European Journal of Obstetrics & Gynecology and Reproductive Biology 218 (2017) 68–72

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European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Full length article

Interactions of physical activity and body mass index with age at

menarche: A school-based sample of Chinese female adolescents
Chao Xinga,1, Zhaohui Huangb,1, Jie Lia,1, Ming Lia , Laichao Xua , Jianhua Taoa , Lijun Fua ,
Yirong Fanga,*
a
Department of Infectious Disease, Shaoxing Center for Disease Control and Prevention, Shaoxing, China
b
Anhui Provincial Family Planning Institute of Science and Technology, Hefei 230031, Anhui Province, China

A R T I C L E I N F O A B S T R A C T

Article history: Background: To test the independent and interactive associations of physical activity (PA) and body mass
Received 26 October 2016 index (BMI) with age at menarche among Chinese adolescence.
Received in revised form 14 September 2017 Methods: We conducted a cross-sectional survey in two elementary schools in September 2015 in
Accepted 18 September 2017
Shaoxing city, Zhejiang province, China. We used self-administered questionnaires to collect the
Available online xxx
information of the participators. Analyses were performed with logistic regression models, and the
relative excess risk due to interaction (RERI), the attributable proportion because of the interaction (AP),
Keywords:
and the synergy index (S) were used to evaluate the biological interaction.
Menarche age
Physical activity
Results: A total of 1530 middle school students from grade 1–3 were selected for this study, and we
Obesity collected 1505 (98.366%) valid questionnaires for the last analyses. The mean age of menarche is 11.603
Interactive effect (SD = 0.447) years. Students with overweight/obesity and without SMPA had the highest risks of early age
of menarche (OR = 3.507, 95%CI: 1.929–6.376) compared with women both with a normal BMI and with
SMPA, and the RERI was 1.846 (95% CI: 0.415–4.107), meaning that there was positive interaction on the
additive scale.
Conclusion: Insufficient PA can significantly modify the association between obesity and early menarche
risk. Therefore, the government and society should pay more attention to the promotion of PA throughout
childhood and adolescence.
© 2017 Published by Elsevier Ireland Ltd.

What is already known on this topic
1. Several international studies during recent decades have
presented a remarkable downward secular trend in age at
menarche.
2. Age at menarche reflects numerous health aspects of a
population, and may also represent a potential health risk if it
deviates from its nominal values.
3. There were many factors affecting the age at menarche, such
as genetics, obesity, geography, dietary habits, physical exercise,
and even climate.
What this paper adds
1. Body mass index (BMI) is significant negatively correlated
with age at menarche, and their correlations was modified by
physical exercise (PA).
* Corresponding author at: Department of Infectious Disease, Shaoxing Center for
Disease Control and Prevention, Shijijie Road, Shaoxing City, 312000, China.
E-mail address: fyr2015@126.com (Y. Fang).
1
Chao Xing, Zhaohui Huang and Jie Li contributed equally to this article.
2. Especially, there was about 52.612% of the risk of early age at
menarche in students attributed to the interaction between
overweight/obesity and insufficient PA.
3. Comparing with vigorous PA, moderate PA may play a more
important role in the moderating Effect model.
Introduction
The onset of menarche is an important milestone in reproduc-
tive life, and changes in the age at menarche have been an area of
great research interest for decades. Several international studies
during recent decades have presented a remarkable downward
secular trend in age at menarche. For example, a study in Europe
reported a significant decrease of the median age at menarche
from 13.66 years to 13.05 years during the half century [1]. In the
United States, the proportion with early menarche (<11 years)
increased from 4.00% to 11.80% over the last 50 years [2]. While, in
China, the average age at menarche also showed a downward trend
from 13.41 years in 1985 to 12.47 years in 2010, and this decrease
has been approximately 4.50 months per decade [3,4].

https://doi.org/10.1016/j.ejogrb.2017.09.018
0301-2115/© 2017 Published by Elsevier Ireland Ltd.
 C. Xing et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 218 (2017) 68–72
Age at menarche reflects numerous health aspects of a
population, and may also represent a potential health risk if it
deviates from its nominal values. Recent studies reported that age
at menarche may affect the risk of various diseases in adulthood.
Epidemiologic evidence have provided the supports for the
conclusion that earlier menarche is associated with detrimental
health effects; for example, early menarche may be associated with
increased risks of cardiovascular disease, gestational diabetes
mellitus, asthma, nonalcoholic fatty liver disease, as well as the
risky sexual behaviors among adolescent females [5–9]. While,
other studies have showed the associations of increasing age at
menarche with some health problems such as infertility and post-
menopausal depression [10,11].
There were many factors affecting the age at menarche, such as
genetics, geography, dietary habits, physical exercise, and even
climate. Body mass index (BMI) has been shown the most
important factor that associated with the age at menarche, and
the inverse correlation between BMI and age at menarche was
statistically significant (R = 0.49) [4]. A recent systematic review
revealed that physical activity (PA) might also influence the onset
of puberty, and age at menarche delay was well documented for
females exposed to regular high intensive physical exercises in
childhood and adolescence [12].
Although PA and BMI were separately associated with the age at
menarche, the interactions of PA and BMI with age at menarche
have been less studied, particularly in general Chinese samples.
The main purpose of this study was to examine (i) the relationship
between PA, BMI and age at menarche; and (ii) the interactive
effects of PA and BMI on age at menarche among Chinese middle
school students.
Method
Participants
We conducted a school-based cross-sectional survey in two
elementary schools in Shaoxing city, Anhui province, China. This
study was conducted in September 2015 and was approved by the
Ethics Committee of Anhui Medical University. Written informed
consents were obtained from all of the participants. We used self-
administered questionnaires to collect the information of the
participators, and the questionnaires needed to be completed
within 30 min in the classroom independently. Teachers remained
in the classroom and took charge of collecting questionnaires and
checking the quality of questionnaires. Teachers also answered the
student questions about the study when necessary. A total of 1530
middle school students from grades 1–3 were selected for this
study, and we collected 1505 (98.40%) valid questionnaires.
Measure of primary outcomes
BMI
The weight and height of participators were measured by
trained interviewers according to a standardized protocol. Weight
was measured to the nearest 0.1 kg with lever scales, and height
was measured to the nearest 0.1 cm, using metal column height
measuring stands. BMI was calculated as the weight (kg) divided
by the height squared (m2). Overweight and obesity were classified
according to the international standard by Cole at al [13].
Physical activity (PA)
PA was assessed by the Youth Risk Behavior Surveillance (YRBS).
The following two questions were used:
(1) Moderate physical activity (MPA): during the past 12 months,
on how many of the past 7 days did you take part in physical
69
activity or exercise for at least 30 min where you heart did not
beat fast or you did not breathe hard, such as fast walking, slow
bicycling, skating, pushing a lawn mower, or mopping floors?
(The responses range from 0 to 7 days)
(2) Vigorous physical activity (VPA): during the past 12 months, on
how many of the past 7 days did you exercise or take part in
physical activity that made your heart beat fast and made you
breathe hard for at least 20 min, such as basketball, soccer,
running or jogging, fast dancing, swimming laps, tennis, fast
bicycling, or similar aerobic activities? (The responses range
from 0 to 7 days)
Sufficient vigorous physical activity (SVPA) was defined as no
less than three days of VPA with 20 min each week. Sufficient
moderate physical activity (SMPA) was defined as no less than five
days of MPA with 30 min each week. Insufficient physical activity
(IPA) was defined as participating in <2 days of 20 min of VPA and
in <4 days of 30 min of MPA in the week preceding the survey [14].
Age at menarche
The age at menarche was determined using the recall method.
The participators were requested to state to the nearest whole year,
how old they were when they first experienced menstrual flow.
Age at menarche was measured to the nearest 0.1 years. We set the
cutoff at 25% of the maximum as early age at menarche and the
cutoff at 75% of the minimum as late age at menarche.
Statistical analysis
The Pearson chi-square was performed to assess differences in
the characteristics between rural and urban participators. The
multivariable logistic regression model was performed to explore
the independent and interactive relationship between BMI and PA
on age at menarche. We also used the relative excess risk due to
interaction (RERI), the attributable proportion because of the
interaction (AP), and the synergy index (S) to evaluate the
biological interaction based on the additive interaction of BMI
and PA, which are often considered the standard measure for
interaction on the additive scale. If there was no biological
interaction, the confidence interval (CI) of RERI and AP included 0,
and the CI of SI contained 1.0 [15,16]. All statistical analyses were
conducted using SPSS version 13.0 (Statistical Package for the
Social Sciences). A P < 0.05 was considered to be statistically
significant.
Result
Characteristics of the study sample
Table 1 presents the characteristics of the sample stratified by
resident area. Overall, 1505 students participated in the assess-
ments. Participants from grade one (n = 465) accounted for
30.897% of the total sample; grade two (n = 519) accounted for
34.485% of the total sample. The mean age of all participators was
13.726 years (standard deviation [SD] = 1.003). The mean age of
menarche is 11.603 (SD = 0.447) years. Overall, 7.708% of the
students were overweight/obesity, and 43.854%, 15.216%, and
52.027% of the students had SVPA, SMPA, and IPA during the past
one year, respectively.
Independent association of BMI and PA with age of menarche
Table 2 presents the independent association of BMI and PA
with age of menarche. Students without SMPA (OR = 1.937, 95% CI:
1.305–2.877), without SVPA (OR = 1.719, 95% CI: 1.323–2.234), and
with IPA (OR = 1.718, 95% CI: 1.329–2.220) was associated with an
70 C. Xing et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 218 (2017) 68–72

Table 1
Characteristics of the sample among Chinese middle school girls.

Variable Total Rural Urban x2-value/t valuea p-value

Age 13.726  1.003 13.768  0.977 13.672  1.032 2.015 0.044
Age at Menarche 11.603  0.447 11.824  0.365 11.322  0.613 4.173 0.000
BMI 19.062  2.754 19.047  2.612 19.082  2.943 0.227 0.821
Overweight/obesity
No 1389(92.292) 804(92.948) 585(91.406) 1.229 0.268
Yes 116(7.708) 61(7.052) 55(8.596)
SVPA
No 845(56.146) 505(58.382) 340(53.125) 4.128 0.042
Yes 660(43.854) 360(41.618) 300(46.875)
SM PA
No 1276(84.784) 724(83.699) 552(86.250) 1.855 0.173
Yes 229(15.216) 141(16.301) 88(13.750)
IPA
No 722(47.973) 405(46.821) 317(49.531) 1.083 0.298
Yes 783(52.027) 460(53.179) 323(50.469)

Note: Values are presented as mean  SD or number (percentage) when appropriate; BMI = body mass index; SVPA = sufficient vigorous physical activity; SMPA = Sufficient
moderate physical activity; IPA = insufficient physical activity.
a
Quantitative data was analyzed using t-test and categorical data was analyzed using chi-square test.

Table 2
Associations of physical activity, BMI and age at menarche among Chinese middle school girls. (n = 1 303).

Variable Early age at menarche Late age at menarche

No. (%) Crude OR (95%CI) Adjusted OR (95%CI)a No. (%) Crude OR (95%CI) Adjusted OR (95%CI)a
SMPA
Yes 33(16.019) 1.000 1.000 88(42.718) 1.000 1.000
No 296(26.983) 1.937(1.305–2.877) 1.926(1.264–2.934) 255(23.245) 0.406(0.298–0.553) 0.383(0.273–0.537)
SVPA
Yes 109(19.569) 1.000 1.000 212(38.061) 1.000 1.000
No 220(29.491) 1.719(1.323–2.234) 1.890(1.422–2.512) 131(17.560) 0.347(0.269–0.447) 0.315(0.240–0.413)
IPA
No 122(19.935) 1.000 1.000 233(38.072) 1.000 1.000
Yes 207(29.957) 1.718(1.329–2.220) 1.926(1.457–2.545) 110(15.919) 0.308(0.237–0.400) 0.270(0.205–0.357)
BMI
Normal weight 277(25.460) 1.000 1.000 279(25.643) 1.000 1.000
Overweight/obesity 46(40.708) 2.010(1.348–2.997) 1.839 (1.193–2.835) 18(15.929) 0.549(0.326–0.926) 0.562(0.333–0.949)

BMI = body mass index; SVPA = sufficient vigorous physical activity; SMPA = Sufficient moderate physical activity; IPA = insufficient physical activity.
a
Adjusted for grade, residential district, the only child in the family, the parents’ education level.

increased risk of early age of menarche. Adjusting for grade,
residential district, the only child in the family, the parents’
education level produced similar results.
Compared with student with normal weight, the students with
overweight/obesity had a significantly increased risk for early age
of menarche (OR = 2.010, 95% CI: 1.348–2.997) and decreased risk
of late age of menarche (OR = 0.549, 95% CI: 0.326–0.926).
Adjusting for grade, residential district, the only child in the
family, the parents’ education level produced similar results.
Interactions of BMI and PA with age of menarche
The interaction effects of BMI and PA with age of menarche are
shown in Tables 3–4. We found a significant additive interaction
between BMI and PA (P < 0.05). The risk of early age of menarche
was much higher in those with overweight/obesity and without
SMPA (OR = 3.716, 95% CI: 2.134–6.472), and the RERI was 2.229
(95% CI: 0.197–4.361), meaning that there was positive interaction
on the additive scale.
Students with overweight/obesity and without SVPA during the
past one year had the highest risks of early age of menarche
(OR = 3.498, 95%CI: 1.977–6.190) compared with women with a
normal BMI and with SVPA, and the RERI was 0.406 (95% CI: 0.018–
2.584), meaning that there was positive interaction on the additive
scale.
Students both with overweight/obesity and IPA had the highest
risks of early age of menarche (OR = 3.595, 95% CI: 2.028–6.373)
compared with women with a normal BMI and with sufficient PA,
and the RERI was 0.746 (95% CI: 0.053–2.897), meaning that there
was positive interaction on the additive scale.
The interaction effects of BMI and PA with late age of menarche
are also performed and presented in Tables 3–4, these results
revealed that there was significant negative interaction only
between overweight/obesity and IPA on the additive scale (the
confidence interval of RERI and AP not include 0).
Discussion
To our knowledge, the present study is the first to examine the
combined effects of PA and BMI on age at menarche in China. We
found that BMI is significant negatively correlated with age at
menarche, and their correlations was modified by PA. Especially,
there was about 52.612% of the risk of early age at menarche in
students attributed to the interaction between overweight/obesity
and IMPA, while the proportion was only 18.215% modified by IVPA
.Therefore, the government and society should pay more attention
to the promotion of moderate PA throughout childhood and
adolescence to prevent the downward trend of age at menarche in
China.
The median age at menarche in the current study (12.36 years)
is similar with the earlier reported Chinese national surveys results
 C. Xing et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 218 (2017) 68–72 71

Table 3
Odds ratio (95% CI) associated with the interaction of physical activity and BMI on age at menarche among Chinese middle school girls. (n = 1 303).

PA BMI Early age at menarche Late age at menarche

a
No. (%) Crude OR (95%CI) Adjusted OR (95%CI) No. (%) Crude OR (95%CI) Adjusted OR (95%CI)a
SMPA
Yes Normal weight 31(17.725) 1.000 1.000 69(39.4) 1.000 1.000
Overweight/obesity 2(14.327) 0.774(0.165–3.635) 0.856(0.170–4.304) 4(28.6) 0.614(0.185–2.037) 0.524(0.150–1.826)
No Normal weight 246(26.875) 1.713(1.132–2.594) 1.805(1.160–2.808) 210(23.0) 0.459(0.327–0.645) 0.414(0.285–0.602)
Overweight/obesity 44(44.05) 3.716(2.134–6.472) 3.507(1.929–6.376) 14(14.1) 0.253(0.133–0.481) 0.263(0.133–0.519)
SVPA
Yes Normal weight 88(19.312) 1.000 1.000 169(37.1) 1.000 1.000
Overweight/obesity 20(35.725) 2.317(1.279–4.197) 2.054(1.077–3.918) 12(21.4) 0.462(0.237–0.898) 0.509(0.250–1.036)
No Normal weight 189(29.876) 1.775(1.331–2.368) 1.932(1.415–2.637) 110(17.4) 0.356(0.269–0.471) 0.325(0.241–0.438)
Overweight/obesity 26(45.587) 3.498(1.977–6.190) 3.651(1.962–6.793) 6(10.5) 0.199(0.084–0.474) 0.199(0.081–0.490)
IPA
No Normal weight 101(20.012) 1.000 1.000 188(37.2) 1.000 1.000
Overweight/obesity 20(34.524) 2.110(1.177–3.783) 1.864(0.989–3.514) 12(20.7) 0.441(0.228–0.854) 0.482(0.238–0.974)
Yes Normal weight 176(30.218) 1.738(1.313–2.302) 1.927(1.423–2.610) 91(15.6) 0.313(0.235–0.418) 0.276(0.203–0.374)
Overweight/obesity 26(47.289) 3.595(2.028–6.373) 3.945(2.260–7.178) 6(10.9) 0.207(0.087–0.493) 0.201(0.082–0.494)

BMI = body mass index; SVPA = sufficient vigorous physical activity; SMPA = Sufficient moderate physical activity; IPA = insufficient physical activity.
a
Adjusted for grade, residential district, the only child in the family, the parents’ education level.

Table 4
Indexes of additive biological interactive effect of BMI and physical activity on age at menarche.

Measure Early age at menarche Late age at menarche

Unadjusted Adjusteda Unadjusted Adjusteda

SMPA  Overweight/obesity
RERI 2.229(0.197–4.361) 1.846(0.415–4.107) 0.180( 0.591–0.951) 0.325( 0.367–1.015)
AP 0.600(0.298–1.002) 0.526(0.035–1.018) 0.710( 2.382–3.802) 1.236( 1.512–3.983)
S 5.573(2.276–34.152) 3.792(2.302–47.559) 0.806(0.351–1.852) 0.695(0.361–1.337)
SVPA  Overweight/obesity
RERI 0.406(0.018–2.584) 0.665(0.187–3.015) 0.382(0.037–0.726) 0.365( 0.029–0.760)
AP 0.116(0.029–0.694) 0.182(0.075–0.744) 1.917( 0.182–4.016) 1.832( 0.469–4.133)
S 1.194(1.028–3.048) 1.335(1.099–3.566) 0.677(0.493–0.928) 0.687(0.480–0.983)
IPA  Overweight/obesity
RERI 0.746(0.053–2.897) 1.054(0.338–3.446) 0.452(0.123–0.782) 0.444(0.073–0.814)
AP 0.208(0.022–0.720) 0.274(0.018–0.766) 2.184(0.490–4.278) 2.207(0.145–4.560)
S 1.404(1.148–3.594) 1.589(1.055–4.203) 0.637(0.472–0.858) 0.643(0.463–0.892)

BMI = body mass index; SVPA = sufficient vigorous physical activity; SMPA = sufficient moderate physical activity; IPA = insufficient physical activity; RERI = the relative excess
risk because of the interaction; AP = the attributable proportion because of the interaction; S = the synergy index. RERI = 1 + OR11-OR10-OR01; AP = RERI/OR11; S = OR11- 1/
OR10 + OR01-2; If there was no biological interaction, the confidence interval of RERI and AP include 0, and the confidence interval of S contains 1.
a
Adjusted for grade, residential district, the only child in the family, the parents’ education level.

[3,4,17], but is earlier when compared with recently published
data, including a cross-sectional study in African cities, Korea
National Health and Nutrition Examination Survey, British
National Child Development Study, Hong Kong's “Children of
1997” birth cohort, and Coronary Artery Risk Development in
Young Adults (CARDIA) study in US and United Kingdom [5,18–21].
We found that BMI is significant positively correlated with the
age at menarche, which is consistent with those from previous
reports. Several studies reported that the downward shifts of the
age at menarche have been accompanied by a simultaneous
increase in BMI [4,22,23]. The prevalence of childhood obesity has
increased dramatically over the past decades and has been a
substantial public health concern worldwide. In China, the average
value of BMI among primary and secondary school students has
also increased dramatically both in boys and girls [24]. Since earlier
menarche and higher BMI acting together may pose a risk for
women’s health in later years, changes are required in sexual
education in primary schools in and interventions such as obesity
prevention should be designed and facilitated for girls with early
menarche in order to decrease their likelihood of future health
risks.
As we all know, the insufficient PA in children appears to
combine with a high prevalence of obesity and overweight.
Therefore, we hypothesized that the combined effect of obesity
and insufficient physical activity may increase the risk of many
chronic diseases or health problems. For example, Wang et al. [25]
reported the combined effects of physical inactivity and obesity
would increase the risk of anxiety and depression in adolescents.
Huxley et al. [26] revealed that the association between BMI with
risk of atrial fibrillation differed by level of physical activity in men.
Obese men who were reported as having sufficient physical
activity at baseline had 37% increased risk of atrial fibrillation
compared with 156% in those with insufficient physical activity.
Then, Azarbal F et al. [27] performed a multiethnic cohort of 81 317
postmenopausal women and further determined the interaction
between obesity and physical activity on the risk of incident trial
fibrillation. Interestingly, although no study have been reported
about the interaction of obesity and IPA on earlier menarche, we
firstly found that PA, a low cost intervention with myriad health
benefits, would be an important modifier of the earlier menarche
risk produced by obesity. This result is imperative for the
development of effective primary prevention strategies.
There are some limitations to the present study. First, the cross-
sectional design was used in this study, which has little power to
determine the causal relationships. Prospective cohort studies are
needed to determine the causal relationships of BMI and PA with
earlier menarche. Second, the age at menarche was assessed by
recall method; thus, recall and reporting biases could not be
avoided. In our study, the collection of age at menarche was
completed soon after puberty; it was reported that the age at
72 C. Xing et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 218 (2017) 68–72
menarche obtained by the recall method was similar for girls who
menstruated within the previous three years; when more than
three years have passed, the recall bias was significant [28].
Therefore, the age at menarche in our study may be near to the true
value. Third, the influence of the type of the physical activity on the
age at menarche may be more important. However, we only used
two questions to collect the information on physical activities, and
divided the physical activities into two categories: MPA and VPA;
therefore we could not explore the influence of the specific type of
the physical activity on age at menarche, for example climbing
stairs, fast walking, running or jogging, and so on. The last, the true
age at menarche of the students might be underestimated. In our
study, a total of 202 (13.4%) students responded that they had not
experienced their first menstrual flow, and we excluded these
students from the last analyses. Therefore, we might underesti-
mate the median age at menarche, and the true age at menarche of
the students might be older than that reported in our study.
However, considering the detrimental health effects associated
with earlier menarche, we should pay more attention to the
continuously declining trend of age at menarche in China, as it was
reported that the average age at menarche have declined from
13.41 to 12.47 years between 1985 and 2010 in China [4].
Conclusions
Despite the above limitations, the present study highlighted the
importance of associations of BMI and PA with earlier menarche in
Chinese middle school students. Our results suggested that the
positive correlation between overweight/obesity and earlier
menarche risk was modified significantly by insufficient PA;
especially, 52.612% of the risk of early age at menarche in students
attributed to the interaction of the insufficient moderate PA. Our
findings might provide support for the suggestion that inter-
ventions are needed to reduce BMI and increase moderate PA in the
lifestyles of young people.
Conflicts of interest statement
The authors declare that they have no conflicts of interest to
declare, including financial, institutional, consultant and other
relationships that might lead to bias or conflicts of interest.
Acknowledgements
The authors would like to thank everyone for their valuable
contributions to this article. The study in this manuscript was
funded by the National Natural Science Fund of China (30972494)
and the Shaoxing city public service technology applied research
projects(2012B70060), and General Research Program for Medical
and Health of Zhejiang Province of China (2012KYB215). They had
no role in study design, data collection and analysis, decision to
publish or preparation of the manuscript.
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