Abstract
Background
Although an effective vaccine has been available, measles still causes mast morbidity and mortality world widely. In Korea, a small number of measles cases have been reported through exposure to imported cases among young people with vaccine-induced measles immunity. Recently due to international migration including marriage, marriage migrants were the second-largest group of foreign population in Korea. Our study was carried out to obtain positive rate of measles antibody among married immigrant women from 12 countries in 10 Gun-Counties and 6 Cities, Korea.
Materials and Methods
A total of 547 blood samples were collected from maternal multicultural members from 12 countries. The measles-specific IgG antibody was measured by ELISA (Enzyme-linked immunosorbent assay; Enzygnost® Anti-measles virus/IgG, Siemens Healthcare Diagnostics Products GmbH, Marburg, Germany). We performed a simple logistic regression to test whether the measles antibody seroprevalence differed by participant age, location, or country of birth and then calculated the likelihood ratio statistics to determine whether measles antibody seroprevalence differed by country of birth.
Results
Overall positive measles seroprevalence was 75.3% (95% confidence interval: 71.7 – 78.9). Participants aged 20 - 24 years, 25 - 29 years, and 30 - 63 years has respective seropositivities of 52.5%, 55.3%, and 82.7%. In this study, the geometric mean titers of participants aged 21 - 29 years were slightly lower than those of participants aged over 30 years, which were 1,372 mIU/ml and 2,261 mIU/ml, respectively (average of total participants: 2,027 mIU/ml).
Conclusion
The study provides detailed information about seroimmunity of the married immigrant population in Korea, which is important for measles elimination. Since the 1980s, most vaccine-preventable diseases including measles have been well-controlled. Nevertheless, sporadic measles outbreaks are still reported. Thus, special attention should be paid to the possible importation of infectious diseases such as measles by immigration.
Keywords: Measles, IgG antibody, multicultural women, Korea
Graphical Abstract
INTRODUCTION
Measles is a potentially infectious and vaccine-preventable disease for which humans are the only reservoir. Routine measles vaccination of children and mass vaccination campaigns are key public health strategies to reduce measles incidence. To ensure adequate population immunity and prevent outbreaks, the World Health Organization (WHO) recommends all children receive at least 2 doses of measles-containing vaccine (MCV) [1]. Sensitive and specific diagnostic tools are available, and the Korea has introduced a mandatory vaccination keep-up program requiring all first-grade elementary school children to present certification of having received a second dose of the measles-containing vaccine [2,3,4,5]. After a massive measles epidemic from 2000 to 2001, a large-scale measles catch-up vaccination was conducted on 5,860,000 children aged 8 - 16 years [6,7]. As a result of the national effort to eliminate measles in Korea, the two-dose measles, mumps, and rubella (MMR) vaccination maintained over 95.0% coverage since 1996, and the reported number of measles cases decreased to 0.93 cases per million people from 2008 to 2013 [1]. A randomized survey in 2010 showed an increase in vaccination coverage of 98.2% for MCV1 and of 66.1% for MCV2 [8]. As a result, Korea was declared the first measles-free nation in 2006 and was again verified to be measles-free in 2014 by the WHO. The WHO reported that establishing a keep-up vaccination program in school settings was one of the most effective measles elimination efforts [9]. Although measles has been effectively eliminated in Korea, import-related resurgence outbreaks have occurred [10]. Until recently, few measles cases were reported annually [11]. Vaccination is a key intervention for interrupting measles transmission and circulation; however, eradication per se of established measles has been limited.
The measles virus is a member of the genus Morbillivirus, the family Paramyxoviridae and the superfamily Orthoparamyxovirinae, which includes parainfluenza virus serotypes 1 - 4, mumps, respiratory syncytial virus, and metapneumovirus [12]. The measles virus is one of the most highly contagious infectious diseases among unvaccinated individuals and is transmitted through direct contact with aerosolized droplets or other respiratory secretions from infected individuals. Measles has an incubation period of approximately 8 to 12 days, which is followed by a prodromal phase of high fever, cough, coryza, conjunctivitis, and malaise. Kolpik spots may also be apparent on the buccal mucosa and can last for 12 to 72 hours [13]. Following this phase, a maculopapular erythematous rash develops behind the ears and on the forehead, later spreading centrifugally to involve the trunk and extremities.
The population of multicultural families in Korea (here defined as consisting of a married immigrant or foreigner with Korean citizenship) has been rapidly growing since the mid-1990s [14]. While international migration has become a global phenomenon in recent decades, Korea has experienced this phenomenon relatively recently. Among the registered foreign population in 2018, 6.7% (159,206 out of 2,367,607) were marriage migrants, which was the second-largest group following nonprofessional migrant workers [15]. About 83% (132,391 out of 159,206) of international marriages occurred between a Korean groom and foreign bride, most of whom originated from East and Southeast Asian countries [16].
The purpose of this study was to evaluate seroimmunity against measles in married immigrant women in Korea. This study focused only on married immigrant women of Korean provinces including 10 Gun-counties and 6 Cities from 12 countries, and measles serologic patterns are considered to be age-dependent. However, our results may be generalized to apply to all immigrants or foreign Korean citizens who are threatened with the alarming international upswing in measles cases. This study provides detailed information on the seroimmunity of the married immigrant and foreign Korean citizen population, which is important for measles elimination in Korea where made the declaration of measles elimination by complying with all standards presented by the WHO in 2006.
MATERIALS AND METHODS
1. Blood collection
In this study, the participant population consisted of women who attended local multicultural centers and local public health authorities with extensive cooperation in the 10 Gun-counties of Damyang, Gangjin, Hwasun, Bosung, Hampyeong, Gosung, Yangyang, Haenam, Shinan and Yeoncheon, and the 6 cities of Mokpo, Gwangyang, Donghae, Taeback, Mungyeong and Yangju. In conjunction with the multicultural centers in each province and county, we performed enzyme activity measurement and blood tests to investigate measles seroimmunity among maternal multicultural members from 12 countries (Philippines, Vietnam, Cambodia, China, Japan, Russia, Kazakhstan, Uzbekistan, Thailand, Indonesia, Laos, and Myanmar). All participants completed a questionnaire that focused on demographic characteristic analysis and previous medical history. The average age of the 547 participating subjects was 35.4 years (range, 21 - 63). After receiving informed consent, blood samples were obtained from venous puncture (3 ml in K2-EDTA vacutainer tubes). A total of 547 blood samples were collected from October 26 through December 8, 2020. All of the interviewers, healthcare workers, and team members completed briefing sessions on the sampling methods and interview techniques used during this study.
2. Ethics statement
All study procedures concerning human sample collection, laboratory investigation, interviews, and questionnaires were reviewed and approved by the Institutional Review Board of Inha University (Approval No. 2020-04-004), and the study was conducted according to the principles of the 1975 Helsinki Declaration (revised in 2013). Before enrollment into the study, participants were informed of the study’s objectives and procedures. Written informed consent was obtained from all study participants, who were informed of their right to refuse to participate and/or to withdraw from the study at any time.
3. Laboratory procedures
Detection of the measles-specific IgG antibody was performed at the Jeollanam-do Province Institute of Health and Environment (JIHE) using an enzyme-linked immunosorbent assay (ELISA; Enzygnost® Anti-measles virus/IgG, Siemens Healthcare Diagnostics Products GmbH, Marburg, Germany) according to the manufacturer’s recommended standard operating procedures. Serum was separated from the blood samples within an hour of collection, and specimens were kept at -80\\xcb\\x9aC prior to testing. On completing the assay, we calculated the difference in absorbance (ΔA) between the antigen-positive and control antigen samples for each specimen and the positive/negative references. Quantitative evaluation of the test was performed by using the a-method and multiplying by a correction factor. Consistent with other seroprevalence studies [17,18,19], we considered specimens with corrected optical density (OD) values of >0.2 to be positive, specimens with OD values of 0.1 - 0.2 to be equivocal, and specimens with OD values of <0.1 to be negative. Specimens yielding equivocal results were retested in duplicate classified as equivocal if the same result was confirmed.
4. Statistical analysis
We used a simple logistic regression to test whether the measles antibody seroprevalence differed by participant age, location, or country of birth. We then calculated the likelihood ratio statistic to determine whether measles antibody seroprevalence differed by country of birth. Descriptive statistics, including percentages and mean values, were used to visualize the data, and were augmented with graphs made in Microsoft Excel® (Microsoft, Redmond, WA, USA).
RESULTS
We tested 547 available specimens from internationally married immigrant women in multicultural families, which were from 12 countries, were average 35.4 years in age (range, 21 - 63), and were habituating in 10 Gun-counties and 6 Cities of Korea. The prevalence of measles antibodies by age group is shown in Table 1. The overall seropositivity of measles in the study population was 75.3% (95% confidence interval [CI]: 71.7 - 78.9) and 9.5% (95% CI: 7.0 - 12.0) were equivocal. The overall measles seroprevalence, including both positive and equivocal samples, was 84.8%. Measles antibody seroprevalence increased with increasing age group, with a positive seroprevalence of 52.5% for ages 20 - 24; 55.3% for ages 25 - 29; and 75.8 - 95.7% for ages 30 and older (P <0.01) (Table 1). In other hand, the equivocal cases deceased with increasing age group (15.0% for ages 20 - 24, n = 40; 14.6% for age 25 - 26, n = 103, 3.2 - 10.7% for ages 30 and older, n = 404). We used a simple logistic regression to test whether the measles antibody seroprevalence increased with age. The regression coefficient associated with age was 0.09; (95% CI: 0.06 – 0.12), indicating that the measles antibody seroprevalence was strongly associated with age. A similar measles seroprevalence study conducted at the Korea Centers for Disease Control and Prevention (KDCA) found that in 2014, individuals aged 20 – 50 years had an overall measles seropositivity of 85.6% (9.4% equivocal; 95.0% combined positive and equivocal) [20]. The seropositivities of individual age groups were 69.6% for ages 20 - 24 (19.2% equivocal); 90.8% for ages 25 - 29 (7.2% equivocal); and 91.1% for ages 30 - 50 (5.5% equivocal). In our study, participants aged 20 - 29 years had a lower geometric mean titer than did those aged 30 years and over (1,372 mIU/ml vs. 2,261 mIU/ml, average of total participants: 2027 mIU/ml, Fig. 1). Although there was a relatively small number of participants over age 40 (n = 116), the general trend was that the anti-measles antibody geometric mean titers were higher in the 30s (n = 288), 40s, and 50s (n = 41) than in the 20s (n = 143) (Fig. 1 and 2). The geometric mean titers were 1,373 mIU/ml for the 20s, 2,110 mIU/ml for the 30s, 2,467 mIU/ml for the 40s, and 2,703 mIU/ml for participants over age 50. This trend may relate to the length of the settlement period after marriage in participants from foreign countries. During the study, seroprevalence did not differ by habitation location (Table 2). The positive seroprevalence was lowest in Yeoncheon Gun-county (37.9%) and highest in Hampyeong Gun-county (88.6%). The positive seroprevalences were 76.7% in rural habitation and 71.0% in urban habitation (Table 2). Similarly, 9.4% in the rural and 9.9% in the urban were equivocal. We used a simple logistic regression to test whether measles antibody seroprevalence differed by rural vs. urban location (“urban” was coded as 1). The associated regression coefficient was -0.296 (95% CI: -0.731 - 0.152; P = 0.189). Therefore, we did not find substantial evidence that measles antibody seroprevalence differs by the location of habitation (Table 2). In addition, we used a simple logistic regression to test whether measles antibody seroprevalence differed by country of birth. Immigrant women from 12 countries participated in the study. We determined a likelihood ratio statistic of 4.834 (df [degrees of freedom of the test] = 5; P = 0.436; Table 3), indicating that the measles antibody seroprevalence did not differ significantly by the country of birth.
Table 1. Sample size and measles seroprevalence among immigrant women by age group.
| Age group | Total No. (n = 547) | No. of positive (%) | 95% CI | No. of equivocal (%) | 95% CI | No. of negative (%) | 95% CI | P-Value |
|---|---|---|---|---|---|---|---|---|
| 20 - 24 | 40 | 21 (52.5) | (37.0, 68.0) | 6 (15.0) | (3.9, 26.1) | 13 (32.5) | (18.0, 47.0) | P <0.01 |
| 25 - 29 | 103 | 57 (55.3) | (45.7, 64.9) | 15 (14.6) | (7.8, 21.4) | 31 (30.1) | (21.2, 39.0) | |
| 30 - 34 | 149 | 113 (75.8) | (69.0, 82.7) | 16 (10.7) | (5.8, 15.7) | 20 (13.4) | (7.9, 18.9) | |
| 35 - 39 | 139 | 120 (86.3) | (80.6, 92.0) | 10 (7.2) | (2.9, 11.5) | 10 (7.2) | (2.9, 11.5) | |
| 40 - 44 | 44 | 37 (78.7) | (73.3, 94.9) | 2 (4.5) | (0.0, 10.7) | 5 (11.4) | (2.0, 20.7) | |
| 45 - 49 | 31 | 27 (87.1) | (75.3, 98.9) | 1 (3.2) | (0.0, 9.4) | 2 (6.5) | (0.0, 15.1) | |
| 50 - 54 | 23 | 22 (95.7) | (87.3, 100.0) | 1 (4.3) | (0.0, 12.7) | 0 (0.0) | (0.0, 0.0) | |
| >50 | 18 | 15 (83.3) | (66.1, 100.0) | 1 (5.6) | (0.0, 16.1) | 2 (11.1) | (0.0, 25.6) | |
| Total | 547 | 412 (75.3) | (71.7, 78.9) | 52 (9.5) | (7.0, 12.0) | 83 (15.2) | (12.2, 18.2) |
CI, confidence interval.
Figure 1. Age-specific distribution of seroprevalence and geometric mean titer (red lines) of measles IgG antibodies of married immigrant women in 10 Gun-counties and 6 Cities, Korea in 2020. Blue boxes represent the positive seroprevalence against measles and orange boxes does the equivocal.
Figure 2. Measles IgG titers and their mean values (red lines) of married immigrant women by age. The measles IgG titers were determined using an enzyme-linked immunosorbent assay (ELISA; Enzygnost® Anti-measles virus/IgG, Siemens Healthcare Diagnostics Products GmbH, Marburg, Germany) and calculated according to the manufacturer’s recommended standard operating procedures.
Table 2. Sample size and measles seroprevalence among immigrant women by location (City or County).
| Habitation | Total No. (n = 547) | No. of positive (%) | 95% CI | No. of equivocal (%) | 95% CI | No. of negative (%) | 95% CI | P-Value | |
|---|---|---|---|---|---|---|---|---|---|
| Damyang | 28 | 18 (64.3) | (46.5, 82.0) | 2 (7.1) | (0.0, 16.7) | 8 (28.6) | (11.8, 45.3) | P = 0.159 | |
| Mokpo | 20 | 14 (70.0) | (49.9, 90.1) | 4 (20.0) | (2.5, 37.5) | 2 (10.0) | (0.0, 23.1) | ||
| Ganjin | 102 | 85 (83.3) | (76.1, 90.6) | 7 (6.9) | (2.0, 11.8) | 10 (9.8) | (4.0, 15.6) | ||
| Hampyeong | 44 | 39 (88.6) | (79.3, 98.0) | 1 (2.3) | (0.0, 6.7) | 4 (9.1) | (0.6, 17.6) | ||
| Gwangyang | 5 | 3 (60.0) | (17.1, 100.0) | 0 (0.0) | (0.0, 0.0) | 2 (40.0) | (0.0, 82.9) | ||
| Goseong | 25 | 20 (80.0) | (64.3, 95.7) | 4 (16.0) | (1.6, 30.4) | 1 (4.0) | (0.0, 11.7) | ||
| Yangyang | 25 | 18 (72.0) | (54.4, 89.6) | 3 (12.0) | (0.0, 24.7) | 4 (16.0) | (1.6, 30.4) | ||
| Donghae | 33 | 22 (66.7) | (50.6, 82.8) | 5 (15.2) | (2.9, 27.4) | 6 (18.2) | (5.0, 31.3) | ||
| Haenam | 36 | 27 (75.0) | (60.9, 89.1) | 3 (8.3) | (0.0, 17.4) | 6 (16.7) | (4.5, 28.8) | ||
| Hwasun | 50 | 38 (76.0) | (64.2, 87.8) | 8 (16.0) | (5.8, 26.2) | 4 (8.0) | (0.5, 15.5) | ||
| Mungyeong | 48 | 33 (68.8) | (55.6, 81.9) | 4 (8.3) | (0.5, 16.2) | 11 (22.9) | (11.0, 34.8) | ||
| Boseong | 46 | 38 (82.6) | (71.7, 93.6) | 5 (10.9) | (1.9, 19.9) | 3 (6.5) | (0.0, 13.7) | ||
| Taebaek | 13 | 10 (76.9) | (54.0, 99.8) | 0 (0.0) | (0.0, 0.0) | 3 (23.1) | (0.2, 46.0) | ||
| Yangju | 12 | 11 (91.7) | (76.0, 100.0) | 0 (0.0) | (0.0, 0.0) | 1 (8.3) | (0.0, 24.0) | ||
| Shinan | 31 | 25 (80.6) | (66.7, 94.6) | 3 (9.7) | (0.0, 20.1) | 3 (9.7) | (0.0, 20.1) | ||
| Yeoncheon | 29 | 11 (37.9) | (20.3, 55.6) | 3 (10.3) | (0.0, 21.4) | 15 (51.7) | (33.5, 69.9) | ||
| Setting | P = 0.189 | ||||||||
| Rural | 416 | 319 (76.7) | (72.6, 80.7) | 39 (9.4) | (6.6, 12.2) | 58 (13.9) | (10.6, 17.3) | ||
| Urban | 131 | 93 (71.0) | (63.2, 78.8) | 13 (9.9) | (4.8, 15.0) | 25 (19.1) | (12.4, 25.8) | ||
| Total | 547 | 412 (75.3) | (71.7, 78.9) | 52 (9.5) | (7.0, 12.0) | 83 (15.2) | (12.2, 18.2) | ||
CI, confidence interval.
Table 3. Sample size and measles seroprevalence among immigrant women by country of birth.
| Country of birth | Total No. (n = 547) | No. of positive (%) | 95% CI | No. of equivocal (%) | 95% CI | No. of negative (%) | 95% CI | P-Value |
|---|---|---|---|---|---|---|---|---|
| Philippines | 99 | 76 (76.8) | (68.4, 85.1) | 9 (9.1) | (3.4, 14.8) | 14 (14.1) | (7.3, 21.0) | P = 0.44 |
| Vietnam | 306 | 230 (75.2) | (70.3, 80.0) | 29 (9.5) | (6.2, 12.8) | 47 (15.4) | (11.3, 19.4) | |
| Cambodia | 74 | 57 (77.0) | (67.4, 86.6) | 6 (8.1) | (1.9, 14.3) | 11 (14.9) | (6.8, 23.0) | |
| China | 20 | 12 (60.0) | (38.5, 81.5) | 3 (15.0) | (0.0, 30.6) | 5 (25.0) | (6.0, 44.0) | |
| Japan | 12 | 11 (91.7) | (76.0, 100.0) | 0 (0.0) | (0.0, 0.0) | 1 (8.3) | (0.0, 24.0) | |
| Other countriesa | 36 | 26 (72.2) | (57.6, 86.9) | 5 (13.9) | (2.6, 25.2) | 5 (13.9) | (2.6, 25.2) | |
| Total | 547 | 412 (75.3) | (71.7, 78.9) | 52 (9.5) | (7.0, 12.0) | 83 (15.2) | (12.2, 18.2) |
aOther countries include Russia (n = 4), Thailand (13), Uzbekistan (5), Indonesia (2), Laos (8), Myanmar (2) and Kazakhstan (2).
CI, confidence interval.
DISCUSSION
This study was designed for obtaining the positive rate of measles antibody among married immigrant women from 12 countries in 10 Gun-Counties and 6 Cities of Korea. In a multivariate analysis of participant age, location of habitation in Korea, and country of birth, we only identified a dependent association between seroprevalence and participant’s age, where age was significantly associated with low positive measles antibody prevalence values (Table 1). The location of habitation in Korea and birth country were not significantly associated with measles antibody prevalence (Table 2 and 3). Thus, differences in measles antibody seroprevalence among internationally married immigrant women may not be due to their different ethnic backgrounds. Measles epidemics are still observed in countries with low vaccination coverage [11,21,22]. Our study showed that susceptible age groups, especially those in their 20s, had observed measles seronegativity. As such, the potential accumulation of measles-susceptible people in the young population of internationally married immigrant women may pose increased risk for measles outbreaks following measles importation from other endemic countries. In particular, in a survey of 102 married immigrant women in Gangjin Gun-county, 12 women said they had been previously vaccinated, 29 said they had not been vaccinated, and 61 did not know their vaccination status. The positive measles antibody seroprevalence in Gangjin Gun-county was 83.3% (90.2% combined positive and equivocal; Table 2). Thus, the proportion of seronegative married immigrant women could be shifted and expanded to unvaccinated preschoolers in multicultural families, resulting in lower seropositivity and antibody levels. Multicultural families have a tendency to visit their home countries, and preschoolers are more likely to travel abroad with their parents. Indeed, Kang et al. reported that measles immunity in Korea was significantly lower in adolescents and young adults in their 20s [20]. As in other countries with high measles rates, small-scale epidemics have been repeated in Korea since 2013 due to the import of measles from other countries [20]. Similar expansion cases have been reported in other countries [10,23]. In 2005, the Regional Committee for the WHO Western Pacific Region (WPR, consisting of 37 countries and area including Philippines, Vietnam and Cambodia) established a goal for measles elimination by 2012 [24]. After a record low of 5.9 cases per million population in 2012, measles incidence increased during 2013 - 2016 to a high of 68.9 in 2014, because of outbreaks in the Philippines and Vietnam and then declined to 5.2 in 2017 [25]. In the case of measles immunization rate, the average values for Cambodia, Vietnam and Philippines during 1982 - 2021 were 65.0% [with a minimum of 27.0% (1984) and a maximum of 92.0% (2009)], 82.0% [1.0% (1982) - 99.0% (2016)], and 75.0% [9.0% (1982) - 92.0% (2004)], respectively [26].
Korean vaccination policies have been successful since the 1980s, and most vaccine-preventable diseases, including measles, have been well-controlled and declared to be eliminated [10]. Nevertheless, sporadic measles outbreaks are still reported [27]. These intermittent outbreaks are generally reported as foreign import cases [10]. Since the 1990s Korea, like other countries, has experienced active migration for marriage and employment. In this study, it demonstrated that measles seroprevalence of the young population of internationally married immigrant women, especially for the 20s, is statistically low, which is possibly due to the low vaccination rates. This situation of the young married women can be a critical trigger for a measles outbreak in Korea, where maintains measles elimination status. Thus, it needs to be considered to check the measles susceptibility and consider MMR vaccination at the time of immigration for immigrant persons from countries where MMR vaccination is not compulsory. Therefore, special attention should be paid to the possible importation of infectious diseases such as measles by migration.
Footnotes
Funding: This study was supported by funding from the National Research Fund (NRF) through the Global Resource Bank of Parasitic Protozoa Pathogens (TSK) and from the National Research Fund (NRF-2022R1F1A1066481) in the Republic of Korea (YYB). The funding source has been involved in the study design; in the sample collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
Conflict of Interest: No conflict of interest.
- Conceptualization: YYB, TSK.
- Formal analysis: EG, WL, MYS.
- Funding acquisition: YYB, TSK.
- Methodology: HCL, JYJ, EG, YK, YL.
- Project administration: TSK, YYB, SKL.
- Writing-original draft: YYB.
- Writing-review & editing: YYB, TSK, SKL.
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