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71―5233（ 53 ）〈Original Article〉

Age-specific incidence of aseptic meningitis following
mumps vaccination from 2013–2016: estimation
based on the number of reported adverse reactions toimmunization in Japan
Hideaki Kumihashi1,*, Munehide Kano1,* and Satoko Ohfuji2
1

Global Vaccine Business Unit, Takeda Pharmaceutical Company Limited,
2–1–1 Nihonbashi-Honcho, Chuo-ku, Tokyo 103–8668, Japan2
Department of Public Health, Osaka City University Faculty of Medicine,
1–4–3 Asahimachi, Abeno-ku, Osaka 545–8585, Japan(Received for publication September 26, 2018)

First-dose mumps vaccination at a younger age may be associated with a lower
risk of vaccine-associated aseptic meningitis. However, to date, there are no
estimates of the age-speciﬁc incidence of aseptic meningitis caused by the Torii
strain-derived mumps vaccine. We investigated post-vaccination aseptic meningitis
incidence in Japan using case data from the Ministry of Health, Labour and Welfare
regarding adverse reactions following the Torii strain-derived mumps vaccine. The
number of age-speciﬁc vaccine administrations was estimated from an Internet
survey dataset and the number of vaccine shipments. Using these numbers, weestimated the age-speciﬁc post-vaccination aseptic meningitis incidence. Between
April 1, 2013, and April 30, 2016, the incidence among ﬁrst-dose vaccinations was
3.5 cases and the incidence among 1-year-old recipients was 1.3 cases (per 100,000
doses). Compared with the incidence at 1 year, signiﬁcantly higher rates wereobserved at ages 2–6, 7–12, and ≥13 years. Our results suggest that vaccination with
the Torii strain-derived mumps vaccine at age 1 carries a lower risk of aseptic
meningitis compared with administration of this vaccine at older ages.

Introduction
Mumps, also known as epidemic parotitis, is a systemic infection caused by the mumps
virus, which is a single-stranded, negative-sense RNA virus belonging to the Rubulavirus genus*Corresponding author: Tel: ＋81–3–3278–3624, Fax: ＋81–3–3278–2502, E-mail: munehide.kano@takeda.com

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Oct. 2018of the Paramyxovirus family. The prognosis is generally good, but some cases complicate meningitis (frequency, ＜1–17%), encephalitis (frequency, ＜1–2%), mumps deafness (frequency,＜1–7%)1). The incidence of mumps infection is estimated to have been 1.356 million in the peakyear (2005) and 0.431 million in the bottom year (2007)2). As mumps can be prevented by vaccination, routine immunization is performed in the majority of developed countries, which has resulted in fewer mumps epidemics in recent years3).
The measles, mumps, and rubella (MMR) vaccine was introduced in Japan as a routine immunization in April 1989. However, aseptic meningitis following vaccination became a problem
with social implications, leading to the discontinuation of MMR vaccination in April 1993. The
incidence (0.05%)4) was higher compared with the incidence (≤0.001%) of aseptic meningitis
following the Jeryl-Lynn strain-derived vaccine, which is used in many countries5). Three typesof mumps vaccines (Hoshino, Miyahara, and Torii strain) were used as voluntary vaccination
thereafter, but the incidences of aseptic meningitis were 0.04%, 0.03%, and 0.06%, respectively6).
Although these incidences seemed to be substantially lower than the incidence following naturalinfection with mumps virus (1.24%)6), mumps vaccination remains voluntary. Two types ofmumps vaccine (Hoshino and Torii strain) are currently available, and the vaccination rate is30%–40%, which has resulted in periodic epidemics every four or ﬁve years including the latest
outbreak in 2015–20167).
The immunization schedule for mumps vaccine in Japan differs from that in other countries.
Based on the package insert, the target age for vaccination is 1 year or older and the number ofvaccinations is basically one, although some pediatricians give the second dose to preschool children. A recent study suggested that receiving the ﬁrst mumps vaccine dose at a younger age reduces the risk of vaccine-associated aseptic meningitis8). However, age-speciﬁc aseptic meningitis incidence caused by the Torii strain-derived mumps vaccine has not been estimated.
Here, we investigated age-speciﬁc incidence of post-vaccinal aseptic meningitis with Torii
strain-derived mumps vaccine, which is produced by Takeda Pharmaceutical Company Limited.
We used data on post-vaccination aseptic meningitis cases from The Adverse Reaction Review
Committee, which is part of the Health Science Council in the Ministry of Health, Labour andWelfare (hereafter referred to as the Committee on Adverse Reactions)9〜15). The number of agespeciﬁc vaccinations was estimated from an Internet survey dataset and the number of vaccine
shipments.

Materials and Methods
Number of aseptic meningitis cases by age following vaccination with the Torii strain
The number of post-vaccination aseptic meningitis cases by age was based on reports submitted to the Committee on Adverse Reactions concerning adverse reactions to the Torii strain-Oct. 2018

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71―5235（ 55 ）derived mumps vaccine. This study reviewed data collected over 37 months from April 1, 2013,
when the ﬁrst meeting of the Committee on Adverse Reactions was held, to April 30, 2016. During this period, the safety of the mumps vaccine was evaluated at the third (September, 2013)9),
eighth (February, 2014)10), eleventh (October, 2014)11), thirteenth (January, 2015)12), sixteenth(November, 2015)13), eighteenth (April, 2016)14), and twentieth (July, 2016)15) meetings of theCommittee on Adverse Reactions. Using the data on adverse reactions reported at these sevenmeetings, cases with any of the following adverse reaction terms were analyzed in this study:“aseptic meningitis,” “mumps meningitis,” “viral meningitis,” and “meningitis.” Information
about the age of the subjects and the vaccine manufacturer in these cases was also collected.
Number of Torii strain-derived vaccine doses administered by age
The number of Torii strain-derived vaccine doses administered by age was estimated by multiplying the number of vaccine shipments by the age fraction of vaccine recipients. The numberof vaccine shipments was regarded as the shipping quantity over the 37 months from April 1,
2013, to April 30, 2016, as reported by Takeda Pharmaceutical Company Limited to the Committee on Adverse Reactions. Because the mumps vaccine is purchased as needed, the number ofdoses that is likely to be discarded as unused in medical institutions is expected to be very low.
Therefore, in this study, we assumed that all products shipped during the study period were administered.
To collect information on the age fraction of mumps vaccine recipients, an online survey wasadministered to pediatricians by Macromill Carenet, Inc., a contractor of Takeda Pharmaceutical
Company Limited, from July 6–12, 2016. A request for participation in the survey was made to
5,350 pediatricians who were registered in a respondent panel of Macromill Carenet, Inc. The
group of contacted pediatricians was selected in a manner aimed at ensuring that there was nobias in prefectures or in regions with local government vaccination funding (categorized by entire
funding, partial funding, or no funding), with a target sample size of 50 responders each from regions with entire funding, partial funding, and no funding.
In this Internet survey, the surveyed pediatricians were asked to provide the following information: age and afﬁliation (clinic or other) of the pediatrician; public funding (entire funding,partial funding, or no funding) for mumps vaccination in the region where the pediatricianʼs facility is located; and the number of mumps vaccine doses administered (by age and by the ﬁrst or
second dose) in the past 3 months. This information was used to calculate the age fractions ofvaccine recipients at the facilities where each pediatrician worked. When estimating the age fraction of vaccine recipients in Japan, we considered the possibility that the age distribution might
differ depending on local public funding, so we also calculated the weighted-average of the age
fraction with respect to local public funding. This integrated information about the funding ofchildhood vaccination in Japan (as of May 27, 2016)16) was provided by the incorporated non-236（ 56 ）THE JAPANESE JOURNAL OF ANTIBIOTICS

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proﬁt organization “KNOW-VPD! Protect our Children”. For example, the vaccination fraction at
1 year of age in Japan was calculated as: vaccination fraction at 1 year of age according to pediatrician responses from the regions with entire funding×proportion of local governments that entirely fund vaccination in Japan (9.8%)＋vaccination fraction at 1 year of age according to pediatrician responses from the regions with partial funding×proportion of local governments thatpartially fund vaccination in Japan (24.4%)＋vaccination fraction at 1 year of age according topediatrician responses from the regions with no funding×proportion of local governments that
do not fund vaccination in Japan (65.8%). A similar formula was used to estimate the vaccination
fraction in each age group.
Age-speciﬁc incidence of post-vaccination aseptic meningitis
To calculate the age-speciﬁc incidence of post-vaccination aseptic meningitis (per 100,000
doses), the number of aseptic meningitis cases by age was divided by the number of doses administered by age and then multiplied by 100,000. Differences in the incidence of aseptic meningitis
by age were tested for signiﬁcance using a Fisherʼs exact test. A two-sided signiﬁcance level of
0.05 was used. All statistical analyses were performed using SAS version 9.3 software (SAS Institute Inc., Cary, NC, USA).

Results
Number of aseptic meningitis cases following vaccination with the Torii strain
During the period from April 1, 2013, to April 30, 2016, 46 cases of aseptic meningitis after
vaccination with the Torii strain were reported. Of these, 44 cases were included in this study
after excluding the following two cases: one case that reported vaccination with another manufacturerʼs vaccine and one case that was the result of double reporting. The number of cases by age
was 11 at age 1, 12 at age 2–6, 8 at age 7–12, 10 at ≥13 years of age, and 3 at an unknown age.
The number of days from vaccination to onset was 3 to 34 days.
Number of Torii strain-derived vaccine doses administered by age
During the period from April 1, 2013, to April 30, 2016, the total number of Torii strainderived vaccine shipments was 1,697,529. The results of the Internet survey conducted to investigate the age fraction of vaccine recipients are shown in Tables 1 and 2. The age distribution ofsurvey participants did not differ from that of pediatricians working at medical facilities according to the “Current State of Physicians, Dentists and Pharmacists in 2014”17) (p＝0.54, Chisquared test; Table 1). Additionally, no signiﬁcant differences were observed in the proportions of
afﬁliated medical institutions (Clinic versus Others) between participating pediatricians and overall pediatricians (p＝0.07, Chi-squared test). There were similar numbers of pediatricians from

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237（ 57 ）Table 1. Characteristics of the physicians who participated in the Internet survey

each region, which indicates that regions with different levels of public funding were equally represented (Table 1).
At the facilities where the survey participants worked, the ﬁrst dose of the mumps vaccine
was administered to 3,465 individuals, of whom 68.9% were age 1 (Table 2). The number of vaccine recipients tended to decrease with increasing age. The second dose was administered to
1,146 individuals, which is 33.1% of the number of ﬁrst-dose administrations. The age distribution of vaccine recipients was investigated according to the public funding status in the region
where the survey participants worked (Table 2). In regions with entire funding, the fraction of
vaccine recipients at age 1 was as low as 37.2%, compared with 64.5% in regions with partial
funding and 56.2% in regions with no funding, suggesting that the age distribution of vaccine recipients differs signiﬁcantly depending on local public funding (p ＜ 0.05). Considering the proportion of public funding for mumps vaccination in each region of Japan, the age fraction ofmumps vaccine recipients in Japan was estimated to be 56.4%, 39.7%, 3.3%, and 0.8% at 1, 2–6,
7–12, and ≥13 year(s) of age, respectively (Table 2, overall, weighted-average of age fraction).
Based on these weighted-average of age fractions, the number of Torii strain-derived vaccine
doses administered in Japan by age was estimated to be 957,406 at age 1, 673,919 at age2–6,
56,018 at age 7–12, and 13,580 at ≥13 years of age.

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Table 2. Age distribution of vaccine recipients by dose and public funding

Age-speciﬁc incidence of aseptic meningitis following vaccination with the Torii strain
The incidence of post-vaccination aseptic meningitis after the ﬁrst dose in all age groups
combined was calculated by dividing the number of aseptic meningitis cases during the study pe-Oct. 2018

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239（ 59 ）Table 3. Age-speciﬁc incidence of aseptic meningitis following vaccination with the Torii strain

riod (44 cases) by the estimated number of vaccine shipments as the ﬁrst dose, yielding 3.5 per
100,000 doses (Table 3).
The age-speciﬁc incidence (per 100,000 doses) from the number of administered ﬁrst doses
was estimated to be 1.3, 3.3, 27.3, and 131 at 1, 2–6, 7–12, and ≥13 years of age, respectively.
Compared with the estimated incidence at age 1, signiﬁcantly higher incidences by Fischerʼsexact test were observed at 2–6, 7–12, and ≥13 years of age (Table 3 and Fig. 1).
If post-vaccination aseptic meningitis is assumed to have occurred after the second dose as
well as after the ﬁrst, the post-vaccination aseptic meningitis incidence for all age groups would
be 2.6 per 100,000 doses, based on the number of ﬁrst doses (Table 3). When this incidence (per100,000 doses) from the total number of administered doses is broken down by age, the rates are
1.2, 1.8, 14.3, and 73.6 at 1, 2–6, 7–12, and ≥13 years, respectively. Compared with the estimatedincidence at age 1, signiﬁcantly higher incidences by Fischerʼs exact test were observed at 7–12,
and ≥13 years of age (Table 3 and Fig. 2).

Discussion
Based on reports that the incidence of adverse reactions following MMR vaccination was
lower among children receiving the second doses than among those receiving the ﬁrst dose18), andconsidering that complications from subsequent viral infection were reported to be less likely240（ 60 ）THE JAPANESE JOURNAL OF ANTIBIOTICS

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Fig. 1. Aseptic meningitis incidence estimated from the number of administered ﬁrst doses

The number of aseptic meningitis cases per 100,000 doses for each age group is shown, as calculated from the number ofadministered ﬁrst doses. The data of ≥13 years of age was excluded in the ﬁgure due to the limited dose number administered tothe age. The exact value for each group is listed in parentheses above the corresponding bar.
*P＜0.05

Fig. 2. Aseptic meningitis incidence estimated from the total number of administered doses

The number of aseptic meningitis cases per 100,000 doses for each age group is shown, as estimated from the combined numberof ﬁrst and second doses. The data of ≥13 years of age was excluded in the ﬁgure due to the limited dose number administered
to the age. The exact value for each group is listed in parentheses above the corresponding bar.
*P＜0.05

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241（ 61 ）after previous infection with or vaccination for mumps19), aseptic meningitis incidence is assumed to have occurred following the ﬁrst dose and, thus, was estimated from the number of administered ﬁrst doses. This resulted in an incidence estimate for age 1 (1.3 per 100,000 doses)that was signiﬁcantly lower than the incidences at ages 2–6, 7–12, and ≥13 years.
If mumps vaccination at age 1 were to be incorporated into the routine immunization program
and the vaccination coverage reached to that of measles-rubella vaccination (MR vaccination)(96.2%)20), which is currently a routine immunization, we estimate that post-vaccination aseptic
meningitis might occur in 13 per million children who are vaccinated at age 1. Notably, this incidence is approximately 1,000–4,000 times lower than that of aseptic meningitis following naturalinfection with mumps virus (1,6). However, if the mumps vaccination were recommended to older
children, many more aseptic meningitis cases would be expected. Therefore, mumps vaccination
should be incorporated into the routine immunization program and the administration of mumps
vaccine at age 1 should be promoted to reduce the risk of post-vaccination aseptic meningitis.
The age dependence of aseptic meningitis following mumps vaccination observed in thepresent study is consistent with the results from a prospective cohort study by Muta et al.8). Theirstudy in Japan of 21,465 recipients of a domestically produced vaccine (Torii, Hoshino, or Miyahara strain) reported that the incidence of aseptic meningitis was 17.8 per 100,000 vaccine recipients who were ＜3 years of age and 78.1 per 100,000 vaccine recipients who were ≥3 years ofage, with a signiﬁcant difference observed between the two age groups (p＝0.04)8). However, thatstudy found that the overall incidence of aseptic meningitis following vaccination with a domestic Japanese strain was as high as 46.5 per 100,000 vaccine recipients8), which is more than 10times higher than that calculated in our study (2.6–3.5 per 100,000 doses). This difference may be
attributed to the different survey methods used by these studies; our study included nationwide
information, but the case detection was based on passive surveillance, while their prospective cohort study involved only limited medical institutions, but the case detection was based on active
surveillance. In addition, the calculation of vaccine administration by the number of vaccine shipments may contribute to these differences.
Our study has some limitations. First, the age fraction of vaccine recipients was estimatedbased on information from an Internet survey. Although such a survey is easy to conduct and canbe completed quickly, it may include selection bias caused by the computer literacy of solicited
participants as well as information bias from the risk of fraud, such as the provision of false answers or replies by someone other than the intended participant. In addition, since the Internet
survey targeted pediatricians, the estimated number of vaccine recipients ≥ 13 years of age might
be obscure, which might bring about the higher incidence of this age group than the actual rate,
because most of medical attendance after 15 years of age in Japan is managed by physicians ininternal medicine and vaccination for preventing hospital infection including educational facilities are also excluded in the survey. Second, since we could not distinguish whether the reported

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aseptic meningitis occurred after the ﬁrst dose or the second dose, precise dose-based risk assessment is not possible. Third, the term of incidence may be inappropriate in this study, since it wascalculated with the numerator being spontaneously reported cases (including cases for which virological diagnosis may not have been made) and as the denominator the quantity of vaccines
shipped, which was assumed to be the number of vaccine recipients. Forth, the coverage of local
public funding was 37% (644/1,718) of whole local governments16). This low coverage of local
funding might be a reason of the difﬁculty to show the relationship between the local funding andthe vaccination age. However, some misclassiﬁcation, if any, would be non-differential, and thus
does not materially affect the validity of the study results.
The Jeryl Lynn strain-derived vaccine and its derivative, the RIT-4385 strain-derived vaccine, are considered to be quite safe1). Besides, the mumps virus is classiﬁed into 12 genotypes
from A to N, which are known to serologically differ from one another21). The Jeryl Lynn and
RIT-4385 strains belong to genotype A, the Japanese domestic strains including the Torii strain
belong to genotype B, and the Japanese domestic epidemic strains belong to genotype G22). Previous reports indicate that while human serum antibodies induced by genotype B vaccines neutralize genotype G viruses as potently as genotype B viruses, hyperimmune rabbit serum antibodies
induced by genotype A vaccines have slightly less potent neutralization activity against genotype
G viruses23). Therefore, it may be important to retain mumps vaccines other than the Jeryl Lynn
strain as options in anticipation of future mutations in the epidemic strains. Keeping in mind thatcomplications of natural mumps infection still occur in Japan and that developing a mumps vaccine with further enhanced safety and efﬁcacy may have its own set of challenges, it is importantto actively recommend the currently available mumps vaccines as the immediate available measure to maximize a reduction in the disease burden.
Our results suggest that vaccination with the Torii strain-derived mumps vaccine at age 1 has
a lower risk of aseptic meningitis compared with administration of this vaccine at higher ages.
Although there were some limitations in the present study, together with the fact that the highest
prevalence of mumps occurs at age 2–5, this ﬁnding suggests that the incorporation of the mumps
vaccine into the routine immunization program of children would ideally target children at age 1.
Acknowledgment
We would like to thank the incorporated non-proﬁt organization KNOW-VPD! Protect ourChildren for providing information about the public funding of mumps vaccination in Japan.
Conﬂict of Interest
Hideaki Kumihashi and Munehide Kano are employees of Takeda Pharmaceutical Company
Limited.

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71―5243（ 63 ）References
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