Measles vaccine coverage and factors related to uncompleted vaccination among 18-month-old and 36-month-old children in Kyoto, Japan
© Matsumura et al; licensee BioMed Central Ltd. 2005
Received: 05 October 2004
Accepted: 04 June 2005
Published: 04 June 2005
Due to low vaccine coverage, Japan has not only experienced outbreaks of measles but has also been exporting it overseas. This study aims to survey measles vaccine coverage and the factors uncompleted vaccination among community-living children.
Subjects were the parents whose children had undergone either an 18-month or a 36-month checkup publicly provided by Kyoto City during November 2001 to January 2002. An anonymous self-administered questionnaire survey was conducted.
The coverage was 73.2% among the 18-month-old children (n = 2707) and 88.9% among the 36-month-old children (n = 2340), respectively. The following characteristics of mothers were related to uncompleted measles vaccination: aged below 30, working, concerned about the adverse events of the vaccine, and had insufficient knowledge. Similarly, the following characteristics among children were related to uncompleted measles vaccination: not the first-born child, interacting with other children in group settings. The coverage was the lowest among the children whose mothers were concerned about the adverse events of the vaccine without proper knowledge of measles and its vaccination.
To increase vaccine coverage among children, parents' awareness about measles and vaccination against it should be promoted, especially for working mothers. Efforts to enhance access to vaccination services and to communicate with parents about changing vaccination schedules are necessary.
Despite the existence of a safe, effective, and inexpensive vaccine, measles is still not being controlled in many parts of the world. The use of measles vaccine over the last 30 years has reduced global measles morbidity and mortality by 74 and 85%, respectively, compared with the prevaccine era. Regional elimination goals have been established in the Americas (by 2000), Europe (by 2007) and the Eastern Mediterranean (by 2010) .
Vaccine coverage in excess of 95% interrupts endemic transmission of measles in many countries, but achievement of such coverage almost always requires great collaborative efforts.  The global strategy began in the 1990s and many countries implemented immunization and enhanced measles surveillance policies related to this during the late 1990's. Some (e.g. the Americas) achieved measles elimination quite early [2, 3]. Since 2000, the WHO and UNICEF have recommended that, in addition to achieving high coverage with the first dose of measles vaccine, all children should be offered a second opportunity for measles vaccination to increase the total number of people who are immune .
In the United States, measles was targeted for elimination, and persisted at low incidence until 1989, when an epidemic swept the country. To prevent spread among school-age populations, a second dose of MMR vaccine is recommended. To increase immunization coverage among inner-city preschool populations, a number of activities have been undertaken to improve the immunization delivery system[5, 6]. Today, measles has been eliminated in the United States .
During 1997 and 2001, a total of 156 (82%) of 191 countries provided a second opportunity to receive a vaccination through supplementary immunization activities or through routine health services. Japan remains as one of the remaining 35 countries that do not give a second opportunity for measles vaccination . Of the 26 imported measles cases detected in the US in 2000, the largest number of these cases was from Japan (seven cases). In 2000, Japan is reported to be the principal exporting country of measles to the US .
The Immunization Law in Japan has been providing children with measles vaccination since 1978. Since Measles-mumps-rubella (MMR) vaccine was introduced into Japan in 1989, a number of cases of post-vaccination aseptic meningitis have been reported and these have been attributed to the use of Urabe Am9 mumps vaccine . In 1993, the Ministry of Health and Welfare (MHW) withdrew the domestically produced MMR vaccine . As of 1994, an amendment to the Immunization Law made vaccination voluntary and not mandatory. According to the present law, a single dose of measles vaccine is recommended for children over one year of age. Children are eligible to receive measles vaccination after 12 months following birth but not beyond 90 months. Until January 2004, adminisiration of measles vaccine was recommended between 12 and 24 months of age, instead of between 12 and 15 months when children have the greatest risk of contracting measles . In Japan, measles vaccine coverage has remained low, and either small or moderate outbreaks have occurred repeatedly in communities. According to an infectious disease surveillance (2000), total measles cases were estimated to be from 180,000 to 210,000, and total deaths were estimated to be 88 [11, 12]. Measles cases are most frequently observed among non-immunized children, particularly between 12 to 24 months. However, a nation-wide survey conducted in 2000 showed that measles vaccine coverage in Japan was 81.4%, which is not enough to prevent outbreaks . In this context, the Japan Pediatric Association, the Japan Child Health Association, and the Japanese Association of Pediatrics jointly appealed to the Ministry of Health, Labor and Welfare to promote vaccination against measles in July 2001 . Although secondary vaccine failure (SVF) has increased in Japan and discussion on two dose measles immunization has begun [15, 16], actual increase in vaccine coverage among children between 12 to 24 months-old become a priority in the present setting. The level of vaccine coverage within a community is necessary to develop appropriate measures. Still, no public system in Japan is capable of providing such information on a regular basis.
The purpose of the present study is to examine the following: measles vaccine coverage among 18-month-old and 36-month-old children; parents' knowledge of and perceptions about measles and its vaccination; and factors related to uncompleted measles vaccination in Japanese local communities.
The present survey was conducted in Kyoto City, an area that covers 610 km2 and is situated in the middle of the Kinki district of Japan and has a population of 1.47 million as of October 2001. The number of one-year-olds and three-year-olds in Kyoto City are approximately 12,000 respectively. The survey covers a period of three months extending from November 2001 to January 2002. Subjects were parents of children who had received either an 18-month or a 36-month checkup at either one of the 11 health centers or the three substations in Kyoto City. In Japan, parents are encouraged to have their children receive 18-month and 36-month checkups at public health centers. The present survey was conducted in cooperation with the Kami-gyo Public Health Center located in Kyoto City. An anonymous self-administered questionnaire was sent out to each subject, enclosed with a pre-consultation form, which is usually posted to the parents prior to the health checkup. Questionnaire, which subjects completed at home, were collected on the day of the checkup. The questionnaire included items on relevant attributes of parents (e.g. gender, age, job status); relevant attributes of children (e.g. birth order, whether or not they interacted with other children in group settings (e.g. attending nursery schools), and presence/absence of allergy); the child's vaccination history; whether or not the child had contracted measles in the past; reasons for not receiving measles vaccination (if the relevant child had not been vaccinated against measles); knowledge regarding measles and its vaccination, and sources of information regarding measles vaccination.
Questionnaire items regarding knowledge of measles and its vaccination were developed based on a survey conducted in 1991, which investigated parents' awareness of the plausible grave consequences of contracting measles and the importance of measles vaccination .
Characteristics of group 1~4
Statistical software (JMP4J, SAS institute) was used to carry out the analysis. For the validation study, the subject's answer to the question regarding the child's vaccination history was checked against the child's Personal Health Record Book (this control was conducted only for a certain number of subjects).
The number of children who received a health checkup and the response rate
During the survey period, 90.6% of 18-month-old children (3072 out of 3391) and 85.7% of 36-month-old children (2836 out of 3308) in the city received a health checkup. The response rate was 88.1% (2707 respondents out of 3072 patients who received a health checkup) and 82.5% (2340 respondents out of 2836 patients who received a health checkup). Because the majority of parents who responded to the questionnaire were mothers (98.1% of respondents among the 18-month-old group and 99.8% of respondents among the 36-month-old group), the analysis was conducted under the assumption that all respondents were mothers.
Measles vaccine coverage and incidence of measles
Measles vaccine coverage was calculated by dividing number of respondents whose children had been vaccinated against measles by total number of respondents. Coverage was 73.2% among the 18-month-old group and 88.9% among the 36-month-old group. In both groups, there were 44 children with a history of measles. The cumulative incidence of measles was calculated as 1.6% for the 18-month-old group and 1.9% for the 36-month-old group. In both groups, measles incidence was significantly higher among children who interacted with other children in group settings compared to children who did not. (18-month-old group: 3.3% (95%CI: 2.1–5.1) vs. 1.2% (95%CI: 0.8–1.7), 36-month-old group: 2.9% (95%CI: 2.0–4.3) vs. 1.3% (95%CI: 0.8–2.0))
To test validity, we compared responses about their children's history of measles vaccination from all respondents whose children received a health checkup at Kami-gyo Public Health Center during this survey period with the data registered in their children's Personal Health Record Books. Results showed that 98.2% of respondents (108 out of 110 respondents) in the 18-month-old group and 98.3% of respondents (117 out of 119 respondents) in the 36-month-old group provided valid answers regarding their children's history of measles vaccination.
The reasons for not receiving measles vaccine
Reasons for not receiving measles vaccination (multiple answers)
Number of non-vaccinated children
n = 698
n = 211
has not yet received measles vaccination but is going to receive it in the near future
had a cold at the time of vaccination
had to receive other vaccinations first
wanted to receive measles vaccination but missed the chance to receive it
wasn't aware of/forgot about the vaccination schedule
was sick at the time of vaccination
has already been infected with measles
was concerned about adverse events of measles vaccination
naturally acquired immunity seems more effective than artificially acquired immunity
vaccination is no longer mandatory
vaccination does not seem to be sufficiently effective
Knowledge about measles
Knowledge about measles among the mothers of children eligible for 18-month or 36-month checkup
Percentage of respondents answering "yes"
n = 2707
n = 2340
All children should be vaccinated against measles once they have reached the age of one
Measles is accompanied by high fever
Measles is accompanied by rashes
Measles is highly contagious
Most people can be immunized against measles through vaccination
The best way to prevent measles is through vaccination
Severe cases of measles are more likely to occur in younger children
There are some reported cases of death from measles in Japan
Measles can cause encephalitis
Some measles-infected children may suffer from the sequelae of measles
Measles can cause pneumonia
Measles is accompanied by severe coughing
Predictors of uncompleted measles vaccination
Factors related to uncompleted measles vaccination (univariate analysis)
Mother's age (< 30 years)
Not first born child
Interaction with other children
Presence of allergy
Concern about adverse events
Mother's age (< 30 years)
Not first born child
Interaction with other children
Presence of allergy
Concern about adverse events
Factors related to uncompleted measles vaccination (multivariate analysis)
18 month group
36 month group
Mother's age (< 30 years)
Not first born child
Interaction with other children
Presence of allergy
High knowledge, low concern (Group 1)
Low knowledge, low concern (Group 2)
High knowledge, high concern (Group 3)
Low knowledge, high concern (Group 4)
Since 1978, measles vaccination has become part of routine vaccination schedules in Japan. Following the amendment to the Immunization Law in 1994, vaccination has become voluntary. According to this law, a single dose measles vaccine schedule is recommended for children over one year of age. Children are eligible to receive measles vaccination after 12 months following birth but not exceeding 90 months. In January 2004, a recommendation was issued that children should be vaccinated between 12 and 15 months of age, not between 12 and 24 months as it was previously. This change was proposed as a measure to prevent increased incidence of measles among non-vaccinated one-year-old children. Optional vaccination is available for individuals who are now older than the conventional age of vaccination. Due to low vaccine coverage, small or moderate outbreaks of measles are quite common in Japan. Although most infections occur in non-vaccinated young children around the age of one-year-old, cases of adult measles has also been on the rise [18–20]. Approximately 60% of reported measles cases in Japan involve people under the age of five years without a history of vaccination, and an increase in vaccination coverage at age one may be decreasing by approximately half, the total number of all measles patients .
To increase vaccine coverage against measles, an accurate estimate of the current rate of vaccine coverage is required. Presently, the coverage rate is calculated by dividing total number of persons vaccinated per year by total number of children between the ages of 12 and 24 months . This formula does not accurately represent the actual number of children who have or have not been vaccinated against measles. In Japan, local governments are responsible for vaccination in their respective populations. Vaccination policy thus differs across different cities, towns and villages (namely, individual or mass vaccination, provided with or without charge, and vaccination age ranging from 12 to 18 months). Approximately 90% of local governments in Japan, including Kyoto City, provide vaccination to children who are older than one-year on an individual basis without charge . According to the nation-wide survey conducted in 2000 (total number of persons vaccinated against measles per year over total number of persons who were going to receive vaccination per year), measles vaccine coverage in Japan is 81.4%, surpassing 80% for the first time since the survey initially began . This survey's methodology, however, is problematic. The definition of denominator (total number of persons who were going to receive vaccination per year) differs across individual local governments. To obtain vaccine coverage is important for each local government.
Kyoto City experienced moderate-scale measles outbreaks in 1984, followed by smaller outbreaks in 1987, 1992 and 1997 at five-year intervals. The number of reported cases of measles at one point in 2001 was 205, with no reported cases of further spread. A further report identified that 44.4% of all measles cases occur in children ages two or below .
In the present survey, measles vaccine coverage, which was calculated by simply dividing the number of respondents whose children had been vaccinated by total number of respondents, was 73.2% among the 18-month-old group and 88.9% among the 36-month-old group. The percentage of children in Kyoto City that actually received health checkup was 90.6% among 18-month-olds and 85.7% among 36-month-olds. Because it can be assumed that vaccine coverage rate may be lower among children who do not receive health checkups, actual coverage rate may also be lower than that indicated in the present study.
Several previous surveys in Japan report vaccine coverage among 18-month children to be around 70% and that among 36-month children to be around 90% [23–25]. These findings are consistent with the present study. Several studies have also reported that factors related to a child-bearing environment, such as young motherhood, mother working, not being the first-born child, and attending nursery school, may contribute to low vaccine coverage [23–25]. Our findings agree. The present study also confirmed that factors such as concern about adverse events and low levels of knowledge were significantly associated with uncompleted measles vaccination. We checked for colinearity in the multivariate regression model. The correlation coefficients except among "mother working" and "interaction with other children" was 0.01–0.29. Although the correlation coefficients among "mother working" and "interaction with other children" was high (0.75 in 18-month group and 0.66 in 36-month group), these are different matters and we are interested in both of them. We put both of them into the final model, and got the result that we can interpret.
Lieu textitet al. examined the MMR vaccination history among 15-month-old children from affluent families and the factors that may delay vaccination. These factors were: having a large number of children, not having a regular doctor, not knowing when the shot was due, and not worrying about the risk of shots . The present study showed that measles vaccine coverage was lowest among the group of children whose mothers were concerned about the adverse events of the vaccine without proper knowledge of measles and its vaccination (the coverage: was 18-month-old group: 61.9%, 36-month-old group: 85.0%). Even among mothers who indicated their concern about adverse events, the odds ratio of uncompleted measles vaccination was higher in those who had insufficient knowledge regarding measles and its vaccination. These results suggest that the level of knowledge is more highly correlated with immunization status than the level of concern about adverse events; this highlights the importance of promoting awareness among parents regarding measles vaccination. Effort is needed to improve benefit and risk communication . Most important to vaccination is a balanced approach to the potential risks of natural infection, vaccine benefits, and adverse reactions to the vaccine. Given the potential risk of natural measles infection and the vaccine's efficiency and safety, the benefits are obvious .
As part of a campaign to raise awareness of measles vaccination in Japan among parents whose children are about to be enrolled in nursery schools, kindergartens and elementary schools, the Japanese Medical Association and the Japanese Association of Pediatrics have jointly launched a Vaccination Week for Children in March, 2004. During this Vaccination Week, consultation regarding measles vaccination was available to parents, and vaccination was carried out both on Saturday and Sunday.
In order to promote measles vaccination, further consideration should be given to the following measures: to promote awareness about measles, the benefits of measles vaccine, and the possibility of adverse events from vaccination among parents, especially among those who are aged below 30 or those who have two or more children; to establish a system to enhance access to vaccination services by, for example, providing vaccination services at nights and on weekends, and; to encourage and support nursery school staff in promoting vaccination as well as in collecting vaccination history data about the children.
We appreciate the cooperation of the Kami-gyo Public health Center, City of Kyoto and its staff.
- Cutts FT, Henao-Restrepo A, Olive JM: Measles elimination: progress and challenges. Vaccine. 1999, 17 (Suppl 3): S47-52. 10.1016/S0264-410X(99)00309-6.View ArticlePubMedGoogle Scholar
- Duke T, Mgone CS: Measles: not just another viral exanthem. Lancet. 2003, 361: 763-773. 10.1016/S0140-6736(03)12661-X.View ArticlePubMedGoogle Scholar
- de Quadros CA, Olive JM, Hersh BS, Strassburg MA, Henderson DA, Branding-Bennett D, Alleyne GA: Measles elimination in the Americas. Evolving strategies. JAMA. 1996, 275: 224-229. 10.1001/jama.275.3.224.View ArticlePubMedGoogle Scholar
- Centers for Disease Control and Prevention: Update: Global measles control and mortality reduction-worldwide, 1991–2001. MMWR. 2003, 52: 471-475.Google Scholar
- Wood DL, Brunell PA: Measles control in the United States: problems of the past and challenges for the future. Clin Microbiol Rev. 1995, 8: 260-267.PubMedPubMed CentralGoogle Scholar
- American Academy of Pediatrics. Committee on Infectious Diseases: Age for routine administration of the second dose of measles-mumps-rubella vaccine. Pediatrics. 1998, 101: 129-133. 10.1542/peds.101.1.129.View ArticleGoogle Scholar
- Centers for Disease Control and Prevention: Measles-United States, 2000. MMWR. 2002, 51: 120-123.Google Scholar
- Fujinaga T, Motegi Y, Tamura H, Kuroume T: A prefecture-wide survey of mumps meningitis associated with measles, mumps and rubella vaccine. Pediatr Infect Dis. 1991, 10: 204-209.View ArticleGoogle Scholar
- Ueda K, Miyazaki C, Hidaka Y, Okada K, Kusuhara K, Kadoya R: Aseptic meningitis caused by measles-mumps-rubella vaccine in Japan. Lancet. 1995, 346: 701-702. 10.1016/S0140-6736(95)92311-X.View ArticlePubMedGoogle Scholar
- Gomi H, Takahashi H: Why is measles still endemic in Japan?. Lancet. 2004, 364: 328-329. 10.1016/S0140-6736(04)16715-9.View ArticlePubMedGoogle Scholar
- Nakatani H, Sano T, Iuchi T: Development of Vaccination Policy in Japan: Current issues and policy directions. Jpn J Infect Dis. 2002, 55: 101-111.PubMedGoogle Scholar
- Nagai M: Second warning report on epidemics and patient estimation. the Study Group on the Evaluation of Sentinel Surveillance Annual Report granted by the Ministry of Health, Labour and Welfare. 2002, (in Japanese)Google Scholar
- Isomura S, Yamamoto N: A study on effective procedures for measles vaccination. Vaccine Working Group Report. granted by the Ministry of Health, Labour and Welfare. 2002, 189-196. (in Japanese)Google Scholar
- President of the Japan Pediatric Society, The Japanese Society of Child Health and the Japan Pediatric Association: For the improvement of measles vaccine coverage and towards its eradication. A petition submitted to the Ministry of Health, Labour and Welfare. 2002, (in Japanese)Google Scholar
- Hirose M, Hidaka Y, Miyazaki C, Ueda K, Yoshikawa H: Five cases of measles secondary vaccine failure with confirmed seroconversion after live measles vaccination. Scand J Infect Dis. 1997, 29: 187-190.View ArticlePubMedGoogle Scholar
- Kobune T, Katayama M, Okada H, Takeda M, Sato T, Tashiro M: Measles vaccine failures and control of measles in Japan. Clinical virology. 2000, 28: 10-14. (in Japanese)Google Scholar
- Isomura S: Factors affecting acceptance rate of measles vaccine. Virus. 1998, 48: 183-188. (in Japanese)PubMedGoogle Scholar
- Infectious Disease Surveillance Center: Measles 1999~2001. Infectious Agents Surveillance Report. 2001, 22: 273-277. (in Japanese)Google Scholar
- Nakano T, Ihara T, Kamiya H: Measles Outbreak among non-immunized children in a Japanese hospital. Scand J Infect Dis. 2002, 34: 426-429. 10.1080/00365540110080638.View ArticlePubMedGoogle Scholar
- Takayama N: Change in the age-distribution of measles patients admitted to our hospital from 1981 to 2002. Kansenshogaku Zasshi. 2003, 77: 488-492. (in Japanese)View ArticlePubMedGoogle Scholar
- Nakayama T, Zhou J, Fujino M: Current status of measles in Japan. J Infect Chemother. 2003, 9: 1-7. 10.1007/s10156-002-0206-6.View ArticlePubMedGoogle Scholar
- Bureau of Public Health and Welfare, City of Kyoto: Infectious Diseases Annual Report. Kyoto-City. 2001, 98-99. (in Japanese)Google Scholar
- Yasui Y, Imamura J, Imai T, Okazawa A, Kida K, Ichii M, Sunagawa T, Ohyama T, Okabe N, Okuno Y: Results of the CAP study on measles vaccine and anti-measures for measles in Sakai, Japan. Infectious Agents Surveillance Report. 2001, 22: 280-282. (in Japanese)Google Scholar
- Kato M, Takahashi H: An analysis of factors related to immunization rates. The journal of child health. 1999, 58: 373-378. (in Japanese)Google Scholar
- Koshida R, Inoue N, Asaka K, Sakurai N: Vaccination coverage at 36-month child health check-ups in the western area of Kanazawa station, Japan. Japanese journal of pediatrics. 2000, 53: 1685-1690. (in Japanese)Google Scholar
- Lieu TA, Black SB, Ray P, Chellino M, Shinefield HR, Adler NE: Risk factors for delayed immunization among children in an HMO. Am J Public Health. 1994, 84: 1621-1625.View ArticlePubMedPubMed CentralGoogle Scholar
- Dittmann S: Vaccine safety: risk communication-a global perspective. Vaccine. 2001, 19: 2446-2456. 10.1016/S0264-410X(00)00470-9.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2458/5/59/prepub