Abstract
To evaluate the connection between menstrual disorders and body fat mass, we examined a group of 30 ballet dancers and a group of 30 non-athletic girls (controls). Body mass index (BMI) was calculated and percent body fat (FAT^sub %^) was measured using the bioelectrical impedance method. A questionnaire was used to obtain age at menarche and duration of menstrual cycles. Ballet dancers had significantly lower values of BMI (18.56 1.53 vs. 19.96 2.2 kg/ m^sup 2^) and FAT^sub %^ (18.85 4.50 vs. 23.41 4.34%) compared with controls. According to BMI, 50.0% of ballet dancers and 23.3% of the control group were underweight. Of underweight ballet dancers, 66.7% had lower values of body fat, while most underweight girls from the control group had normal body fat. Normal-weight obesity was registered in 40.9% of the control group and in 6.7% of ballet dancers. Amenorrhea was found in 20.0% and oligomenorrhea in 10.0% of ballet dancers. Ballet dancers more frequently had later appearance of menarche and menstrual cycles of longer duration than did non-athletic girls. A significant negative correlation was found between menstrual cycle duration and FAT^sub %^ among ballet dancers (r=-0.415). To prevent complications caused by changes of body fat mass, we conclude that body composition assessment in ballet dancers is very important.
Keywords: Body fat, amenorrhea, ballet dancers, bioelectrical impedance, body mass index
Introduction
It has been reported that reduced body fat and weight loss are accompanied by later appearance of menarche, menstrual cycle disorders and problems with conception, related to the reduction of sex-specific body fat involved in functioning of the reproductive system [1-3]. It has been recognized that the critical amount of body fat leading to amenorrhea is below 17%, while 22% is needed for regular menstrual cycles [4]. Athletes have lower values of body fat mass than sedentary individuals. Body fatness values for most female athletes range from 12 to 16%, depending on the sport [2]. For female athletes who participate in esthetic-acrobatic activities (like ballet and gymnastics) and strenuous endurance sports, low body fat is desirable because it is believed to enhance performance [2,3]. These sportswomen are those with the highest prevalence of amenorrhea [5]. Amenorrhea is accompanied by low bone density and early osteoporosis development owing to low estrogen secretion. Its occurrence in conjunction with a high level of physical activity accompanied by disordered eating and osteoporosis is described as the ‘female athlete triad’ [5]. The exact pathophysiological mechanism for developing amenorrhea has not yet been defined. Abnormal patterns of endogenous hypothalamic secretion of gonadotropin-releasing hormone, with decreased production of luteinizing hormone, is a mechanism considered to lead to decreased production of estrogen. Discovery of the adipose tissue hormone, leptin, has provided a possible connection between fat stores and the reproductive axis [6,7]. In amenorrheic athletes a typical diurnal pattern of leptin secretion is absent [5]. Although low body fat is commonly associated with amenorrhea, the ‘critical body fat hypothesis’ has not been substantiated by longitudinal research. Women with normal body fat may also experience hypothalamic amenorrhea [5].
On the other hand, overweight is usually due to body fat enlargement. Yet some conditions, like muscle hypertrophy or edema, can also result in body weight increase, which can be characterized as obesity according to body mass index (BMI). In contrast, normal- weight people can have a higher amount of body fat, called normal- weight obesity or sarcopenic obesity, with body fat enlargement being made at the expense of lean body mass, especially muscle mass, while total body weight does not change [8].
The present study was undertaken to determine BMI and percentage body fat and to evaluate their relationship with amenorrhea prevalence in ballet dancers and non-athletic girls.
Methods
The study group comprised 30 ballet dancers (mean age 17.4 2.01 years). The mean period of ballet dancing was 9.3 1.75 years, and the mean training intensity was six 6-h sessions per week. The control group comprised 30 non-athletic high-school girls with mean age of 18.01 1.3 years. The study was performed according to the principles of the Helsinki Declaration, and informed consent was obtained from all participants.
A questionnaire was used to obtain age at menarche and duration of the menstrual cycle. Primary amenorrhea was diagnosed if menstrual bleedings had not occurred by age 14 and the subject had not developed secondary sexual characteristics, or by age of 16 if secondary sexual characteristics were present. Secondary amenorrhea was diagnosed when there were no regular menstrual cycles in a 3month period if previous menstruation had been regular, or in a 6- month period if previous menstruation had been irregular. The appearance of menstrual bleeding in a period of 35 days to 6 months was defined as oligomenorrhea [5].
With the subject wearing light indoor clothes and no shoes, body weight (BW) and height (BH) were measured to the nearest 0.1 kg and 0.1 cm, respectively, and BMI was calculated with the formula: BMI = BW/BH^sup 2^ (kg/m^sup 2^). Evaluation of BMI values was based on the criteria given by the World Health Organization [9] (Table I). Subjects with BMI
Body composition was assessed with the bioelectrical impedance method using a Tanita TBF-310 Body Composition Analyzer (Tanita Corporation, Tokyo, Japan). This impedance analyzer provides measurements of body fat mass (FATkg), percent body fat (FAT^sub %^), lean body mass (LBM^sub kg^) and total body water (TBW^sub kg^). For evaluation of body fat amount we used the reference values given by the manufacturer (Tanita Body Fat Scale) (Table II). Normal- weight obesity was defined as higher percent body fat (> 24%) in normal-weight subjects (BMI =18.5-24.9 kg/m^sup 2^).
Table I. Body mass index (BMI) references for adults.
Table II. Desirable ranges of percent body fat (Tanita Body Fat Scale).
Data are presented as mean standard deviation. In statistical analyses we used Student’s t test and linear correlation.
Results
Table III gives the basic anthropometric characteristics of the group of ballet dancers and the control group of non-athletic girls. Body weight (51.48 5.01 vs. 57.53 7.57 kg, p = 0.000021), body height (166.55 6.07 vs. 169.66 6.30 cm, p = 0.00858) and BMI (18.56 1.53 vs. 19.96 2.12 kg/m^sup 2^, p = 0.00066) were significantly lower in ballet dancers than in the control group.
Mean values of body composition parameters in both study groups are summarized in Table IV. Ballet dancers had significantly lower values of body fat, both as a percentage (18.85 4.50 vs. 23.41 4.34%, p = 0.000012) and absolute amount (10.01 2.68 vs. 13.70 4.17 kg, p = 0.00012), compared with the control group.
Evaluating BMI values (Figure 1) it was noticed that underweight was present in both groups, but to a greater extent in the group of ballet dancers (50.0%). Most subjects from the control group had normal body weight (73.3%) compared with the group of ballet dancers, where it was 50.0%. Pre-obesity was found only in the non- athletic girls (3.3%).
Most of the underweight ballet dancers (66.7%) had at the same time lower values of FAT%, while only 33.3% had normal values of body fat (Figure 2). In the control group, most of the underweight subjects (85.7%) had normal values of body fat with only 14.3% of these subjects having lower values of body fat. In the group of normal-weight ballet dancers, 6.7% had lower values of body fat, while the same category was not registered in non-athletic girls. Normal values of body fat were found for 86.7% of normal-weight ballet dancers and 59.1% of normal-weight subjects in the control group. The phenomenon of normal-weight obesity was registered in 40.9% of subjects from the control group and in 6.7% of ballet dancers. All pre-obese non-athletic girls had higher values of body fat.
Applying the criteria stated above for defining amenorrhea and oligomenorrhea, we analyzed their presence in the study and control groups (Figure 3). No subject from the control group had either of these menstrual cycle disorders, while the presence of amenorrhea in the group of ballet dancers was 20% (secondary amenorrhea) and of oligomenorrhea, 10%. Ballet dancers more frequently had later appearance of menarche (from 14 to 16 years) (Figure 4), and menstrual cycles longer than 30 and 60 days, compared with non- athletic girls (Figure 5). We correlated age at menarche and menstrual cycle duration with BMI, FAT^sub %^, and FAT^sub kg^, finding a significant negative correlation among ballet dancers between duration of the menstrual cycle and both BMI (r=-0.386) and percent body fat (r=-0.415) (Table V).
Table III. Values of anthropometric parameters in ballet dancers and non-athletic girls.
Table IV. Parameters of body composition in ballet dancers and non-athletic girls.
Figure 1. Distribution of body mass index (BMI) values in ballet dancers and non-athletic girls.
Figure 2. Body mass index (BMI) compared with percen\t body fat (FAT%) in ballet dancers and non-athletic girls.
Discussion
It has been very well documented that the prevalence of amenorrhea is much greater in the population of athletes than in the general female population. Skolnick found 3.4-66% of female athletes and 2-5% of non-athletic women to suffer with amenorrhea [10], while a Finnish study reported menstrual disturbances in 27-37% of esthetic, endurance and weight-bearing athletes and in 5% of controls [11].
Frisch and Revelle postulated the ‘critical weight hypothesis’ for the induction of sexual maturation and found a connection between body fat and reproduction, which was confirmed later by the discovery of leptin and its influence on the hypothalamo-hypophyso- ovarian axis [12]. According to Frisch, the minimum level of fatness associated with menarche is 17% and 22% is necessary for the onset of regular menstrual cycles [4]. Recent findings suggest that low energy availability, rather than low body fatness or exercise stress, is the likely mechanism by which exercise negatively influences the hypothalamo-hypophyso-ovarian axis in female athletes [13]. Despite speculations about the possible pathophysiological mechanism of amenorrhea, routine clinical practice needs some useful parameters that could provide early recognition of subjects at higher risk. Ballet dancers have very low body weight and body fat (13-20%) and are known to be at high risk for the development of hypothalamic amenorrhea [1,14-17]. Our results of body fat mass estimation in ballet dancers (mean 18.85 4.5%) are similar to previous values given by Hergenroeder and colleagues (20.1 3.6%) [18] and Yannakoulia and associates (19.4 4.3%) [19]. In our study, amenorrhea was present in 20% and oligomenorrhea in 10% of the ballet dancers, with more frequent later appearance of menarche and menstrual cycles longer than 30 and 60 days, compared with non- athletic females.
Table V. Correlation of age at menarche and menstrual cycle duration with body mass index (BMI), percent body fat (FAT^sub %^) and body fat mass (FAT^sub kg^).
Figure 3. The presence of amenorrhea, oligomenorrhea and eumenorrhea in ballet dancers and non-athletic girls.
Figure 4. Age at menarche in study and control subjects.
Figure 5. Menstrual cycle duration in study and control subjects.
Lin-Su and co-workers noted that although body fatness as a determinant of menarche has been well documented, it is limited to underweight females [20]. Underweight subjects can have normal body fat; as can normal-weight subjects have low body fat. According to our data, 50% of the ballet dancers were underweight. However, underweight was present in a great number of control group subjects too (23.3%) but we did not register menstrual disorders among them. These two groups of underweight subjects showed differences in body fat mass: a higher percentage of underweight ballet dancers had lower values of body fat at the same time (66.7%), while the largest number of underweight subjects from the control group had normal values of body fat (85.7%). These results suggest lower reliability of BMI in the prediction of risk for menstrual disorders compared with body fat. We also found a stronger negative correlation between body fat and menstrual cycle duration, compared with BMI. In contrast, Falseti and colleagues emphasized the value of BMI as a good prognostic factor in recovery from hypothalamic amenorrhea [21]. BMI has been suggested a good predictor of body fat mass, which is used in the diagnosis of underweight, overweight and obesity [9]. But a number of studies have confirmed that discrepancies arise between BMI and body fat. BMI does not discriminate between fat, muscle and bone mass. Some data indicate that even though BMI is reliable measure of fatness, an adolescent’s percentage of fat can change by as much as -3 to + 7% without any difference in BMI; for an individual adult, the same BMI can correspond to changes in fat of 5% [22-24]. Some studies also refer to its low and variable sensitivity as an indicator of the risk for overweight and the presence of overweight, and show that accuracy of prediction is lowest when BMI is
Conclusion
Our data show that ballet dancers had statistically lower values of BMI and percent body fat than did non-athletic girls of the same age. The largest number of underweight ballet dancers (66.7%) had at the same time lower values of body fat, while the most underweight girls from the control group (85.7%) had values of body fat in the normal range. Normal-weight obesity was present in 40.9% of the control group and even in 6.7% of the ballet dancers. Amenorrhea was present in 20% and oligomenorrhea in 10% of the ballet dancers, while the same disorders were not found in the control group. Ballet dancers also more frequently had later appearance of menarche and menstrual cycles longer than 30 and 60 days, compared with non- athletic girls. The finding of a significant negative correlation between menstrual cycle duration and body fat mass (r =-0.415) in ballet dancers leads us to the conclusion that body composition assessment can help in the detection and prevention of menstrual cycle disorders.
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EDITA STOKIC1, BILJANA SRDIC2, & OTTO BARAK3
1 Department of Endocrinology, Diabetes and Metabolic Disorders, Institute for Internal Medicine, Novi Sad, Serbia and Montenegro, 2 Department of Anatomy, Medical Faculty, Novi Sad, Serbia and Montenegro, and 3 Department of Physiology, Medical Faculty, Novi Sad, Ser\bia and Montenegro
Correspondence: E. Stokic, Department of Endocrinology, Diabetes and Metabolic Disorders, Institute for Internal Medicine, Hajduk Veljkova 1, 21000 Novi Sad, Serbia and Montenegro. Tel: 381 21 524563. Fax: 381 21 524563. E-mail: [email protected]
Copyright CRC Press Apr 2005
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