Meat consumption and age of menarche among schoolgirls in Shanghai

Abstract

Background

Precocious puberty is defined as the precocious onset of pubertal manifestations, which is considered as the advanced occurrence of secondary sexual characteristics before age 9 in boys and age 8 in girls⁽¹⁾. Precocious puberty is reported to lead to accelerated growth, accelerated bone maturation and, ultimately, reduced stature⁽¹⁾. The incidence of precocious puberty has been rising worldwide in the past decades^{(2; 3; 4; 5)}. A Korean study showed the annual incidence of central precocious puberty (CPP) in girls significantly increased from 3.3 to 50.4 per 100 000 in girls and gradually increased in boys from 0.3 to 1.2 per 100 000 between 2004 and 2010⁽²⁾.

Menarche is a remarkable event in puberty, symbolizing the developmental process that transforms a sexually immature child to a reproductively capable adult⁽⁶⁾. The timing of menarche has been reported to influence prediabetes, diabetes and hormone-related cancers in adults^{(7; 8; 9; 10)}. Cohort studies have shown that early menarche is associated with increased risk of cardiometabolic disease, coronary heart disease and other vascular diseases^{(8; 11)}. A systematic reduction in the mean age at menarche has been shown in several studies from different countries^{(12; 13)}. For example, data from the 2005 Korean National Health and Nutrition Survey showed a downward trend of 0.68 years per decade (95% confidence interval [CI]: 0.64–0.71) in age at menarche⁽¹²⁾. Thus, research on modifiable factors that may prevent the early onset of menarche are worth public health attention.

Dietary intake may play an important role in pubertal timing⁽¹⁴⁾. Previous studies have reported that higher intake of animal and lower intake of plant protein were associated with earlier age at menarche⁽¹⁴⁾. Among 3 298 British girls participating in the Avon Longitudinal Study of Parents and Children, animal protein intakes at 3 years of age were positively associated with odds ratio (OR) for reaching menarche by 12 years 8 months old (OR for 1 standard deviation (SD) increment: 1.11, 95% CI: 1.02–1.21). These associations were stronger for protein intakes at 7 years old (OR for 1 SD increment: 1.17, 95% CI: 1.08–1.28)⁽¹⁵⁾. Similarly, the Harvard Longitudinal Study found that girls who consumed more animal protein at the same ages had earlier menarche⁽¹⁶⁾. Dietary fat intake may also play a role in the onset of puberty although the results are still inconclusive. Some studies found that higher intakes of polyunsaturated fatty acids were associated with earlier menarche^{(15; 16; 17)}, while several studies reported that higher intakes of saturated fatty acids, monounsaturated fatty acids, or animal fat were related to a later age of menarche^{(18; 19; 20)}. Previous reports regarding the association between energy intake levels and menarche age have been inconsistent. An Athens study found that increased energy intake and expenditure were associated with an increased age at menarche, while a report on a cohort of 213 girls reported no association^{(20; 21)}.

Meat intake has also been implicated in pubertal timing, but conclusions remain inconsistent. Cohort studies, as well as one cross-sectional study, have reported that higher intakes of meat were associated with earlier menarche^{(15; 22; 23)}. For example, a prospective investigation of 230 white girls from southern California found that girls who consumed meat at age 9–15 years reached menarche an average of 6 months earlier than girls with a vegetarian diet⁽²³⁾. However, studies exist that report no association between meat intake and age at menarche^{(24; 25)}.

Therefore, the relationship between dietary intake and pubertal development is still unclear. The purpose of our study was to examine the association between meat intake, particularly different types of meat, and risk of early menarche among school girls in Shanghai. Since most previous studies concentrated only on total intake of meat, we decided to add new research findings by investigating the frequency of intake of specific categories of meat.

Methods

Study population

For the Dietary and Health Status of Primary and Secondary School Students in Shanghai study, a total of 4 320 students which included 2160 girls and 2160 boys were randomly selected from primary and middle schools in Shanghai through a two-stage random sampling design. The sampling was conducted in 20 randomly selected primary schools, 20 junior middle schools, and 20 senior middle schools. One class was randomly selected per grade per school. Classes with at least nine boys and nine girls in them were selected although only girls were included in our study of the relationship between meat consumption and menarche. Students with missing information on diet (n=165) or age (n=14) were excluded from the analysis. Therefore, the remaining 1981 girls were full data available, of whom 986 girls who had experienced menarche were included for final data analysis.The ethical application and consent procedure of this study were approved by the Ethical Review Committee of the Shanghai Municipal Center for Disease Control and Prevention (No.2015-15). By filling in the questionnaire, patients and their parents gave written consent to participate in this study.

Dietary assessment

Meat intake was determined using a semi-quantitative food frequency questionnaire. Between August and November 2015, trained field interviewers went to students’ home to administer the FFQ for obtaining information on their children’s usual intake before the girls experienced menarche or boys experienced first ejaculation. The FFQ was modified from the validated semi-quantitative food frequency questionnaire which was used for China National Nutrition and Health Survey. The questionnaire asked the frequency (times per day, per week, per month or quarterly), times and the quantity (grams per time on average) the participants consumed a specific type of meat. The types of meat included pork, beef, lamb, poultry and processed meat (including sausage, ham sausage, pork luncheon meat, dried meat floss, ham, preserved meat and so on). Total meat intake was defined as the sum of the different types of meat mentioned above. Meat intakes were estimated by multiplying the consumption frequency of each food by the quantity.

Data quality control was guaranteed by a high standard of training of the field interviewers, who were trained for at least three days in the collection of dietary data. Where outliers were found, the household and individuals in question were revisited and asked about their food consumption to resolve these discrepancies.

Assessment of menarche

Girls were asked ‘whether you have menstrual periods’ and also ‘when you had your first menstrual bleeding (in years and months)’. Early menarche was defined as having first menses at <12 years of age, considering that this threshold has been associated with a higher risk of breast cancer and cardiovascular disease in adulthood^{(9; 26; 27; 28)}.

Assessment of covariates

Information on parental and household characteristics was collected by a standardized questionnaire, which was administered face to face by trained interviewers. The questionnaire inquired about parental educational levels, parental occupation and household income. Data on physical activity and sleep time were collected through a physical activity questionnaire. Physical activity was calculated as average minutes spent in moderate and high intensity exercise per day and sleep time was calculated as average hours spent sleeping per day. Anthropometric measurements, including height, weight, waist and hip circumference and percentage of body fat, were taken by trained field staff. Percentage of body fat was measured using the TANITA BC601 body fat measuring instrument (Tanita, Tokyo, Japan).

Statistical analysis

The included girls were divided into two groups based on whether their menarche age was before or after their 12th birthday The frequency of meat intake was categorized into three levels: never eats meat (0 time/week ), meat intake less than once a week (<1 time/week), and meat intake once or more per week (≥1 time/week). The total meat intake was also categorized into tertiles.

The relationship between meat intake frequency and age at menarche was investigated by comparing average menarche age for the three levels of meat intake using analysis of variance. We used age at menarche onset of less than 12 years as an outcome. Logistic regression models were applied to examine the unadjusted and adjusted associations between meat consumption frequency and age at menarche. We began with an unadjusted model (model 1) then added variables. In the first multivariable model (model 2), we adjusted for age and body mass index (BMI). We further adjusted for physical activity, sleep, household income, and parental education level (model 3). Using age at menarche as a continuous variable, multilinear regression analysis was used to determine the unadjusted and adjusted associations between meat consumption frequency and age at menarche. All data were analysed using the SPSS version 22.0 software package. A two-tailed P value of <0.05 was considered statistically significant.

Results

Of the 1 981 school girls aged 6–18 years selected, 49.80% (n=986) had experienced menarche at the point of the study. The mean age at menarche was 11.97±1.24 years. A total of 518 (26.10%) girls had their first menses before 12th birthday.

Of the 986 school girls who had had menarche, girls with earlier menarche tended to be taller and heavier, after adjusting for age. They had significantly higher waist circumference, hip circumference, weight and BMI. Earlier menarche age was associated with a higher percentage of body fat. Girls with earlier menarche spent more time on physical activity and sleeping compared to those with later menarche (P<0.05 for physical activity). No significant association was found between menarche age and mother or father’s education level or household income (Table 1).

Compared with those consuming meat less than once a week (<1 time/week), girls who consumed pork, beef, lamb, poultry or processed meat once or more a week (≥1 time/week) had a later menarche age (P<0.05 for pork and processed meat). Similarly, the average menarche age of girls who consumed pork, beef, lamb, poultry or processed meat once or more a week (≥1 time/week) was higher than those who did not consume meat at all (0 time/week). Overall, girls with higher total meat intake were more likely to have a later menarche age (P>0.05, Table 2).

Girls with pork intake less than once a week (<1 time/week) had a significantly higher risk of early menarche than those consuming pork once or more per week (≥1 time/week) (OR: 1.65, 95% CI: 1.17–2.34, Table 3). However, the association was not significant after adjusting for BMI and age. A similar association was found between processed meat intake and age at menarche. Girls consuming processed meat less than once a week (<1 time/week) had a higher risk of early menarche (OR: 1.38, 95% CI: 1.02–1.85) than those with intake once or more per week (≥1 time/week). After adjusting for BMI and age, the association was not significant. A lower consumption of poultry was associated with a lower risk of early menarche (P for trend <0.05, Table 3). After adjusting for BMI, age, physical activity, sleep, household income and parental education, the relationship remained. Girls who never consumed poultry (0 time/week) had a lower risk of early menarche compared with those who consumed poultry at least once a week (≥1 time/week) (OR: 0.61, 95% CI: 0.39–0.96) (Table 3).

The results of multilinear regression analysis revealed no statistical significant association between age at menarche and consumption of pork, beef, lamb, poultry, processed meat and total meat respectively, after controlling for BMI, age, physical activity, sleep, household income and parental education (data not shown).

Discussion

Our study results showed that a higher intake of poultry was associated with a higher risk of early menarche among school girls in Shanghai. The relationship remained after controlling for the girls’ BMI, age, physical activity, sleep, household income and parental education level. Neither the intake of pork, beef, lamb, processes meat nor total meat was associated with menarche age, after adjusting for BMI, age, physical activity, sleep, household income and parental education.

To our knowledge, this is the first report revealing an association between poultry intake and risk of early menarche. One potential explanation of the results is hormone abuse during poultry feeding. According to media reports, oestrogen as a ‘ripening agent’ is widely used for accelerating the growth of chicken on the ‘black’ market⁽²⁹⁾. In 2009 the Guangzhou Centre for Disease Control and Prevention reported a detection rate as high as 22.30% in poultry for diethylstilboestrol, a type of synthetic oestrogen⁽³⁰⁾. In 2001, 2003, 2004 and 2006, the sex hormone residue detection rates in poultry were 26%, 25%, 37.84% and 22.73%, respectively. The mean diethylstilboestrol residue in poultry was 1.24 mg/kg, and maximum residue can be up to 4.98 mg/kg⁽³⁰⁾. Chinese poultry products are usually sold nationwide, thus the above data from Guangzhou can also be considered representative for other big cities, including Shanghai.

Epidemiological studies strongly support the hypothesis that early or prepubertal exposure to oestrogenic compounds may induce human pubertal development^{(31; 32; 33; 34; 35)}. An investigation into an alarming incidence of premature menarche and precocious puberty from 1978 to 1984 in Puerto Rico suggested that early sexual development could be caused by exogenous oestrogen contamination in meat ingested by children⁽³¹⁾. A multicentre analysis of CPP distribution in north-west Tuscany, Italy, revealed a significantly higher annual CPP incidence in the Viareggio area than in other north-west Tuscany areas. The geographic distribution of CPP strongly suggested the involvement of environmental oestrogen exposure in CPP onset⁽³³⁾. That early menarche may be caused by hormone residues in poultry is also supported by our results showing that higher intake of poultry was associated with a higher risk of early menarche. Further studies are needed to confirm the finding, following which related government agencies must implement efficient measures to end hormone abuse in poultry feeding. Chinese Ministry of Agriculture Announcement number 235 was, in fact, promulgated to prohibit the use of synthetic hormones (trenbolone acetate and zeranol) in animal fattening. Thus, stronger and more efficient governmental supervision and management are required to avoid the illegal use of sex hormones in the poultry industry.

In our study, the total intake of meat was not significantly associated with early menarche. Consistently, a prospective study of 5 583 US girls and a cross-sectional study of 777 schoolgirls in Spain also concluded that the risk of early menarche was not associated with meat intake^{(24; 25)}. In the US prospective study, red meat (including pork, beef, lamb) as a whole was found not associated with age at menarche⁽²⁴⁾. Likewise, there were no statistically significant associations between age at menarche and consumption of pork, beef, lamb respectively in our study, after adjusting for covariates. However, several other studies have reported that higher intakes of meat were associated with earlier menarche^{(15; 16; 36; 37)}. A British cohort study reported that those with the highest meat intake (>8 portions/week) at 7 years had a 1.75 (95% CI: 1.25–2.44) times higher risk of early menarche, compared with girls in the lowest meat intake category (<4 portions/week)⁽¹⁵⁾. In a cross-sectional study of 422 Korean children, breast development was significantly positively associated with the factor score of ‘shellfish and processed meat’ after adjusting for age, body fat, and bone mineral content⁽²²⁾. Additionally, a recent prospective study reported that higher red meat intake frequency during childhood was associated with an earlier age at menarche. Girls who consumed red meat twice or more a day had a 64% higher probability of earlier age at menarche, compared with girls whose intake of red meat was less than four times a week⁽³⁸⁾. There are several reasons to explain the different results. Firstly, the classification of intake frequency of meat differed with our study. The British cohort study categorized the meat intake into five levels⁽¹⁵⁾, whereas total meat intake was categorized into tertiles in our study. Secondly, outcome measures differ between studies. The longitudinal Dortmund Nutritional and Anthropometric Longitudinally Designed Study used age at menarche as a continuous variable to analyse the association⁽³⁶⁾ and the outcome of the British cohort study was whether menarche was reached before or after 12 years 8 months, which was likely to be as near as possible to the median age at menarche of their study population⁽¹⁵⁾. Breast development was also used as the outcome in some studies^{(22; 39)}. Thirdly, differences in dietary assessment may be another reason. A food frequency questionnaire combined with a 3-day dietary record was used in the British cohort study⁽¹⁵⁾. The Korean cross-sectional study derived dietary patterns from 3-day food records. The food preference ‘shellfish and processed meat’ in the Korean cross-sectional study was vague; our study analysed the intake of specific categories of meat from a food frequency questionnaire. Notably, previous studies have yielded mixed results for different dietary assessments and different classifications of outcome. Further studies to confirm the association between age at menarche and total meat intake as well as red meat intake are required.

Our study reported that the mean age at menarche was 11.97±1.24 years and 26.10% of the girls had early menarche. Owing to the two-stage random sampling design, the result could be representative of the entire Shanghai school girl population, and even that of all large Chinese cities. The reported average age at menarche was 0.3 years earlier than that of urban Chinese girls in 2012 (12.28 years)⁽⁴⁰⁾, and also earlier than in some developed countries, including Denmark (13.13 years)⁽⁵⁾ and the United Kingdom (12.9 years)⁽⁴¹⁾. It may be time for China to take action to stop this worrying trend.

Some limitations are of note: the FFQ has not been formally validated. However the FFQ was modified from the validated semi-quantitative food frequency questionnaire which was used for China National Nutrition and Health Survey. The China National Nutrition and Health Survey is a nationally representative cross-sectional study on nutrition and non-communicable chronic diseases. It covered all 31 provinces, autonomous regions, and municipalities directly under the Chinese central government (except Taiwan, Hong Kong, and Macao). The FFQ has been used for decades. Many previous studies provided strong evidence for its validity^{(42; 43)}. Next the study design was cross-sectional and there was unavoidable recall bias when surveying with food frequency questionnaires. As the information of ‘age at menarche’ as well as ‘sleep time’ and ‘physical activity’ were also self-reported, they were all also subject to recall bias. And Data quality control was guaranteed by a high standard of training of the field interviewers.

Conclusions

 In conclusion, our study first reports that poultry intake is associated with the risk of early menarche. However, further studies are strongly suggested, to confirm the association between poultry intake and precocious puberty. Our research group is further studying this in both our ongoing cohort study and case–control studies.

Abbreviations

CPP: central precocious puberty, CI: confidence interval, OR: odds ratio, SD: standard deviation, BMI: body mass index

Declarations

Ethics approval and consent to participate

The ethical application and consent procedure of this study were approved by the Ethical Review Committee of the Shanghai Municipal Center for Disease Control and Prevention (No.2015-15).By filling in the questionnaire, patients and their parents gave written consent to participate in this study.

Consent for publication

Not applicable.

Availability of data and material

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding:

This work is supported by the Natural Science Foundation of Shanghai (No.17ZR1415700) and the National Natural Science Foundation of China (No.81773407). The sponsors had no role in data collection, analysis, or interpretation of the data, the writing of the report, or the decision to submit for publication.

Authors’ contributions

X. S. and W. C. designed the study. Z. Z., F. W., J. Z. and Z. W. contributed to the sample collection. Y. W. analysed the data. Y. W., X. S. and Q. G. wrote the manuscript. X. C. gave advice to the data analyse. All the authors accepted the final version.

Acknowledgements:

The authors would like to acknowledge the personnel of all teams for their participation and contribution to this work. We thank Ms. Yi Zhao for the English editing.

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Tables

 Table 1. Baseline characteristics of 986 school girls by age at menarche ^†

^† Values are age-adjusted means ± SDs, unless otherwise specified.

Table 2. Average age at menarche in 986 school girls by meat consumption frequency

Table 3. Odds ratio of early menarche (age <12 y) in 986 school girls by meat consumption frequency

^† Unadjusted model

^‡ Adjusted for BMI, age(years)

• Adjusted as for model 2 plus physical activity(min/d), sleep(hours/d), household income(<30000,30000-70000,or >70000 yuan per capita per year), parental education level(middle school or lower, high school, college or higher)

^¶ Calculated by treating categorical variables for meat as continuous variables