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Contents lists available at ScienceDirect
Journal of Infection and Public Health
journal homepage: http://www.elsevier.com/locate/jiph
Epidemiological characteristics of measles from 2000 to 2014: Results
of a measles catch-up vaccination campaign in Xianyang, China
a,b c,1 d b b,∗
Rong-Qiang Zhang , Hong-Bing Li , Feng-Ying Li , Li-Xin Han , Yong-Min Xiong
a
School of Public Health, Shaanxi University of Chinese Medicine, Shiji Road, Xianyang, Shaanxi 712046, PR China
b
Institute of Endemic Diseases of School of Public Health, Health Science Center, Xi’an Jiaotong University; Key Laboratory of Environment and Genes
Related to Diseases of Ministry of Education; Key Laboratory of Trace Elements and Endemic Diseases of Ministry of Health, Xi’an, Shaanxi 710061, PR China
c
Center for Disease Control and Prevention of Baoji City, Shaanxi 721006, PR China
d
Center for Disease Control and Prevention of Xianyang City, Shaanxi 712046, PR China
a r t i c l e i n f o a b s t r a c t
Article history: This study was a cross-sectional case-control study aimed at (1) identifying risk factors contributing to
Received 25 July 2016
the measles epidemic and (2) evaluating the impacts of measles-containing vaccines (MCVs), with the
Received in revised form 21 January 2017
goal of providing evidence-based recommendations for measles elimination strategies in China. Data on
Accepted 4 February 2017
measles cases from 2000 to 2014 were obtained from a passive surveillance system at the Center for Dis-
eases Prevention and Control in Xianyang. The effectiveness of MCVs was evaluated in 357 patients with
Keywords:
a vaccination history and 503 healthy randomly selected controls. Patient data were subjected to multi-
Epidemiological characteristics
variable logistic regression modeling. From 2005 to 2014, the average incidence of measles in Xianyang
Measles
Vaccination was 5.42 cases per 100,000 people. The second MCV dose was highly protective in 8-month-old infants.
MCVs in general have been highly protective in 8-month-old infants. Multivariable logistic regression
modeling indicated that age (≥2 years vs. <2 years), MCV dose 2 vaccination, and MV vaccination were
each independently associated with measles case status. In conclusions: A MCV should be administered
on time to all age-eligible children, reproductive-age women, and migrant populations, to maximize herd
immunity to measles.
© 2017 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health
Sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
Introduction measles-related deaths were reported worldwide in 2014, with
most of these deaths occurring in children under 5 years old [2].
Measles is an acute highly contagious disease that is caused by Measles remains a leading vaccine-preventable cause of child
the measles virus, which is transmitted mainly by droplets through mortality in China. According to the Chinese Health Statistics Year-
the nose, mouth or throat of infected persons. A measles vaccine book, in 2013, the incidence rate for measles was 0.46/100,000
has been available in China since the 1960s, and China initiated its Chinese citizens, with a fatality rate of 0.13%. This incidence rate
Expanded Program on Immunization in 1978 [1]. In China, measles represents a marked improvement relative to 2001, when China
has affected primarily children, especially after 1978 [2]. Although saw a measles incidence of nearly 25/100,000 people. This improve-
substantial decreases in the measles incidence rate and measles- ment can be attributed to the introduction of routine measles
related mortality have occurred, measles remains common in many immunization recommendations and supplementary immuniza-
countries around the world. According to the World Health Organi- tion activities [2]. The Chinese government has committed to
zation (WHO), more than 20 million people develop measles every joining the global effort to eliminate measles [1–4], by implement-
year and 95% of measles deaths in recent years occur in developing ing robust routine immunization services and a supplementary
countries with weak health infrastructures. An estimated 114,900 immunization activities (SIAs) program with the aim of achiev-
ing this goal. Many countries and regions have benefitted from
WHO-recommended SIAs, including Xianyang. The measles inci-
dence rate decreased dramatically in Xianyang after 2007, when
∗ SIA commenced in the region.
Corresponding author at: School of Public Health, Health Science Center of
By 1989, measles had been nearly eliminated. However, in
Xi’an Jiaotong University, No 76 Yanta West Road, Xi’an, Shaanxi 710061, PR China.
2010, surveillance data detected a small measles epidemic in
Fax: +86 29 82655032.
E-mail address: [email protected] (Y.-M. Xiong). Xianyang, China. The number of reported measles cases in 2010 1
Co-first author.
http://dx.doi.org/10.1016/j.jiph.2017.02.005
1876-0341/© 2017 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Zhang R-Q, et al. Epidemiological characteristics of measles from 2000 to 2014: Results of a measles
catch-up vaccination campaign in Xianyang, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.02.005
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2 R.-Q. Zhang et al. / Journal of Infection and Public Health xxx (2017) xxx–xxx
(January–December) was nearly five times greater than that in within the prior month); four-fold or greater increase in anti-
2009. We analyzed the epidemiological characteristics of the measles serum IgG antibody; or antibody-negative in acute phase
measles from 2001 to 2014, with the aim of identifying contributory and antibody-positive in recovery phase; and isolation of confirmed
factors, and evaluated the impacts of measles-containing vaccines measles virus (e.g. viral RNA identification) from nasopharyn-
(MCVs) with the aim of providing evidence-based recommenda- geal secretions or blood. These cases should be categorized as
tions for measles elimination strategies in Shaanxi province. For laboratory-confirmed cases.
the purposes of this study MCVs included MCV dose 1 (first dose To ensure diagnosis reliability, confirmatory serological testing
given at 8 months), MCV dose 2 (second dose at 1–2 years), and the was performed on all patients with suspected measles (including
measles and rubella vaccine. clinical measles cases) by detecting specific measles IgG antibod-
ies (detection threshold of 0.3 IU/L) with a commercially available
Materials and methods ELISA kit (Yanhui Biotechnology Company, China), according to the
manufacturer’s instructions. When laboratory results contradicted
Study area, data collection, and management clinical signs, we used the results of the laboratory diagnosis. In this
study, we used data from all laboratory-confirmed and clinically
Xianyang is a city in Shaanxi province located in the hinterland
diagnosed measles cases.
of the Guanzhong plains with a population of about 5.4 million
people. Beyond its populous urban areas, Xianyang includes remote
Case-control study
villages that can only be reached on foot.
Measles is a legally mandated notifiable disease in China. The
To evaluate the role of the MCVs in measles prevention, we con-
National Notifiable Diseases Surveillance System (NNDSS) was
ducted a case-control study from 2009 through 2014. The patients
established by the Chinese National Centers for Disease Control
in the case group had been treated in one of 13 counties or districts
(CDC) in 2004 and updated to include the expanding variety of
in Xianyang between 2009 and 2014; their data were obtained from
infectious diseases and more disease-related information (such as
the NNDSS.
immunization history) of case investigations in 2008. This system
The subjects in the control group were healthy people who had
requires physicians to report all suspected measles cases to the local
not been infected with measles; they were confirmed to be serum-
CDC within 12 h. For each suspected case, the local health author-
negative for measles-specific IgG antibodies. Firstly, five regions
ities are required to carry out an epidemiological investigation,
within Xianyang Province (Qin Du District, Wu Gong County,
which includes obtaining specimens for laboratory confirmation.
Chun Hua County, Jing Yang County, and Chang Wu County) were
The regional authorities reported the case report forms immedi-
selected from the 13 counties and districts of Xianyang by simple
ately to the Ministry of Health and the National CDC. The measles
random sampling. Based on the serum epidemiological charac-
incidence rates for the population, and the vaccination schedule
teristics of measles, infected patients (cases) and healthy control
from the annual disease surveillance reports (2000–2014) were
participants were divided into five age groups: <8 months, ≥8
downloaded from NNDSS for analyzing. The Center for Disease Con-
months to <2 years, ≥2 years to <10 years, >10 years to <20 years,
trol and Prevention of Xianyang is responsible for data collection
and ≥20 years.
and case reports in the region. In this paper, two types of data were
To obtain a control group of at least 500 subjects, at least 20
collected. First, the annual measles surveillance reports from 2001
subjects were selected randomly for each age group from each of
to 2014 were downloaded from NNDSS. Second, the measles and
the five selected regions. A total of 503 subjects were selected (with
rubella vaccine histories were recorded for 503 healthy individ-
the extra 21st individuals coming from Qin Du District, Chun Hua
uals in 2013–2014. The ministry of health required that the CDC
County, and Chang Wu County). Control data including vaccination
must carry out measles initiative monitoring at all geographic lev-
history and demographic characteristics were collected in 2009 and
els, and in 2013 proposed a mandatory measles reporting system to
2014 via a questionnaire. Our study protocol conforms to the eth-
improve reporting rates and prevent omissions. The demographic
ical guidelines of the Declaration of Helsinki-Ethical Principles for
data from 2000 to 2014 were acquired from the Xianyang Statis-
Medical Research Involving Human Subjects adopted by the 18th
tics Bureau. We were able to obtain detailed information about
World Medical Association General Assembly in Helsinki, Finland,
measles cases after 2005, following the 2004 NNDSS update. In
June 1964, as revised in Tokyo 2004. The ethics committee at Xi’an
2012–2014, there was no measles cases reported. Therefore, the
Jiaotong University approved the protocol, and all participants gave
presently analyzed dataset encompasses 2005–2011.
informed consent for their inclusion in the study.
Measles diagnosis Data analysis
All reported measles cases in this study were confirmed accord- We calculated odds ratios (ORs) to examine the association
ing to the WHO’s criteria [5]. Specifically, diagnoses were based on between several independent variables (sex, community, age, MCV
the clinical case descriptions and laboratory confirmation criteria. dose 2, and MCV dose 1) and measles case status. Individuals with
A clinical measles case is defined as an illness characterized by all of unknown vaccination status were excluded from the analysis of
◦
the following signs: red skin rash; fever of 38 C or higher; coughing, how vaccination history relates to measles infection. The precision
upper respiratory catarrhal symptoms, or conjunctivitis; measles of the results was assessed with 95% confidence intervals (CIs). We
spots (Koplik’s spots); and extension of red skin from the ear to the used chi-square tests to evaluate significance, with a significance
whole body. A number of conditions have features that may resem- cut-off level of 0.05. All statistical analyses were performed using
ble measles, including other viral infections (especially rubella), SPSS 20.0 statistical software. All significance tests were two-sided.
scarlet fever, Kawasaki disease, and toxic shock syndrome. These
diseases need to be ruled out before making a definitive measles Results
diagnosis.
For those cases in which the patients did not show typical symp- Measles incidence and mortality, 2000–2014
toms, the following laboratory findings were considered indicative
of a measles diagnosis: detection of anti-measles IgM antibod- With the implementation of a national routine program for
ies in the serum (unless live attenuated measles vaccine received immunization from 2000 to 2006, the measles incidence rate
Please cite this article in press as: Zhang R-Q, et al. Epidemiological characteristics of measles from 2000 to 2014: Results of a measles
catch-up vaccination campaign in Xianyang, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.02.005
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R.-Q. Zhang et al. / Journal of Infection and Public Health xxx (2017) xxx–xxx 3
Fig. 1. Measles incidence rates in Xianyang, China, 2000–2014 (incidence rates
available since 2000). EPI: National Expanded Programme on Immunization
including 15 vaccinations for infectious diseases based on the WHO/UNICEF rec-
ommendations of 1978.
decreased markedly. Routine vaccination was recommended to
continue to reduce the numbers of measles cases and strengthen
population immunity levels. The measles incidence rate reached
more than 23.63 per 100,000 people before 2006. A prioritized
measles catch-up vaccination campaign for children between 9
months and 7 years of age began in 2007. Expanded immuniza-
tion programs (including 15 vaccinations for infectious diseases,
such as Hepatitis A, measles, etc.) began in 2008, and a general
Fig. 2. Seasonal distribution and categories of measles cases, 2005–2011.
≥
population ( 8 months old) catch-up vaccination campaign com-
menced in 2010. As shown in Fig. 1, a total of 1,492 cases of measles
Age distribution of measles cases, 2005–2014
(including 1 death) were reported in the city of Xianyang from 2005
to 2014, yielding an average incidence of 5.42 measles cases per
During the period of 2005–2014, the largest portion of measles
100,000 people (from 2012 to 2014, there were no measles cases
cases (46.45%) occurred in infants and children under 3 years old.
reported in Xianyang).
Meanwhile, 9.99% of cases occurred in 4–6 year olds, 17.83% in
The geographical distribution and incidence of measles cases
7–15 year olds, and 25.73% in adults (≥16 years old).
were denoted by epidemiological intensity. In the period of
2000–2003, measles broke out in all districts, with district inci-
Immunization status, 2009–2014
dence rates ranging from 9.9/100,000 to 17.2/100,000. Measles
cases were observed in all of the districts within Xianyang, and
We collected data on vaccination history for measles cases from
the geographical distribution of measles cases varied from 2000 to
2009 to 2014. Of the 357 subjects that we investigated, 51.8% were
2014.
not vaccinated. The MCV dose 1 coverage rate was 14.94%, though
the vaccination status of a large proportion (33.05%) of subjects was
Seasonal distribution and categories of measles cases, 2005–2014 unknown. With respect to MCV dose 2, 59.10% subjects were not
vaccinated, the coverage rate of the rubella vaccine was only 3.36%,
From 2005 to 2014, a total of 1,492 measles cases were enrolled, and the vaccination status of a large proportion (37.54%) of subjects
including 566 clinically diagnosed cases and 926 laboratory con- was also unknown.
firmed cases. Most of the case confirmations were made through
lab testing (62.06%), and there were more than 400 measles cases
Correlation between measles vaccination and measles infection
in 2005 (Fig. 2A). Measles occurred in every month. Peaks in the
measles mainly occurred from April to July, which accounted for
The sociodemographic characteristics of the cases and controls
50.27% (750/1492) (Fig. 2B).
are reported and compared in Table 1. Briefly, the proportions of
Table 1
Sociodemographic characteristics of measles cases versus controls.
Sociodemographic characteristic Descriptor Cases of measles (N = 357) Controls (N = 503) t/Chi square P
Mean age (±SD) 4.31 ± 2.49 4.23 ± 3.45 0.374 0.708
Gender Males 228 (63.87) 299 (59.44) 1.721 0.190
Females 129 (36.13) 204 (40.56)
Community Urban 121 (33.89) 132 (26.24)
Rural 236 (66.11) 371 (73.76) 5.887 0.015
MCV dose 1 Given 54 (15.13) 358 (71.17) 318.571 0.000
Not given 185 (51.82) 31 (6.16)
Unknown 118 (33.05) 114 (22.66)
MCV dose 2 Given 12 (3.36) 246 (48.91) 233.684 0.000
Not given 211 (59.10) 208 (41.35)
Unknown 134 (37.54) 49 (9.74)
Note: SD, standard deviation.
Please cite this article in press as: Zhang R-Q, et al. Epidemiological characteristics of measles from 2000 to 2014: Results of a measles
catch-up vaccination campaign in Xianyang, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.02.005
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Table 2
Univariate analysis of vaccination history related to measles infection.
Vaccination history Number (proportion) OR 95% CI
Cases of measles (N = 357) Controls (N = 503)
MCV dose 1
Vaccinated 54 (15.13%) 358 (71.17%) 0.025 0.016, 0.041
Not vaccinated 185 (51.82%) 31 (6.16%) REF
MCV dose 2
Vaccinated 12 (3.36%) 246 (48.91%) 0.048 0.026, 0.089
Not vaccinated 211 (59.10%) 208 (41.35%) REF
Note: OR, odds ratio; CI, confidence interval. Individuals with unknown vaccination status were excluded from the analysis.
Table 3
Vaccination history of cases and controls.
Vaccine Age Cases of measles, N (%) Control, N (%)
Yes No Unknown Yes No Unknown
MCV dose 1 <8 mos. 0 (0.00) 12 (100.00) 0 (0.00) 0 (0.00) 10 (100.00) 0 (0.00)
≥8 mos. to <2 y 30 (12.50) 147 (61.25) 63 (26.25) 120 (88.89) 15 (11.11) 0 (0.00)
2 y to <10 y8(25.81) 9 (29.03) 14 (45.16) 195 (93.30) 0 (0.00) 14 (6.70)
10 y to <20 y 5 (20.83) 1 (4.17) 18 (75.00) 30 (37.97) 0 (0.00) 49 (62.03)
≥20 y 11 (22.00) 16 (32.00) 23 (46.00) 13 (18.57) 6 (8.57) 51 (72.86)
MCV dose 2 <8 mos. 0 (0.00) 19 (100.00) 0 (0.00) 0 (0.00) 22 (100.00) 0 (0.00)
≥8 mos. to <2 y 8 (3.48) 157 (68.26) 65 (28.26) 72 (49.66) 51 (50.34) 0 (0.00)
2 y to <10 y 2 (5.41) 12 (32.43) 23 (62.16) 145 (70.73) 60 (29.27) 0 (0.00)
10 y to <20 y1(4.76) 1 (4.76) 19 (90.48) 19 (22.89) 39 (46.99) 25 (30.12)
≥
20 years 1 (2.00) 22 (44.00) 27 (54.00) 10 (14.29) 36 (51.43) 24 (34.29)
Table 4
rates were among infants <8 months old [6]. In 2015, there was
Multivariable logistic regression of factors associated with measles case status.
an adult measles outbreak in Beijing. The incidence rate and vac-
Variable P OR 95% CI cination rate were both notably higher in Shaanxi province in
northwestern China than in other provinces. Owing to supplemen-
Lower Upper
tal immunization activities aimed at limiting the transmission of
Sex (female vs. male) 0.966 1.015 0.512 2.014
the measles virus among children aged 8 months to 14 years, dra-
Community (rural vs. urban) 0.519 1.256 0.628 2.511
matic decreases in the reported incidence of measles cases were
Age (≥2 y vs <2 y) 0.000 0.452 0.199 0.845
MCV dose 2 0.000 0.078 0.037 0.167 recorded nationally [7].
MCV dose 1 0.000 0.040 0.022 0.071 After several vaccination programs were implemented, the inci-
dence of measles declined markedly in Shaanxi province. However,
Note: OR, odds ratio; CI, confidence interval.
in recent years the incidence of measles has increased slightly
in the province, especially in Ankang city where a measles out-
urban population in the Case group were higher than those in the
break occurred in 2015. Meanwhile, the incidence of measles in
Control group. Conversely, the proportions of first and second MCV
Xianyang has decreased in recent years compared to other cities
doses given were much lower in the Case group than in the Control
owing to a program to eliminate measles, expanded immunization
group (Table 1).
programs, and the catch-up vaccination campaign. However, there
Analysis of the case-control data, which involved 357 cases and
was a small rise in the apparent measles incidence in 2005 likely
503 controls, showed that MCV dose 1 and MCV dose 2 were both
due to improved measles surveillance. In 2012–2014, measles inci-
highly protective (Table 2). We found that the vaccination rate
dence rates were reduced to the target level of 1 case of measles
for MCV dose 1 was lower in the case group than in the control
per 1 million people.
group, especially among subjects between 8 months and 10 years
Most previous measles vaccination studies in Xianyang [8,9] did
of age; findings for MCV dose 2 were similar to those for MCV dose
not consider age and were limited by a small sample size. Our study
1 (Table 3).
is the first to include individuals’ vaccination statuses in an anal-
ysis of the epidemiological characteristics of measles cases, and
Factors associated with measles case status to assess the possibility of a measles outbreak in Xianyang. Our
analysis indicated that nearly half of the cases in the city (46.45%,
The results of a multivariable logistic regression examining fac- 693/1492 cases) occurred in very young children between 1 month
tors associated with measles case status are reported in Table 4. and 3 years old. In most of these cases, the children were not vac-
Briefly, multivariable logistic regression modeling indicated that cinated, or their vaccination status was unknown; thus the MCV
≥
age ( 2 years vs. <2years), MCV dose 2, and MCV dose 1 were each coverage rate was low or unclear. The risk of measles was found
independently associated with measles case status. to increase with increasing age among children under 8 months
old, especially among children who had not been vaccinated [10].
Discussion The univariate analysis and case-control investigation showed that
the measles vaccination and second MCV dose were highly pro-
tective. Our Mantel Haenszel age-adjusted analysis confirmed that
With the success of MCVs, the WHO and the Chinese gov-
widespread use of MCV dose 1 and MCV dose 2 has had a signifi-
ernment set a goal of measles elimination by 2012 [5], and the
cant impact on measles epidemiology, especially for children under
incidence rate of measles in China has decreased markedly since
1 year old, consistent with previous reports [11,12].
2001. In 2012 and again in 2013, the highest measles incidence
Please cite this article in press as: Zhang R-Q, et al. Epidemiological characteristics of measles from 2000 to 2014: Results of a measles
catch-up vaccination campaign in Xianyang, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.02.005
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R.-Q. Zhang et al. / Journal of Infection and Public Health xxx (2017) xxx–xxx 5
There are many risk factors that increase the risk of a measles the epidemiological characteristics of the measles. And based on
outbreak, including climate, the immune status of the population, measles epidemiology in Xianyang, we assumed that the measles
and low birth weight in infants, among others. Xianyang has had a omission rate was less than 10% and would not have an obvious
two-dose vaccination policy for more than 25 years with the first impact on the analysis of its epidemiological characteristics.
dose scheduled for administration at 8 months of age, and the sec- Our analysis indicated that the incidence of measles decreased
ond dose being given between 7 and 18 years of age [13]. Despite in recent years in Xianyang, China after a series of strategies
the vaccination policy, measles still occurs in Xianyang, with the have been implemented, and most cases of measles occurred in
majority of measles cases occurring in non-vaccinated individuals. non-vaccinated individuals. Measles vaccinations were highly pro-
Despite high MCV coverage, measles and mumps outbreaks con- tective in children who were at least 8 months of age. This study
tinue to occur in infants and young adults in Xianyang. Reported confirms that widespread use of MCVs in healthy people has had
immunization coverage can overestimate actual immunity level a significant impact on measles epidemiology. The MCVs should
greatly in infants [14], due to the fact that not all vaccinated infants be administered on time to all age-eligible children, women of
will produce the measles antibodies required for immunity. Prior reproductive age, and the floating population, to maximize the
to the MCV era, infants relied solely on passive transfer of mater- elimination of measles in the non-immunized group.
nal anti-measles antibodies [15,16]. However, a high proportion of
pregnant women were not vaccinated. Measles vaccination status
Acknowledgements
was unknown or missing for 67% of pregnant women with measles
[3]. Studies showed that seropositive measles rates decreased from
The authors wish to thank the staff at the CDC offices in the 13
60.0% in the 0–1-month-old group to 18.2% in the 6–7-month-old
counties of Xianyang, Shaanxi Province, China, for their contribu-
group. Seropositivity increased starting with the 8–9-month age
tions to measles case reporting. The authors would specifically like
band and reached 90.1% in the 24–47-month age band [4]. Maternal
to thank Y. Yang from the CDC office in Qindu District and Y.Y. Feng
attitudes and knowledge, including perception of vaccine neces-
from the CDC office in Wugong County for their research support
sity and knowledge of the immunization schedule, were associated
and help.
with measles vaccination and timeliness of measles vaccination
[17]. Among women born before 1985, measles antibody presence
rates are low in Shaanxi [18]. These low rates can be attributed to References
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Please cite this article in press as: Zhang R-Q, et al. Epidemiological characteristics of measles from 2000 to 2014: Results of a measles
catch-up vaccination campaign in Xianyang, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.02.005