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Amenorrhea in ballet dancers in the Netherlands


Medicine & Science in Sports & Exercise: May 1996 - Volume 28 - Issue 5 - p 545-550
Clinical Sciences: Clinical Investigations

The prevalence of amenorrhea was studied among 113 professional and student ballet dancers in the Netherlands (mean age 23.3 yr, SD 4.8). Sixty-one dancers not on oral contraceptives were included in the subsequent analyses. Six cases (prevalence 9.8%, 95% confidence interval: 2.4-17.2) with secondary amenorrhea (≤4 cycles per year; previous menstruation ≥3 months prior to the study; menarche ≥1 yr prior to the study) were found. Two dancers had primary amenorrhea (no menarche at the age of ≥16). There was a negative correlation between the age of menarche and the number of menstrual cycles during the 12 months preceding the study (r = -0.46, P = 0.001). Body composition (four-compartment model), amount of dancing (recorded), resting energy expenditure (ventilated hood), dietary intake (recorded), and indices of eating disorders (Eating Disorders Inventory, EDI) were studied in 15 of the dancers, 5 amenorrheic and 10 eumenorrheic. No significant differences were found between the amenorrheic and eumenorrheic dancers. An explanation for the lower prevalence of amenorrhea in ballet dancers in the Netherlands, compared with U.S. dancers, was not obvious. Relatively low EDI scores (25.8, SD 14.5) in a subsample of 24 dancers could indicate less rigid emphasis on leanness and dieting.

UKK Institute for Health Promotion Research, Tampere, FINLAND; and University of Limburg, Department of Human Biology, Maastricht, THE NETHERLANDS

Submitted for publication October 1994.

Accepted for publication October 1995.

This study would not have been fulfilled without the cooperation of the ballet companies and schools. We are also indebted to the Department of Nuclear Medicine, at the Academic Hospital in Maastricht, for use of DXA apparatus, and to Loek Wouters, who performed the deuterium analyses.

Address for correspondence: Dr. Mikael Fogelholm, The UKK-institute for Health Promotion Research, P.O.B. 30, FIN-33501 Tampere, Finland.

Lean and intensively physically active females have an increased risk for late menarche and post-menarcheal menstrual disorders, that is, oligomenorrhea and amenorrhea(6,23,35,40). Women with athletic amenorrhea have been found to have reduced plasma levels of estrogen, progesterone, lutenizing hormone (LH), and follicle-stimulating hormone (FSH)(23). The hormonal milieu of amenorrhea may lead to premature bone loss (7,25), lower peak bone mass(6), and increase the risk for stress fractures(11,21,26) and scoliosis(37). Hence, amenorrhea might affect a dancer's or an athlete's career, increase her future risk for postmenopausal osteoporosis, and cause transient infertility (6).

Ballet dancers have been reported to have a high risk for amenorrhea: in four studies (2,4,5,16), the pooled(N = 151) mean prevalence of amenorrhea (absence of menstruation for≥4 months) was 31.4% (95% confidence interval: 23.9-38.8). Irregular cycles, oligomenorrhea, or amenorrhea (totaled) has been found in 55%-67% of ballet dancers (1,2,10,14). Hergenroeder et al. (15) found much lower prevalence: 17% of 112 ballet dancers had no more than six cycles per year. Nevertheless, even the reported 17% exceeded the 2%-5% prevalence of amenorrhea in the U.S.(40).

Several factors have been hypothesized to explain athletic amenorrhea: genetic predisposition (30), little body fat or low weight-for-height (10), strenuous training(3,29,35), low energy intake(15,17), and eating disorders(2), perhaps indicating socio-psychologic stress(24), unbalanced diet, or both. Factors associated with amenorrhea among American athletes have been studied frequently (e.g.,(7,17,20,24,25,27,30,33,39). Comparable data on American ballet dancers are less abundant(15,36,37), and data on European dancers are, to the best of our knowledge, not available.

The aims of the present study were: 1) to assess the prevalence of amenorrhea in ballet dancers in the Netherlands and to compare this prevalence to the corresponding prevalence previously reported in the U.S.; 2) to describe the dancers' training characteristics, resting energy expenditure, body composition, dietary intake, and indices of eating disorders; 3) to compare amenorrheic dancers' data with eumenorrheic dancers.

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Subjects and Study Design

This study was carried out in two phases. First (field phase or screening), 113 female dancers in four leading Dutch ballet companies (N = 63) and two ballet schools (N = 50) were asked about menstrual frequency, age of menarche, age at which dancing ballet started, and use of oral or intrauterine contraception. Both schools trained classical ballet dancers for a professional career. All dancers lived in the Netherlands; they were predominantly European, but only half of them were Dutch. Ten dancers were originally from North or South America, or Australia. Present users of oral contraceptives (N = 50) or intrauterine device (N = 2) were excluded from the subsequent part of the study.

In the second (laboratory) phase, training characteristics, resting energy expenditure, body composition, dietary intake, and indices of eating disorders were studied in 24 of the dancers (not on oral contraceptives). Five of these dancers had secondary amenorrhea (≤4 cycles per year; previous menstruation≥3 months prior to the study; menarche ≥1 yr prior to the study); ten reported 11 or 12 cycles during the previous 12 months (eumenorrheic dancers). The remaining nine dancers were excluded from further analysis. The variables were assessed between 8:00 a.m. and 2:00 p.m., after an overnight stay at the laboratory. For eumenorrheic dancers, the measurements were done within 14 d after the start of a menstrual period. All participants had been weight stable(±1 kg) for at least 1 month (self-report).

After being informed about the study, all subjects signed a written informed consent. The subjects' anonymity was preserved, excluding from the authors. The study was approved by the ethics committee of the University of Limburg, Maastricht, the Netherlands.

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Height, Weight, and Body Composition

Height was recorded in centimeters and weight, in a swimsuit on a high-precision digital-scale, in 0.005-kg increments. Weight change during the previous 12 months was estimated as the difference between the dancers' self-reported highest and lowest weight.

Body composition was assessed by a four-compartment model, which combines body density (Db) from underwater weighing (UWW), total bone mineral content (TBMC) from dual energy x-ray absorptiometry (DXA) and total body water (TBW) by deuterium dilution. Percent body fat (BF%) was calculated from the equation of Lohman (22): Equation where Db was expressed as kg·l-1, TBW as liters, and weight (WT) and TBMC as kg.

UWW was done with simultaneous lung volume measurement (He dilution; Volugraph 2000, Mijnhardt, the Netherlands) with an accuracy of 0.1 l. Weight was measured to the nearest 0.005 kg with a digital scale connected to a microcomputer. The mean value of four to six measurements of underwater weight(and lung volume) was used for the calculation of body density.

TBW was determined by deuterium dilution with deuterium-labeled water(2H2O). After an overnight fast, 0.1 g 2H2O per liter estimated TBW (99.8% 2H2O, Akademie der Wissenschaften, Leipzig, Germany), diluted with tapwater to 0.075 l, was taken orally. Background urine sample was taken immediately before isotope administration. Another urine sample for measurement of isotope enrichment was taken from the second voiding, 4 h after dose administration. Isotope abundances in urine were determined in duplicate with an isotope-ratio mass spectrometer(Aqua-Sira, VG Isogas Ltd, Cheshire, UK). TBW was calculated as described by Schoeller et al. (32), using a correction for 40 g·kg-1 nonaquaeous dilution.

TBMC was determined using a DXA total-body scanner (model DPX, Lunar Radiation Corp., Madison, WI), using the “medium speed” (80 mm·s-1) mode and resolution (pixel size) 4.8 · 9.6 mm2. The scan time was approximately 25 min. TBMC was calculated from the scan data by Lunar software 1.3z. The scanner was calibrated daily.

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Resting Energy Expenditure and Description of Dance Training

Resting energy expenditure (REE) was measured in the morning, after a 10-h fast, with a ventilated-hood (indirect calorimetry) system. During the measurement, the dancer was watching a movie in a semirecumbant position with constantly ventilated canopy on her head. ˙VO2, ˙VCO2, ventilation and respiratory exchange ratio, integrated over 1-min periods, were measured (Servomex, Crowborough, Sussex, UK) for 45 min. The first 15 min were excluded from the analyses. Using the formula of Weir(38), energy expenditure (EE, kJ·min-1) was calculated for the last two 15-min periods. The lower of these two values was used as REE. Both the O2 and CO2 analyzers were calibrated before and after each measurement.

All dancers kept a prospective training diary on seven sequential days. The kind and amount of dance training was recorded to the nearest quarter of an hour.

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Dietary Intake and Eating Disorders

All dancers kept a 7-d dietary record on the same days as the dance training record. Participants were given both oral and written instructions on how to fill in records with exact descriptions and amounts of all foods consumed. Amounts were measured using household measures (glasses, cups, tablespoons, slices, etc.) or grams. All records were checked by one of the authors (R.O.). The reported dietary intakes were calculated by Becel® microcomputer program, version 1994 (Unilever Research Laboratorium, Vlaardingen, The Netherlands). The main part of the food composition data has been obtained from Dutch food analyses (18).

Behavioral and cognitive dimensions characteristic of eating disorders(preoccupation with weight and appearance) was assessed by the 64-item Eating Disorders Inventory (EDI) (13). Of eight subscales, the first three (drive for thinness, bulimia, and body dissatisfaction) assess attitudes and behaviors related to eating and body shape. The remaining five subscales (interpersonal distrust, perfectionism, interoceptive awareness, maturity fears, and ineffectiveness) measure aspects of eating disorders' psychopathology. The dancers were also interviewed orally about their eating and weight-control behaviors.

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Statistical Analyses

Pearson product moment correlations (BMDP statistical software, 3D program) were used to test simple associations between the number of menstrual cycles per year, age at the start of dancing, menarcheal age and present age. Age of menarche, age at the start of dancing, and present age (as independent variables), and the number of menstrual cycles per year (as the dependent variable), were also entered in a linear stepwise regression (2R program). The data of 5 amenorrheic and 10 eumenorrheic dancers, in the laboratory phase, were compared by Mann-Whitney's U-test (3D program). Group results are expressed as mean values, standard deviations (SD) and ranges. P< 0.05 in a two-sided test was accepted as the level of significance.

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The mean age of 113 participants in the screening phase was 23.3 yr (SD 4.8, range: 16-42). They started dancing ballet at an age of 8.1 yr (SD 4.1, 10-20). The mean age of menarche was 14.2 yr (SD 1.7, 10-20). The students were younger (20.5 yr, SD 2.8, 16-26, vs 25.5 yr, SD 4.8, 17-42; Student'st-test: P = 0.0001), but the rest of the above characteristics were not different between ballet students and company dancers.

The contraceptive pill was presently used by 50 dancers (44%) and intrauterine device (coil) by 2 (2%). The prevalence of amenorrhea was assessed among those 61 dancers (39 from companies, 22 from schools), who were not on oral or intrauterine contraception. The frequency distribution of their menstrual status is shown in Figure 1. Eight dancers (5 professionals, 3 students, pooled prevalence: 13.1%, 95% confidence interval: 5.3-20.9) had no more than four yearly cycles during the past 12 months. Two(aged 16 and 20 yr) had primary amenorrhea (no menstruation before the age of 16 yr), and six (prevalence: 9.8%, 95% confidence interval: 2.4-17.2) met the criteria of secondary amenorrhea (≤4 cycles during the previous 12 months, no menstruation for the previous 3 months). There was a moderate, but significant, correlation (r = -0.46, P = 0.001) between the age of menarche and the number of yearly cycles (Fig. 2). The regression equation between these two variables was: MENS = 21.7 - 0.82·MENA (r2 = 0.21; SEE 3.20), in which MENS = number of cycles during the past 12 months and MENA = age of menarche. Age at the start of dancing and age did not correlate (P > 0.05) with the number of menstrual cycles and these variables did not enter the stepwise regression.

Five of the 24 dancers volunteering for the laboratory phase had secondary amenorrhea (83% out of all dancers with secondary amenorrhea). Also the two dancers originally classified as primary amenorrhea participated, but both had menstruated ≤1 month before the laboratory investigations. The remaining 17 dancers had 9-13 cycles during the previous 12 months. Results on the above 24 dancers' body composition, energy expenditure, dietary intake, and indices of eating disorders (EDI scores) are shown in Table 1. The participants' body fat, expressed as percent of their body weight, was 18.3%. The proportion of water and bone minerals in the fat free mass (FFM) was 71.0% and 5.7%, respectively.

The dancers spent, on average, 4.2 h·d-1 (29.4 h·wk-1) in different dancing activities. However, the reported energy intake (EI) was only 16% above REE (6.50 vs 5.59 MJ·d-1). The number of dancers with total EDI scores ≤19, 20-39, or ≥40 were 7, 11, and 6, respectively. The sum of the three subscales related to eating and body shape (drive for thinness, bulimia, and body dissatisfaction) correlated positively with total EDI scores (r = 0.90, P < 0.0001), and with weight (r = 0.48, P = 0.02), but not with BF% (r = 0.03, P= 0.90). The correlation between total EDI score and weight did not quite reach significance (r = 0.40, P = 0.054).

Three of five amenorrheic dancers had late menarche, that is, at the age of 16 yr (Fig. 3). However, no statistically significant differences were found between amenorrheic and eumenorrheic dancers with regard to menarcheal age, body composition, body weight or weight fluctuation, age at start of dance training, present training volume, energy intake, or EDI scores.

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In the Netherlands, the prevalence of secondary amenorrhea among ballet dancers not on oral contraceptives was 9.8%. The prevalence was lower than previously reported in U.S. dancers(2,4,5,16), although varying definitions of amenorrhea make comparisons somewhat uncertain. A rather high proportion(44%) of the present dancers used oral contraception. The reason for current oral contraceptive use (i.e., for birth control or for previous history of irregular menstruation) was not questioned in the study. Consequently, one could argue that use of oral contraception may have been primarily due to menstrual disorders and bias the estimation of the prevalence of amenorrhea resulting in lower prevalence. However, users of oral or intrauterine contraceptives were eliminated because the same exclusion criterion was also used in previous studies on athletic amenorrhea(2,10,17,27,30).

In comparison with the mean menarcheal age of the general population in the U.S. and Northern Europe (12.5-12.9 yr)(2,10,29,35), ballet dancers start menstruating later, that is, at a mean age of 13.7-15.4 yr(2,5,10,14,16,35). In the present study, infrequent menstruation, including amenorrhea, was associated with late menarche, agreeing with the results of Sandborn et al.(30).

An explanation for the association between delayed menarche and later amenorrhea is difficult to conceive. It is likely that a third factor (e.g., genetic inheritance) links the two above mentioned. Among the present participants, age at the start of dancing was not associated with the age of menarche. However, because our questionnaire gave no information on training intensity before puberty, the possibility that strenuous premenarcheal training had an effect on maturation and later menstrual function(25) could not be excluded.

Athletic amenorrhea has been shown to associate with lower bone mineral density in the lumbar spine as well as generalized decrease in bone mineral density (7,25,41). It is possible that a combination of late menarche and secondary amenorrhea might be even more serious for bone health. This question warrants more attention.

In two studies with UWW or DXA assessments(4,41), the mean BF% in American dancers was 15.7%-16.9%, that is, comparable to the result found in the present 24 dancers. Elite ballet dancers in the study of Stensland and Sobal(34) began dancing at the age of 8.3 yr and they reported dancing 4.5 h·d-1. Both results were similar to those obtained from ballet dancers in the Netherlands.

The reported EI of the present dancers was very low. However, two groups from the U.S. (11,15) reported even lower EI (mean results: 5.3-5.4 MJ·d-1), while two others(1,5) found higher EI (7.0-7.9 MJ·d-1). The present dancers did not show energy conservation by decreased REE, agreeing with the results of Wilmore et al. (39). In fact, the measured REE was about 10% higher than the mean REE predicted from the regression equation (28): REE = 1807 + 70.3·FFM + 19.6·FM = 5004 kJ·d-1 Recent studies using the doubly labeled water technique have strongly suggested that lean, athletic, women underreport their EI and/or undereat during food recording(8,31). Low reported EI seems to be associated with weight consciousness and body dissatisfaction(8,33). This apparent methodological bias should be remembered when interpreting the above “low” intakes

Although most of the variables described in the present dancers were not evidently different from results reported in the U.S., higher EDI scores in American dancers (mean results: 38.8-40.2) (12,19) may indicate a stronger tendency toward disordered eating. This could be related to a more rigid emphasis on leanness and dieting, and more severe competition among dancers in the U.S. The lack of anonymity (between the subjects and the authors) might also have contributed to lower EDI scores in the present dancers.

The small number of amenorrheic cases limited the information obtained from the cases versus controls-comparison. A tendency for late menarche corroborated with our findings in the field phase. In the present study, special attention was paid for careful body composition measurements. To the best of our knowledge, this is the first comparison of amenorrheic and eumenorrheic dancers' body composition with a 4-compartment model. The model corrects for variation in TBMC and TBW that might influence comparisons between physically active females with varying menstrual status(7,25). Nevertheless, even the four-compartment model was in agreement with the general view of similar body composition in amenorrheic and eumenorrheic dancers or athletes(7,17,20,24,25,27,30,33,39). Moreover, a “critical body fatness”, as originally suggested by Frisch and McArthur (9), was not found in the present study.

In summary, in the Netherlands, the prevalence of secondary amenorrhea among ballet dancers not on oral contraceptives was 9.8%. An explanation for the apparently lower prevalence of amenorrhea, compared with U.S. ballet dancers, was not obvious. Rather low EDI scores could be related to less rigid emphasis on leanness and dieting. Later menarcheal age was associated with a decreased number of yearly menstrual cycles. These conclusions should be viewed against the main limitations: 1) comparison of true prevalence of amenorrhea is difficult due to the different definitions of amenorrhea; 2) oral contraceptive use may have been due to prior menstrual dysfunction, limiting the studies conclusions; 3) past history of menstrual dysfunction and reason for current oral contraceptive use should have been one of the variables assessed on the questionnaire to clarify these confounding factors.

Figure 1-The frequency distribution of menstrual status (number of yearly cycles) in 61 ballet dancers not using oral or intrauterine contraception.

Figure 1-The frequency distribution of menstrual status (number of yearly cycles) in 61 ballet dancers not using oral or intrauterine contraception.

Figure 2-Regression between the age of menarche (yr) and the number of yearly menstrual cycles in 61 ballet dancers.

Figure 2-Regression between the age of menarche (yr) and the number of yearly menstrual cycles in 61 ballet dancers.

Figure 3-Individual data of five amenorrheic and 10 eumenorrheic ballet dancers' menarcheal age, body fat percentage, body weight, body weight variation during the previous 12 months, age at the start of dancing, present dance training, dietary energy intake, and Eating Disorders Inventory scores.

Figure 3-Individual data of five amenorrheic and 10 eumenorrheic ballet dancers' menarcheal age, body fat percentage, body weight, body weight variation during the previous 12 months, age at the start of dancing, present dance training, dietary energy intake, and Eating Disorders Inventory scores.

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