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Hum. Reprod. Advance Access originally published online on September 30, 2005
Human Reproduction 2006 21(3):833-836; doi:10.1093/humrep/dei271
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© The Author 2005. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oupjournals.org

Age at menarche and its influencing factors in North Korean female refugees

Seung-Yup Ku1,2, Jong Won Kang3, Heon Kim3, Yong Dae Kim3, Byung Chul Jee1, Chang Suk Suh1,2, Young Min Choi1,2, Jung Gu Kim1, Shin Yong Moon1,2 and Seok Hyun Kim1,2,4

1 Department of Obstetrics and Gynaecology, Seoul National University College of Medicine, Seoul 110-744, 2 Institute of Reproductive Medicine and Population, Medical Research Centre, Seoul National University, Seoul 151-742, 3 Department of Preventive Medicine, Chungbuk National University, Chungbuk 361-763, Republic of Korea

4 To whom correspondence should be addressed. E-mail: seokhyun{at}plaza.snu.ac.kr


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
BACKGROUND: Age at menarche is known to be regulated by genetic and environmental factors. To date, no menarcheal data are available on North Korean women. In this cross-sectional survey, we investigated age at menarche and its possible influencing factors in North Korean refugees. METHODS: Four hundred and eleven North Korean refugees were surveyed at a North Korean female refugee camp using a structured questionnaire within 3 months of immigration. Menarcheal age was requested and the data obtained were analysed with respect to age at interview, region of residence in North Korea, education, food preference and sleep duration. RESULTS: Mean age at menarche was 16.0 ± 2.1 years (mean ± SD). Univariate analysis demonstrated a significant difference in the menarcheal age among the different food preference groups (P = 0.0236). Sleep duration was found to be significantly and negatively correlated with age at menarche (R = –0.23, P < 0.0001). However, generalized linear model (GLM) analysis revealed that region of residence at menarche (P = 0.0209) and sleep duration (P = 0.0007) were significant determinants. Food preference played a role as an effect modifier in the relationship between the region of residence at menarche and age at menarche. CONCLUSION: Age at menarche seemed to be delayed in North Korean refugees. GLM analysis showed that sleep duration and region of residence at menarche were significant influencing factors of age at menarche in this study population.

Key words: age at menarche/influencing factors/North Korean refugees


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
Menarche, the beginning of menstruation, has important implications not only in terms of the possibility of child-bearing, but also because age at first menses is related to several pathologic conditions such as breast cancer (Gilani and Kamal, 2004Go; ESHRE Capri Workshop Group, 2004Go), endometriosis (Missmer et al., 2004Go) and bone density response to calcium supplementation in later life (Chevalley et al., 2005Go). Moreover, convincing evidence indicates that menarche is regulated by a variety of environmental factors (Speroff and Fritz, 2005Go).

The Korean peninsula has been divided into two countries since the mid-1940s. North Korea has a unique environment, and thus North and South Korean women might be expected to experience menarche at different ages though they share the same genetic backgrounds. Volumes of menarcheal data and statistics are available on various ethnic groups, including South Korean women (Hwang et al., 2003Go). However, no published data are yet available on North Korean women.

Though the North Korean refugees cannot be viewed as wholly representative of the North Korean female population, we considered that an investigation of North Korean refugees should provide an indirect but quite a reflective measure. The authors performed the present study to determine age at menarche among North Korean female refugees and to identify influencing factors. Since all study subjects had experienced menarche whilst living in North Korea and had immigrated <3 months prior to the survey, their age at menarche is a solid variable independent of the psychophysical stress that they had experienced during their emigration. The age at menarche of this group of women may probably reflect the environmental conditions including lifestyles when they lived in North Korea.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Acknowledgements
 References
 
Design and samples
This cross-sectional survey was conducted at a North Korean refugee camp. Four hundred and eleven subjects were recruited. All had experienced menarche whilst living in North Korea and had immigrated <3 months prior to the survey. All participants provided informed consent. Research assistants met the subjects on a one-to-one basis and explained the purpose of this study. A structured questionnaire was used and data were collected by direct interview. Age at interview, parity, body weight and height, age at menarche, region of residence at menarche, education, food preferences, sleep duration, religion, current alcohol intake and age at menarche of mother and sisters were included in the questionnaire.

Statistical analyses
For each independent variable, differences in age at menarche were analysed for categorized subgroups. SAS for Windows (Version 8.02, SAS Institute Inc., Cary, NC, USA) was used for the statistical analysis. Age was categorized as ≤24 years, 25–29 years, 30–34 years and ≥35 years. Region of residence at menarche was dichotomized as ‘Hamkyungbuk-do’ or ‘Other provinces’, since ~70% of the study subjects were from Hamkyungbuk-do province. This province is the northernmost region of North Korea with the lowest temperature, most of the region being mountainous. Education was trichotomized as ‘elementary school or lower’, ‘middle or high school’ and ‘university or higher’. Food preference was also trichotomized as ‘meat, fish and dairy’, ‘rice and starch’, or ‘fruits and vegetables’, as was sleep duration as ≤5 h, 6–7 h and ≥8 h. Differences in the mean levels of continuous variables were analysed using the t-test and by one-way ANOVA (analysis of variance). Pearson correlation analysis was used to analyse continuous variables. Relevant variables were selected and subjected to generalized linear model analysis.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Acknowledgements
 References
 
Table I summarizes the general characteristics of the study population. The mean age of the study subjects was 31.3 ± 6.2 years (mean ± SD), and age at menarche was 16.0 ± 2.1 years. Mean subject height was 155.1 ± 4.8 cm, weight 52.0 ± 7.0 kg, and body mass index (BMI) 21.6 ± 2.6 kg/m2. Information on BMI at menarche was unavailable (Table I).


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  		Table I. General characteristics of North Korean refugees (n = 411)

 

The mean age at menarche decreased from 16.3 years for those aged ≥35 years to 15.9 years for those aged 30–34 years, and to 15.5 years for those aged 25–29 years (P = 0.0316), which corresponded to a –0.4 year/5-year reduction. However, contrary to any trend, the ≤24 year group showed delayed menarche versus the other groups (Table II).


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  		Table II. Distribution and results of ANOVA on age at menarche

 

The study subjects were from 11 different provinces in North Korea. Women from Hamkyunngbuk-do were far more numerous than those from other provinces. Univariate analysis showed no significant difference between these two groups in terms of menarcheal age. In addition, age at menarche was not found to be related to education level (Table II).

However, food preferences were associated with age at menarche differences. Women experienced their first menses at 15.9 ± 2.1 years in the ‘rice and starch’ group, 15.6 ± 2.0 years in the ‘meat and fish’ group, and 16.4 ± 2.2 years in the ‘fruits and vegetables’ group (P = 0.0236). Thus, individuals in the ‘meat and fish’ group experienced menarche at a lower age (Table II).

Sleep duration showed significant differences. Women experienced their first menses at 16.8 ± 2.3 years in the ≤5 h group, 16.0 ± 1.9 years in the 6–7 h group, and 15.3 ± 1.9 years in the ≥8 h group (P < 0.0001). Women with longer sleep duration showed an earlier menarche (Table II).

Pearson correlation analysis revealed that age at menarche was strongly positively correlated with that of sisters (R = 0.51, P <0.0001). A strong negative correlation was found between age at menarche and sleep duration (R = –0.23, P <0.0001).

Generalized linear model analysis identified region of residence at menarche and sleep duration as significant determinants of age at menarche and that age, food preference and education were not (Table III). Food preference played a role as an effect modifier in the relationship between region of residence at menarche and age at menarche. Although the ‘meat and fish’ (Hamkyungbuk-do 15.9 ± 2.2 years versus others 15.8 ± 1.7 years, P = 0.8270) and the ‘rice and starch’ (Hamkyungbuk-do 15.7 ± 2.0 years versus others 15.5 ± 1.9 years, P = 0.6930) subgroups showed no differences in age at menarche with respect to region of residence at menarche, the ‘fruits and vegetables’ subgroup showed a statistically significant difference (Hamkyungbuk-do 16.8 ± 2.1 years versus others 15.7 ± 2.1 years, P = 0.0116).


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  		Table III. Generalized linear model analyses of the effects of age, food preference, education, region of residence and sleep duration on age at menarche

 


   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Acknowledgements
 References
 
Our study is the first to report on age of menarche in North Korean women. The main purpose of the present study was to determine age of menarche and to identify the influencing factors. Although the study subjects could not be taken to represent North Korean women, we speculate that North Korean refugees in their 20s or 30s experience a late menarche.

Age at menarche of North Korea refugees (16.0 ± 2.1 years) as determined by this study differs from those reported in America (12.1 years in African-Americans and 12.7 years in Caucasians) (Speroff et al., 2005) and in South Korea (12.7 years) (Hwang et al., 2003Go), which may be attributed to differences in genetic and environmental factors. An analysis of the US Third National Health and Nutrition Examination Survey showed an ethnic difference in age at menarche (Wu et al., 2002Go). Environmental factors may probably have played an important role in making a difference in menarcheal age, especially in the case of Korean women who are of one race.

Mean menarcheal age in the study subjects decreased from 16.3 years (≥35 years) to 15.9 years (30–34 years), then to 15.5 years (25–29 years), corresponding to a decrease of –0.4 years per 5 years. This decreasing trend conforms to a well-known decline in menarcheal age over the past years (Speroff et al., 2005). However, ≤24 year group showed delayed menarche versus the other groups (Table II). One possible explanation for this delay is economic fluctuations and the accompanying insufficient nutritional status for the youngest groups. In the mid-1990s, repeated natural disasters such as heavy rains and drought struck the North Korean economy (Korea Institute for National Unification, 2004Go). Although there are little data available with respect to the economic indices of North Korea, the Asian Development Bank estimated the gross national income (GNI) per capita in 2001 to be low (≤$745) (Asian Development Bank, 2003Go).

BMI at menarche is related to age at menarche (Kaplowitz et al., 2001Go). However, such BMI data were not available since the study subjects could not remember their weights and heights when they had experienced menarche. We did not analyse the effect of current BMI on age at menarche since current BMI does not have a linear relationship with BMI at menarche.

Food preference was observed to significantly affect age at menarche (Table II, P = 0.0236). This may be just a phenomenal finding. Or, it may be explained by the fact that critical body weight must be reached by a girl to achieve menarche (Frisch and MacArthur, 1974Go) and that food preference may probably, in part, reflect habitus or weight.

Regarding the effect of region of residence, those from Hamkyungbuk-do comprised ~70% of our study subjects. No regional differences were found by univariate analysis between those from Hamkyungbuk-do and those from other regions (Table II). However, multivariate analysis showed that region of residence became a significant determinant of age at menarche after adjusting for age, food preference, education, and sleep duration (Table III). Hamkyungbuk-do is the northernmost region of North Korea and it is, therefore, possible that the low temperature and other climate differences may affect age at menarche. However, since no difference was found at the univariate analysis level, further larger scale studies are necessary.

Interestingly, in univariate analysis, there was no difference in the age at menarche between refugees from Hamkyungbuk-do and those from other provinces. However, in the generalized linear model analysis, region of residence at menarche appears as a significant determinant. In contrast, food preference in this generalized analysis does not appear as a determinant of the age at menarche, although there was a difference in age at menarche among the three food preference subgroups. Stratified analysis revealed that food preference played a role as an effect modifier in the relationship between the residence at menarche and age at menarche. Although those from the ‘meat and fish’ and the ‘rice and starch’ groups showed no differences in age at menarche with respect to region of residence at menarche, those from the ‘fruits and vegetables’ group showed a statistically significantly different age at menarche (P = 0.0116).

Social class is known to influence age at menarche (El Dosoky and Al Amoudi, 1997Go). However, it was difficult to classify the social factors in this survey, as the questionnaire used was deliberately constructed to avoid politically sensitive economical or social questions that might reveal information about the social standings of study subjects. The question ‘nearest’ the issue of socio-economic status concerned education level, but no differences were found between the three different education subgroups in terms of age at menarche (Table II).

The influence of genetic background on age at menarche was observed in this study as reported previously (Speroff et al., 2005). A Pearson correlation analysis revealed that age at menarche was strongly positively correlated with the ages of sisters at menarche (R = 0.51, P < 0.0001). However, this relationship was not observed between subjects and mothers, possibly due to the low number of subjects that responded to this question (n = 92).

One point worth noting is that the present study suggests that age at menarche is influenced by sleep duration, i.e. a strong negative correlation was observed between age at menarche and sleep duration (Tables II and III). If one presumes that sleep duration reflects a consistent lifestyle, then it may affect menarche as sleep is an important mediator of GnRH secretion, which has known stimulatory effects during puberty (Boyar et al., 1972Go).

This study has some potential limitations. First, its cross-sectional design is vulnerable to information bias due to recall inaccuracies. Secondly, our study subjects might not well represent the North Korean population as described previously. Thirdly, the information obtained may have been biased by the political sensitivities of our study subjects, i.e. it is possible that there was a differential bias. However, we believe that any information bias would probably be non-differential, since the study subjects had a relatively low level of education (Table II) and thus were unaware of the political implications or otherwise of age at menarche and/or of its influencing factors. In fact, the majority of the study subjects had emigrated for non-political reasons.

In conclusion, we report on age at menarche among a population of North Korean refugees and on its influencing factors. Region of residence, food preferences and sleep duration were found to influence menarche in our study subjects. Further investigations are needed to evaluate the effects of genetic factors such as estrogen receptor gene polymorphism on age at menarche.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
References
 
We wish to give our sincere thanks to Professor Sang Chul Park, Professor Sung Tae Hong and Professor Tae Gyun Park for their constructive comments on the manuscript. This study was supported by a grant (No.800-20030373) from the Seoul National University Research Fund for Unification Studies.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
Asian Development Bank (2003) GNI per capita 2001, Atlas method and PPP. http://www.adb.org/Statistics/icp/files/gni_pc.pdf

Boyar R, Finkelstein J, Roffwarg H, Kapen S, Weitzman E and Hellman L (1972) Synchronization of augmented luteinizing hormone secretion with sleep during puberty. N Engl J Med 287,582–586.[ISI][Medline]

Chevalley T, Rizzoli R, Hans D, Ferrari S and Bonjour JP (2005) Interaction between calcium intake and menarcheal age on bone mass gain: an eight-year follow-up study from pre-puberty to post-menarche. J Clin Endocrinol Metab 90,44–51.[Abstract/Free Full Text]

El Dosoky M and Al Amoudi M (1997) Menarcheal age of school girls in the city of Jeddah, Saudia Arabia. J Obstet Gynaecol 17,195–198.

ESHRE Capri Workshop Group (2004) Hormones and breast cancer. Hum Reprod Update 10,281–293.[Abstract/Free Full Text]

Frisch RE and McArthur JW (1974) Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185,949–951.[Abstract/Free Full Text]

Gilani GM and Kamal S (2004) Risk factors for breast cancer in Pakistani women aged less than 45 years. Ann Hum Biol 31,398–407.[CrossRef][ISI][Medline]

Hwang JY, Shin C, Frongillo EA, Shin KR and Jo I (2003) Secular trend in age at menarche for South Korean women born between 1920 and 1986: the Ansan Study. Ann Hum Biol 30,434–442.[CrossRef][ISI][Medline]

Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE and Herman-Giddens ME (2001) Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 108,347–353.[Abstract/Free Full Text]

Korea Institute for National Unification (2004) White Paper on Human Rights in North Korea 2004. Adwill, Seoul, Korea, pp.206–216.

Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Malspeis S, Willett WC and Hunter DJ (2004) Reproductive history and endometriosis among premenopausal women. Obstet Gynecol 104,965–974.[Abstract/Free Full Text]

Speroff L and Fritz MA (2005) Clinical gynaecologic endocrinology and infertility. 7th edn, Lippincott Willliams & Wilkins, Philadelphia, USA, pp.366–370.

Wu T, Mendola P and Buck GM (2002) Ethnic differences in the presence of secondary sex characteristics and menarche among US girls: the Third National Health and Nutrition Examination Survey, 1988–1994. Pediatrics 110,752–757.[Abstract/Free Full Text]

Submitted on April 28, 2005; resubmitted on July 19, 2005; accepted on July 25, 2005.


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