Human Vaccines & Immunotherapeutics

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Age-appropriate vaccination coverage and its

determinants for the polio containing vaccine
1-3 and measles-containing vaccine doses in
Zhejiang province, China: A community-based
cross-sectional study

Yu Hu, Yaping Chen, Ying Wang, Hu Liang & Huakun Lv

To cite this article: Yu Hu, Yaping Chen, Ying Wang, Hu Liang & Huakun Lv (2020) Age-
appropriate vaccination coverage and its determinants for the polio containing vaccine 1-3
and measles-containing vaccine doses in Zhejiang province, China: A community-based
cross-sectional study, Human Vaccines & Immunotherapeutics, 16:9, 2257-2264, DOI:
10.1080/21645515.2020.1718439

To link to this article: https://doi.org/10.1080/21645515.2020.1718439

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HUMAN VACCINES & IMMUNOTHERAPEUTICS
2020, VOL. 16, NO. 9, 2257–2264
https://doi.org/10.1080/21645515.2020.1718439

RESEARCH PAPER

Age-appropriate vaccination coverage and its determinants for the polio containing
vaccine 1-3 and measles-containing vaccine doses in Zhejiang province, China: A
community-based cross-sectional study
Yu Hu, Yaping Chen, Ying Wang, Hu Liang, and Huakun Lv
Institute of Immunization and Prevention, Zhejiang Center for Disease Control and Prevention, Hangzhou, China

ABSTRACT ARTICLE HISTORY

Background: This study aimed to evaluate the age-appropriate coverage and its associated risk factors Received 13 November 2019
for the primary vaccination of Polio containing vaccine (PCV) and measles-containing vaccine (MCV) Revised 26 December 2019
through the secondary use of the 2018 Zhejiang provincial coverage survey among children aged 12–23 Accepted 14 January 2020
months. KEYWORDS
Methods: Data were collected through structured pre-tested Chinese version questionnaire by face-to- Vaccination coverage; age-
face interview among 770 mothers whose children aged 12–23 months. Age-appropriate vaccination appropriate; determinant;
coverage was measured using Chinese vaccination schedule recommendation. Bivariate and multivariate polio containing vaccine;
logistic regression models were adopted to identify determinants of the age-inappropriate vaccination. measles containing vaccine
Results: The age-appropriate vaccination coverage of PCV1, PCV2, PCV3, and MCV was 88.8%, 80.8%,
73.6%, and 75.7%, respectively. The risk factors associated with the age-inappropriate vaccination of PCV
1–3 dose and MCV included child’s gender, birthplace, living area, maternal education level, immigration
status, monthly household income, participation of the pregnant women’s seminar, antenatal care
follow-up, knowledge on vaccination.
Conclusion: The proportions of age-appropriate vaccination coverage were low compared with the up-
to-date coverage. Modifiable factors were associated with age-inappropriate vaccinations. Vaccination
interventions should consider identified modifiable factors to improve age-appropriate vaccination
coverage.

Introduction
Remarkable progress on up-to-date vaccination coverage has
been made since 1980 worldwide, which resulted in the reduc-
tion of 2–3 million children’s death from vaccine-preventable
diseases (VPDs) every year.1 However, an estimate of 1.5 million
children still die from VPDs every year, mainly in developing
countries.2 It requires both high vaccination coverage and timely
administration of vaccines to attain full benefits of vaccination as
untimely but high vaccination coverage will lead the policy
makers to false assumption of disease protection. Hence, each
vaccine dose should be administrated at defined age and delay is
undesired and with a required interval, based on the immuniza-
tion schedule.3,4
The recommended vaccination schedule is designed to
protect infants and children early in life, when they are most
vulnerable to VPDs, though reducing the risk of infection of
VPDs among unimmunized children as an effect of herd
immunity. Administrating a vaccination before the minimum
recommended age to start or the minimum interval of 4-week
would reduce the immune response and it should be repeated
if the vaccination is given more than 4 days before the mini-
mum age.5 However, prolonging the interval between doses of
vaccine doses leads to the higher antibody level theoretically,
but may increase vulnerability to VPDs. Moreover, delayed
vaccination may end up with an altered schedule of vaccina-
tion that causes nonspecific effects with negative conse-
quences on the prevention of VPDs. Besides, delayed
vaccination was found as an independent risk factor for per-
tussis, measles, and invasive haemophilus Influenzae type b -
diseases.6–8
As a developed province in east China, Zhejiang has
a geographic area of 101,800 km2, with a population of
69 million. Zhejiang province consists of 11 cities, 90 counties,
and 1319 towns. Vaccination is one of the public health policy
strategies to improve the children’s health through the admin-
istration of vaccines to develop children’s protection from
VPDs since 1978, when China launched the expanded pro-
gram on immunization (EPI). Vaccines are categorized into
two types: EPI vaccines are mandatory and free to all children,
provided by the central government, and non-EPI vaccines
are voluntary and need out-of-pocket expense. Polio contain-
ing vaccine (PCV) and measles-containing vaccine (MCV) are
an EPI vaccine. According to the Chinese EPI primary sche-
dule, three doses of PCV and one dose of MCV should be
administrated at 2,3,4 and 8 months of age, setting a goal of
90% vaccination coverage among target children.
Previous reports indicated that few children received all
vaccinations at the relevant recommended age timely, even

CONTACT Huakun Lv zjmyslhk@sina.com Institute of Immunization and Prevention, Zhejiang Center for Disease Control and Prevention, No. 3399 Binsheng
Road, Binjiang District, Hangzhou, P.R. China
© 2020 Taylor & Francis Group, LLC
2258 Y. HU ET AL.
achieving the high coverage.3,9,10 Similarly, researchers had
observed a substantial delay in timely vaccination in
China.11,12 However, these studies so far focused solely on
completeness of vaccination schedule and studies that evalu-
ated the timeliness of vaccination were scarce. PCV and MCV
were reliable parameters for assessing age-appropriate vacci-
nation among children.13 Hence, we evaluated the age-
appropriate coverage and its associated risk factors for the
primary vaccination of PCV (1–3 dose) and MCV in Zhejiang
province through the secondary use of the 2018 provincial
coverage survey among children aged 12–23 months.
Methods
Study period and design
A community-based cross-sectional study was implemented
to evaluate the timeliness vaccination coverage and its risk
factors in September 2018.
Setting and target population
The annual birth rate was increasing due to the opening of
two-child policy in recent years. Based on the census of 2017,
the estimated new birth was 709542 and 357726 were males,
with an average birth rate of 1.1%. Due to the rapid social-
economic development in last two decades, more than
22 million migrants from undeveloped middle or western
areas of China have flown into Zhejiang province. The immu-
nization program was coordinated by the EPI office at pro-
vincial, municipal, and district levels, who led the
implementation of EPI in all 1628 immunization clinics
located in the community health service center or its satellite
health post in every community. The vaccination service was
managed by 2–4 full-time and well trained EPI focal persons
in immunization clinics. Except for providing vaccination, the
EPI focal persons were responsible for a house-to-house chil-
dren identification and registration, defaulter tracing and
awareness creation in their catchment areas. The focal persons
conducted a house-to-house visit at least once per month to
update the target children’s information while having the
vaccination registration at hand. Hence, even though a child
was born in the community or flow into the community from
other area or whether he/she had been vaccinated, he/she
would be registered and get vaccinations finally.
Children aged 12 to 23 months (born from
1 September 2016 to 31 August 2017) with their mothers
living in Zhejiang province in the study period were the
source population. Children who had an immunization card
with written records of vaccination dates were included.
Sample size and sampling technique
The sample size was determined using the household-based
cluster survey method recommended by WHO14 as follows:
z2 pð1pÞ
Nmin ¼ deff  ð1α=2Þ d2 . Following assumptions were
considered: a two-tailed α error of 5%, a permissible error
(d) of 0.05, a design effect (deff) of 2, and the expected age-
appropriate coverage of PCV 1–3 and MCV at 50%, as there
were no previous estimates in Zhejiang province. As such, the
final sample size was required for each city was 70 eligible
children for each city, corresponding to 770 children at pro-
vincial level, respectively.
The sample size was divided in seven towns of ten. The
investigation procedures included three steps: first, seven
towns were selected from all towns of each city, by probability
proportional to population size. Second, one community was
randomly selected from each town and one index household
was randomly selected from the list of all households in that
town, both two selection processes were based on the table of
random numbers. Third, the adjacent household right to the
previous household was selected till 10 households were
investigated in that town. There were three other criterions
to follow: (1) Only one eligible child per household was
chosen; (2) Households should arranged another visit if
there was somebody living but without any response; (3)
The closest community was selected if adequate sample
could not be obtained in the selected community.
Data collection and quality assurance
Data were collected through structured pre-tested Chinese
version questionnaire by face-to-face interview. The question-
naire had variables of socio-demographic factors, health ser-
vice utilization, vaccination status and reasons for none, early
or delayed vaccination. Children’s vaccination status was col-
lected from immunization card held by mothers.
Fifty-five EPI professionals participated in this study as
data collectors and supervisors. Before the actual survey, all
data collectors and supervisors received a training to make
them understand the main objectives of this study and each
questions in the questionnaire. Supervisors should check the
data quality daily, by examining the completeness, consis-
tency, accuracy, and clarity.
The reliability of the eight questions measuring the knowl-
edge on vaccination was assessed by using Cronbach’s alpha
(α) and the internal consistency estimate of the reliability was
found in a good range (α = 0.877).
Definitions
Hereby we made some definitions for this study as follows: (1)
Age-appropriate vaccination (timely) was defined if a child
was vaccinated within 1 month after the minimum age to
administer the dose as recommended by Chinese EPI or the
package insert of the vaccine. (2) Age-inappropriate vaccina-
tion (untimely) was defined if a child was vaccinated earlier
and/or delayed than the recommended age. (3) Delayed vac-
cination was measured as not having received the recom-
mended vaccine dose within 1 month (30.5 days for every
month in average) beyond the minimum age. Accordingly,
the PCV 1–3 dose and MMR were categorized as delayed at
>92, >122, and >153 and >580 days, respectively. (4) Early
vaccination was defined as dose given before the minimum
age. (5) Up-to-date vaccination was defined as the proportion
of target children who were vaccinated with PCV 1–3 dose

and MCV regardless of the time of vaccination. (6) Sufficient
knowledge was defined as score greater than the mean when
eight knowledge questions were asked. (7) Favorable attitude
was measured when respondents positively reacted to at least
three out of the four attitude questions regarding vaccination.
Data analysis
Data were entered into Epi-data 3.0 software after checking
the completeness and exported to Stata 14.0 (Stata Corp. 2015,
Stata statistical software, college station, TX, USA) for data
analysis. Descriptive statistics were conducted to describe the
data after cleaning and coding. The status of each vaccination
was dichotomized as age-appropriate and age-inappropriate.
The cumulative probability of being vaccinated at age for each
vaccine dose was calculated through inverse Kaplan-Meier
survival function. Children who had not received vaccine
doses at 23 months of age were considered as censored.
Bivariate and multivariate logistic regression models were
adopted to identify determinants of the age-inappropriate
vaccination. Each variable was checked by using the chi-
square goodness of fit test to be identified as a candidate
variable in the regression model. Multi-collinearity between
independent variables was also checked by calculating the
variance inflation factor (VIF) before the multivariate regres-
sion. In order to control the confounding effect, each variable
of P-value ≤0.2 in the bivariate analysis was considered to be
a candidate variable for multivariate logistic regression model.
Forward stepwise regression method was also used to control
confounding effect between independent variables. Crude
odds ratio (COR) and adjusted odds ratio (AOR) with 95%
confidence interval (CI) were calculated to observe the
strength of association between the outcome variable and
independent variables. All analyses were based on a two-
tailed P-value of 0.05 as significant. We used survey weights
through the STATA “svy” command in our analyses.
Ethics considerations
This study was approved by the ethical review board of
ZJCDC (T-072-W). All surveys were conducted in accordance
with the relevant regulation and study protocol. Written
informed consent was obtained from each mother once
there was a decision to participate.
Results
Socio-demographic characteristics of mothers and their
children
A total of 770 mothers with their children aged 12–23 months
were surveyed. Of these mothers, 404 (52.5%) were living in
rural areas and 483 (62.7%) were under 30 years of age. Five
hundred ninety-six (77.4%) mothers had an education back-
ground over senior middle school and 550 (71.4%) mothers
were resident. Four hundred ninety-seven (64.5%) were
employed and 38.4% of mothers had a monthly household
income over 10000 CNY. The proportion of male children
was 50.3% and the proportion of the 1st birth order was 57.5%
HUMAN VACCINES & IMMUNOTHERAPEUTICS 2259
and 92.9% were born at hospitals. Moreover, 6.8% of mothers
did not attend the pregnant women’s seminar at all and 23.0%
did not receive the postnatal care service and 13.5% did not
receive the antenatal care follow-up. The proportion of suffi-
cient knowledge and favorable attitude on vaccination was
55.3% and 92.3%, respectively (Table 1).
Age-appropriate vaccination
Up-to-date vaccination coverage for PCV 1–3 dose and MCV
was 99.4%, 99.0%,98.6% and 96.1%, respectively. However,
only 88.8% for PCV1, 80.8% for PCV2, 73.6% for PCV3 and
75.7% for MCV were vaccinated age-appropriately. Overall,
71.7% of the surveyed children received all the four target
doses at their appropriate age, while 5.2% had not received
any dose on time. The proportion of vaccine doses admini-
strated earlier than the recommended vaccination schedule
was 3.1%, 3.7%, 1.7% and 1.9% for PCV 1–3 dose and
MCV, respectively. The magnitudes of delayed PCV 1–3
dose and MCV were 8.1%, 15.5%, 24.6% and 22.4%, respec-
tively (Table 2). Figure 1 shows the cumulative vaccination
coverage for each vaccine dose at a specified age. Four refer-
ence lines on this figure showed the proportion of children
delayed the specific vaccinations (after the reference line).
Reasons for none or age-inappropriate vaccination
Table 3 presents the reasons for none or age-inappropriate
vaccination for PCV 1–3 dose and MCV. The most common
reason for none or delayed vaccination was child being sick
on the appointment day (49.2%). Other reasons included
mother or caregivers being too busy (20.0%), forgotten or
no vaccination appointment (12.9%), inconvenient due to
the appointed time or place (5.6%) and vaccine stock out
(4.2%). The reason given by mothers for early reception of
vaccination was health workers’ appointment before the
recommended time (8.1%).
Factors associated with age-inappropriate vaccinations
The risk factors associated with the age-inappropriate vaccination
of PCV 1–3 dose and MCV in the multivariate logistic regression
models were presented in Table 4. The risk factors of age-
inappropriate PCV1 included child’s gender of female (AOR:
2.1, 95% CI:1.5–3.5), birthplace at home (AOR:3.2, 95%
CI:1.9–4.6), child who living in urban area (AOR: 1.7, 95%
CI:1.2–2.5), maternal education level under senior middle school
(AOR: 2.5, 95% CI:2.0–3.6), migrant children (AOR: 3.6, 95%
CI:2.3–5.4), monthly household income of under 5000 CNY
(AOR: 1.7, 95% CI:1.1–2.5), not participated the pregnant
women’s seminar (AOR: 4.3, 95% CI:2.6–6.5), no antenatal care
(ANC) follow-up (AOR: 1.8, 95% CI:1.2–3.2), insufficient knowl-
edge on vaccination (AOR: 3.5, 95% CI:1.8–5.2). The risk factors of
age-inappropriate PCV2 included birthplace at home (AOR:1.8,
95% CI:1.5–3.0), child who living in urban area (AOR: 1.4, 95%
CI:1.2–1.9), maternal education level under senior middle school
(AOR: 2.5, 95% CI:1.9–3.8), migrant children (AOR: 2.7, 95%
CI:1.8–4.2), not participated the pregnant women’s seminar
(AOR: 3.5, 95% CI:1.9–4.3), no ANC follow-up (AOR: 2.0, 95%
2260 Y. HU ET AL.

Figure 1. Cumulative coverage of PCV 1–3 dose and MCV.

Table 1. Socio-demographic characteristics of respondents and their children in Table 3. Frequency of reasons for none or age-inappropriate vaccination among
Zhejiang province, east China, 2018 (N = 770). children aged 12–23 months in Zhejiang province, east China, 2018.
Variable Level Frequency % Reasons Frequency %
Child‘s gender Male 387 50.3 Health workers appointed me before the recommended 54 8.1
Female 383 49.7 time
Birth order 1 443 57.5 Mother or caregivers being too busy 133 20.0
2 297 38.6 Forgotten or no vaccination appointment 86 12.9
≥3 30 3.9 Inconvenient due to the appointed time or place 37 5.6
Birthplace Hospital 715 92.9 Child being sick on the appointment day 328 49.2
Home 55 7.1 Vaccine stock out 28 4.2
Residency Rural 404 52.5 Total 666 100.0
Urban 366 47.5
Age (years) <30 483 62.7
≥30 287 37.3
Mother‘s education < Senior middle school 174 22.6
≥ Senior middle school 596 77.4
CI:1.6–4.3), insufficient knowledge on vaccination (AOR: 2.7, 95%
Immigration status Resident 550 71.4 CI:1.9–5.2). The risk factors of age-inappropriate PCV3 included
Migrant 220 28.6 child who living in urban area (AOR: 1.6, 95% CI:1.2–2.3), mater-
Maternal employment status Home fulltime 273 35.5
Employed 497 64.5 nal education level under senior middle school (AOR: 2.4, 95%
Household income per month <5000 CNY 96 12.5 CI:1.8–4.5), migrant children (AOR: 2.4, 95% CI:1.9–3.8), not
5000-10000 CNY 378 49.1
>10000 CNY 296 38.4 participated the pregnant women’s seminar (AOR: 3.6, 95%
Pregnant women’s seminar Not participated 52 6.8 CI:2.6–5.7), no ANC follow-up (AOR: 2.1, 95% CI:1.5–3.6), insuf-
≤2 432 56.1 ficient knowledge on vaccination (AOR: 1.6, 95% CI:1.2–2.4). The
≥3 286 37.1
PNC service Not received 177 23.0 risk factors of age-inappropriate MCV included maternal educa-
At least once 593 77.0 tion level under senior middle school (AOR: 2.2, 95% CI:1.6–3.6),
ANC follow-up No follow-up 104 13.5
≤2 184 23.9 migrant children (AOR: 1.7, 95% CI:1.5–2.9), not participated the
≥3 482 62.6 pregnant women’s seminar (AOR: 2.4, 95% CI:1.5–2.9), no ANC
Knowledge on vaccination Sufficient 426 55.3 follow-up (AOR: 1.8, 95% CI:1.4–2.6). No Intersectionality was
Insufficient 344 44.7
Attitude toward vaccination Unfavorable 59 7.7 found between the risk factors of the age-appropriate vaccination
Favorable 711 92.3 coverage for PCV 1–3 dose and MCV.
PNC: postnatal care; ANC: antenatal care; Pregnant women’s seminar: is
a monthly pregnant women’s meeting held at each community health center
regarding pregnancy, childbirth, postnatal care and other health-related issues.
Discussion
Full benefits of vaccination could be attained through both high
Table 2. Timeliness of vaccination among children aged 12–23 months in coverage and timely administration. The target set by WHO of
Zhejiang province, east China, 2018.
90% for each vaccine dose was achieved for up-to-date cover-
Timeliness PCV1(%) PCV2(%) PCV3(%) MCV(%)
age, which was consistent with previous reports from various
Early 24(3.1) 28(3.7) 13(1.7) 14(1.9)
Age-appropriate 679(88.8) 616(80.8) 559(73.6) 560(75.7) parts of world.15–17 However, the age-appropriate coverage for
Delayed 62(8.1) 118(15.5) 187(24.6) 166(22.4) PCV 1–3 and MCV ranged from 73.6% to 88.8%. Although the
Up-to-date 765(100) 762(100) 759(100) 740(100) results were higher than the findings from other setting,4,10,18
Table 4. Risk factors associated with age-inappropriate PCV and MCV vaccination among children aged 12–23 months of age in Zhejiang province, east China, 2018.
PCV1 PCV2 PCV3 MCV
Variable Level COR (95% CI) AOR (95% CI) COR (95% CI) AOR (95% CI) COR (95% CI) AOR (95% CI) COR (95% CI) AOR (95% CI)
Child‘s gender Male Ref Ref Ref Ref Ref - Ref -
Female 2.0(1.4–3.1) 2.1(1.5–3.5)* 1.5(1.2–2.6) 1.1(0.9–1.6) 1.2(0.9–1.4) - 1.1(0.8–1.4) -
Birth order 1 Ref - Ref - Ref - Ref -
2 1.3(0.9–1.6) - 1.1(0.8–1.4) - 1.2(0.9–1.8) - 1.1(0.9–1.3) -
≥3 1.2(0.9–1.7) - 1.1(0.8–1.6) - 0.9(0.8–1.4) - 0.9(0.8–1.2) -
Birthplace Hospital Ref Ref Ref Ref Ref Ref Ref Ref
Home 3.4(1.7–5.4) 3.2(1.9–4.6)* 2.1(1.6–4.0) 1.8(1.5–3.0)* 1.7(1.2–2.5) 1.6(1.2–2.3)* 1.3(1.1–1.6) 1.1(0.8–1.8)
Residency Rural Ref Ref Ref Ref Ref - Ref -
Urban 1.8(1.2–2.9) 1.7(1.2–2.5)* 1.6(1.2–2.6) 1.4(1.2–1.9)* 1.2(0.8–1.7) - 1.1(0.9–1.5) -
Age (years) <30 Ref Ref Ref - Ref - Ref -
≥30 1.3(1.1–1.7) 1.1(0.9–1.6) 0.9(0,8–1.2) - 1.2(0.8–2.2) - 1.0(0.8–1.4) -
Mother‘s education ≥ Senior middle school Ref Ref Ref Ref Ref Ref Ref Ref
< Senior middle school 3.7(2.7–5.6) 2.5(2.0–3.6)* 3.1(2.2–4.9) 2.5(1.9–3.8)* 3.2(2.4–5.6) 2.4(1.8–4.5)* 2.8(2.0–4.2) 2.2(1.6–3.6)*
Immigration status Resident Ref Ref Ref Ref Ref Ref Ref Ref
Migrant 4.3(2.5–6.7) 3.6(2.3–5.4)* 4.0(2.0–6.3) 2.7(1.8–4.2)* 3.6(2.4–4.0) 2.4(1.9–3.8)* 1.9(1.6–3.2) 1.7(1.5–2.9)*
Maternal employment status Home fulltime Ref Ref Ref Ref Ref - Ref -
Employed 1.6(1.3–2.7) 1.2(0.9–2.3) 1.7(1.2–2.4) 1.2(0.9–1.8) 1.2(0.9–1.7) - 1.1(0.8–1.2) -
Household income per month <5000 CNY 1.6(1.2–2.4) 1.7(1.1–2.5)* 1.5(1.2–2.1) 1.3(0.9–1.7) 1.2(0.9–1.6) - 1.1(0.8–1.3) -
5000-10000 CNY 0.9(0.6–1.4) 1.0(0.9–1.3) 1.0(0.8–1.3) 1.0(0.9–1.0) 0.9(0.8–1.2) - 1.0(0.9–1.2) -
>10000 CNY Ref Ref Ref Ref Ref - Ref -
Pregnant women’s seminar Not participated 3.3(1.9–5.6) 4.3(2.6–6.5)* 3.7(2.0–5.4) 3.5(1.9–4.3) * 3.0(2.2–4.1) 3.6(2.6–5.7)* 2.7(2.2–3.1) 2.4(1.5–2.9)*
≤2 1.4(1.0–2.0) 1.3(0.8–1.1) 1.6(1.2–3.2) 1.4(0.9–2.1) 1.4(0.8–2.0) 1.2(1.1–2.4)* 1.1(0.9–2.4) 1.2(0.9–1.9)
≥3 Ref Ref Ref Ref Ref Ref Ref Ref
PNC service Not received 1.4(1.2–2.3) (0.8–1.3) 1.2(0.8–2.1) - 1.1(0.9–1.8) - 1.0(0.8–1.4) -
At least once Ref Ref Ref - Ref - Ref -
ANC follow-up No follow-up 2.3(1.4–4.0) 1.8(1.2–3.2)* 2.5(1.7–3.8) 2.0(1.6–4.3)* 2.5(1.9–4.4) 2.1(1.5–3.6)* 2.4(1.4–4.2) 1.8(1.4–2.6)*
≤2 1.6(1,2–2.7) 1.4(0.9–2.0) 1.2(0.8–1.5) 1.1(0.9–1.3) 1.4(1.2–1.5) 1.2(0.9–1.7) 1.4(1.0–2.2) 1.1(0.9–1.6)
≥3 Ref Ref Ref Ref Ref Ref Ref Ref
Knowledge on vaccination Sufficient Ref Ref Ref Ref Ref Ref Ref -
Insufficient 4.3(2.1–5.8) 3.5(1.8–5.2)* 3.5(2.2–6.3) 2.7(1.9–5.2)* 2.8(1.5–3.2) 1.6(1.2–2.4)* 1.2(0.9–1.7) -
Attitude toward vaccination Favorable Ref - Ref - Ref - Ref -
Unfavorable 1.2(0.9–1.7) - 1.1(0.8–1.6) - 1.2(0.9–1.5) - 1.0(0.9–1.4) -
*P < 0.05 in the multivariate logistic regression models.
HUMAN VACCINES & IMMUNOTHERAPEUTICS
2261
2262 Y. HU ET AL.
the age-appropriate coverage was still lower than the up-to-date
coverage. It could be due to the national EPI policy, which had
target to achieve a more than 90% vaccination coverage for
each vaccine dose, had simply focused on the crude estimate of
coverage, irrespective of the time of administration. This was
also in line with the previous studies from developing and even
developed countries, which reported a high proportion of
delayed vaccination despite of the observed high up-to-date
coverage.4,10,19 Pooling of unprotected or delayed protected
susceptible individuals would contribute for the occurrence of
outbreaks of VPDs. As such, we recommended that the age-
appropriate vaccination coverage should be considered as
another important indicator of performance of EPI to ensure
the timely administration of vaccination for children.
Moreover, as the experience of Italy,20 measles elimination, of
course to all VPDs, would remain unrealized dreams unless the
EPI focused on its timeliness of vaccination with strong poli-
tical commitment.
In this study, we found that the age-appropriate coverage
was not only low, but also declined as the dose went from
PCV1 to PCV3 and MCV. We assumed that the possible
reason was due to the increased mother’s workload with
domestic activities while her child became older and thereby
might be with little regard for her child’s vaccination appoint-
ments. Another explanation was the adverse events such as
fever, pain or swelling on the injection site, following the prior
doses that would restrain mothers for the next appointment.
Several studies worldwide did not consider the negative
effects of the early administration of vaccines, we found that
1–3% early administration of antigens for PCV1-3 or MCV.
These results were lower than the findings from Burkina
Faso.21 According to the Chinese Advisory Committee on
Immunization Practice (CACIP) recommendation, these
early administrated doses could lead to low seroconversion
level that might not protect children from infection of VPDs.
These doses would count as invalid and should be repeated. It
indicated that vaccination providers appointed mothers and
administrated vaccine doses before the schedule for a variety
of reasons. For example, in a study from Ethiopia,15 the early
administration of measles vaccine was associated with the
multi-dose vial opening policy and nearly all mothers blamed
the providers for appointing them before the schedule of
measles vaccine. In fact, the vaccinators want to find sufficient
numbers of children in a vaccination session to save the
multi-dose vial measles vaccine. However, this reason might
not to explain the finding observed in this study as the MCV
was one dose vial in China. Hence, further research on the
early administration of vaccines was thus warranted.
Four vaccine, dose specific models produced a unique
combination of mother’s education level, immigration status,
participation of pregnant women’s seminar, and ANC follow-
up as the risk factors to timeliness of vaccination. It indicated
that difference existed in risk factors associated with time-
liness of each vaccine dose. This distinction was very impor-
tant to understand the characteristics of children who were
more likely to experience the delayed vaccinations and to
intervene accordingly. Being male child was found to be
a protective factor from age-inappropriate PCV1 vaccination.
It was possible that our result represented a gender preference
toward a male, which was consistent with the previous report
done in Ethiopia.22 However, no correlation was detected
between gender and untimely vaccination in Kenya.19 It was
largely attributed to the false belief that only boy could carry
on the family name.19 Children born at hospitals were more
likely to receive the vaccinations in a timely manner in our
research. It was in line with the studies done in other
areas.23,24 We assumed that mother who gave birth at hospital
was more likely to be informed to use the health service such
as childhood immunization, through the health education
from hospitals. Furthermore, the administration of HBV1 at
birth would also inform mother to get the subsequent vaccine
doses timely. The disparity in age-appropriate coverage
between urban and rural could be explained by the different
provision methods of primary health care. In rural areas,
vaccination was an important part of the village doctors’
regular work and a closer relationship could be observed
between providers and rural population. The close-knit nature
of the community results in the rapid spread of information
and encourages each eligible individual to participate in the
clinic. However, the connection between children’s caregivers
and provider was lacking and most doctors working in urban
health facilities had little time to explain the importance of
vaccinations to every people that could have a negative impact
on vaccination coverage and its timeliness. Lower education
level would also impede mother to understand or accept the
knowledge or advice on childhood vaccination from provi-
ders, which could have a negative impact on the timeliness of
vaccination. Our findings indicated that migrant children
never replicated the patterns of utilization of vaccination
service in residents. We attributed the higher delayed vaccina-
tion among migrant children to the vulnerability of migrants
in the new sociocultural environment, poor demand for
health service, poor satisfaction, as well as the capacity of
providing the extra services toward migrant people. Children
from poorer families probably had untimely vaccinations in
our study. It was in line with a previous report that showed
the poverty impeded the utilization of public health service.25
The possible explanation was that indirect cost or deducting
wages for work leave caused by bringing children to get
vaccination would restrict the utilization of vaccination ser-
vice. Failure to participate in pregnant women’s seminar
increases the odds of age-inappropriate vaccination, which
was consistent with previous reports that supported the effec-
tiveness of early intervention in the prenatal care settings.26,27
ANC follow-up was observed as a positive factor of the timely
vaccination. We considered that ANC follow-up could convey
the concepts in a manner that would allow mothers easily
understand and accept them, and would induce a positive
influence on maternal vaccination knowledge.
Our study was subjected to several limitations. First, mother’s
recall bias in remembering the frequency of maternal health
service utilization and the reasons for none or age-inappropriate
vaccination could not be ignored, especially if the child aged 2
years. Second, knowledge and attitude congruent with the social
acceptable values could be over-reported while those congruent
with socially undesirable could be under-reported. Nonetheless,
this study provided detailed information to support the policy-
makers in low timeliness settings in directing resource or

designing interventions toward a goal of protecting children from
VPDs. Third, only children with written vaccination records were
included in the survey and it would induce the potential selection
bias which would increase the age-appropriate coverage since
children without any written vaccination records were more
likely to be missed by routine vaccination service.
Conclusions
The age-appropriate coverage was significantly lower than the
up-to-date coverage. The risk factors of age-inappropriate vac-
cination included child’s gender, birthplace, living areas, mater-
nal education level, immigration status, household income,
participation of pregnant women’s seminar, ANC follow-up
and vaccination knowledge. Our results suggested the policy-
makers integrate the age-appropriate vaccination coverage rate
into the measurements system of EPI performance. Any inter-
vention should consider identified risk factors to increase the
age-appropriate vaccination. Vaccination providers should also
focus on reducing the early or delayed vaccinations.
Acknowledgments
The authors would like to thank the vaccination staff from 11 CDCs at
city level for their investigation and data collection.
Author contributions
Yu Hu, Huakun Lv conceived and designed the experiments; Yaping Chen
performed the experiments; Yu Hu and Ying Wang analyzed the data; Hui
Liang contributed reagents/materials/analysis tools; Yu Hu wrote the paper.
Disclosure of potential conflicts of interest
The authors declare no conflicts of interest.
Funding
This work was supported by the Research on the commercial insurance
compensation system of adverse effect after immunization in Zhejiang
Province [2020376461].
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