in nonlocal-majority townships had the lowest rate of vaccination, whereas locals living in local-majority townships had more rapid, and more timely, uptake of the vaccine.

Cumulative vaccination coverage of MCV1, MCV2 and PCV1 among Shanghai children born between January 1, 2008, and July 4, 2012.

There was low frequency of invalid doses because of administration earlier than recommended or administration within an interval shorter than recommended. The interval between the first 2 PCV doses ranged from 9 to 1532 days (median: 48 days, interquartile range: 34 to 67 days), and the median interval between the first 2 MCV doses was 306 days (range: 1 to 5271 days; interquartile range: 297 to 329 days). Only 0.05% (7/14,742) of PCV2 doses were administered <24 days from PCV1; 0.06% (155/274,369) of MCV2 doses were given at or after an invalid interval. The proportion of doses administered too early was 0.06% (19/30,630) for PCV1, 1.00% (3425/339,646) for MCV1 and 1.06% (3162/294,179). Nonlocals had higher proportion of early-invalid doses for MCV1 (1.24% vs. 0.64%, P < 0.0001) and MCV2 (1.49% vs. 0.49%, P < 0.0001), but there was no statistically significant difference for PCV1 (0.08% vs. 0.05%, P = 0.31).


Before the advent of widespread childhood vaccination in China, 3 to 4 million cases of measles35 and almost 700,000 cases of IPD21 occurred each year. With widespread measles vaccination, the number of measles cases has dropped precipitously, while the burden of IPD has remained high because of less usage of pneumococcal vaccines. The wide divergence between measles and pneumococcal vaccination coverage is evident in our study; we found very few children receiving pneumococcal vaccination by 2 years, in contrast to almost universal, and mostly timely, measles vaccination of Chinese children. This difference is a direct consequence of the Chinese government’s considerably different public health policies and funding mechanisms for these 2 vaccines.

Given that measles is so infectious, our findings that MCV1 and MCV2 timeliness fell below 90% indicates that there is a delay in attaining protective levels of herd immunity in young infants. These results are similar to findings from our previous study in Tianjin, another large municipality in China, where <90% of children had an on-time administration of MCV1.15 A 2012 study in Zhejiang, a province that borders Shanghai, found even lower timeliness of MCV1 with only 70.1% of children receiving on-time administration of MCV1.14 Our estimates of on-time MCV2 administration were closer to those in studies from developed countries: Dannetun et al36 found administration of MMR by 2 years to be between 80% and 90% in 3 different cohorts in Sweden, and only about 90.4% of American parents who did not intentionally delay vaccination had timely MMR according to the 2003 National Immunization Survey.37 Although each of these studies shows high levels of on-time MCV administration, it is nonetheless below herd immunity thresholds, meaning that infants’ protection against measles is unnecessarily delayed.38 Despite several studies suggesting there is high coverage of measles and other EPI vaccines in China regardless of timing,4,14,15 the late vaccine administration could be one explanation for the difficulty in controlling some vaccine-preventable diseases and is manifest in China’s inability to meet the 2012 measles elimination target.13

We found very low uptake of PCV. A survey of parents across all provinces in mainland China found that a slightly higher proportion of children, 9.9%, had received PCV1 by 2 years compared with this study.39 In contrast, in the 73 countries eligible for financial support from the Global Alliance for Vaccines and Immunization, uptake of the third dose of PCV, a more stringent standard than what we or Zheng et al investigated, was 19%.39,40 It is concerning that China, which is too wealthy to be eligible for funding from Global Alliance for Vaccines and Immunization, has lower PCV coverage than many poorer countries supported by Global Alliance for Vaccines and Immunization. Although academicians and Chinese public health officials have called for China to introduce PCV as a government-funded vaccine,5 Che et al41 indicated that this may not be cost effective. Government funding is likely necessary for eliminating disparities in PCV administration between demographic groups while realizing sizeable reductions in IPD morbidity. Moreover, newer, higher-valent vaccines than the 7-valent PCV may provide greater coverage and be more cost effective in China.

Urbanicity in China is correlated with other sociodemographic factors; more urban areas are generally characterized as economically developed with residents who have better health compared with counterparts in less urban areas.42 Accordingly, we found that PCV1 administration is lower in suburban districts compared with urban districts, possibly indicating greater sensitivity to higher prices in economically less-developed districts. Conversely, on-time MCV administration was higher in suburban districts compared with urban districts. Future research can address the reasons behind this positive association. For example, are doctors in suburban districts more conscientious about vaccinating children on time? Is it easier to attend clinics for suburban dwellers (because of transportation, child cared for by grandparents or other relatives, job situations, etc.)? And do suburban residents express more positive social norms toward free vaccines? We also note that our models controlled for township residency composition, which is correlated with urbanicity. Previous studies that have found lower uptake of vaccines in suburban versus urban areas did not control for the composition of different townships,6,43 and therefore may have incurred residual confounding.

On-time MCV and PCV administration was found to be lower in nonlocals than locals. Considering that there is substantial clustering of people by residency within China, these low vaccination levels may herald future challenges to controlling the spread of measles and pneumococcal disease within the nonlocal population. Moreover, nonlocals had even worse outcomes in nonlocal-majority townships compared with local-majority townships. This disparity may result from other factors associated with nonlocal-majority townships, such as low socioeconomic status, lower performing immunization services or heterogeneity in where different types of migrants settle within Shanghai.44

In the context of the CDR, there was a clear delineation between patterns for MCV versus PCV administration. A larger CDR was associated with worse MCV timeliness, perhaps because it is more difficult to arrange vaccination services for children within a recommended time frame with greater numbers of children in the township. However, a larger CDR was also associated with greater probability of pneumococcal vaccination, suggesting that a greater number of children in someone’s living area may be accompanied by a commensurate increase in social norms that prompts parents to seek vaccination for their child.

Strengths and Limitations

This study has a number of limitations. We used data from the SIPIS to calculate vaccination coverage, which limited us to data since the year 2000. However, data before 2008 were sparse and SIPIS was not comprehensively used throughout the city until after 2010. Absolute numbers may be biased and may overestimate vaccination outcomes, especially for earlier years. Additionally, attrition may be a problem: children who move away from Shanghai will still have vaccination records in SIPIS from when they lived in the city, but vaccinations occurring outside of the city will not be entered into SIPIS, even though SIPIS will still have a record of that child; by limiting our dataset to children with known vaccinations at the milestone ages, we were able to ensure that they had not yet moved out of the city. Finally, the SIPIS dataset includes few individual-level variables. Income, education and personal beliefs toward health care services could confound the relationship between residency status or township characteristics and vaccination outcomes. In addition, there is plausibly substantial heterogeneity within both locals and nonlocals in terms of socioeconomic status and health care beliefs that could be important predictors of up-to-date vaccination status. Future studies should collect this information to better explore how parents in Shanghai elect to give their child certain vaccines. The composition of nonlocals may also have changed over time as more people move into the city. Future studies could also provide more insight on how to best categorize the township-level factors that we consider in this article. Nonetheless, this study population constitutes a representative sample of children in Shanghai, and we were able to observe characteristics associated with rare outcomes (like PCV uptake) because of the large sample size.


China has made great strides in reducing the burden of vaccine-preventable diseases through its EPI, but late measles vaccination continues to be a challenge to reducing measles cases among infants and the overall coverage with pneumococcal vaccines is extremely low by international standards. China’s efforts to eliminate measles should be accompanied by improvements in immunization services as a whole; vaccination against measles should not be the sole objective but rather a means and opportunity to improve programs that provide immunizations against other diseases.45 To this end, both measles vaccination and pneumococcal vaccination could be used as standard indicators of different but equally important aspects of immunization program performance.

The SIPIS was the source of data for this study. Although immunization information systems like this one may have limited capacity for obtaining data on individual-level behaviors, they nonetheless can provide critical immunization data for analysis that can then be used to evaluate and improve public health practices.46,47 As China’s public health information systems become more comprehensive, their potential for predicting areas with low vaccination coverage, detecting hot spots for potential disease outbreaks, identifying clinics that have difficulties in organizing immunization services and delineating populations that are, or are not, willing to obtain novel immunizations will likely improve.


Data for the China 2010 Census was obtained from the China Data Center through the University of Michigan Asia Library. We wish to extend our appreciation to the staff at the Shanghai Centers for Disease Control and Prevention for familiarizing us with SIPIS. This research was funded by the University of Michigan Office of Global Public Health and by a University of Michigan Rackham International Research Award. The study sponsors had no role in the study design, data collection, data analysis and interpretation, manuscript preparation or decision to submit the manuscript for publication.


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measles vaccines; pneumococcal vaccines; immunization programs; China

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