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ORIGINAL RESEARCH COMMUNICATION |
1 From the Department of Exercise and Nutritional Science, San Diego State University, San Diego, CA (MTB, MJR, H-SB, and JFN), and the Graduate Program in Orthopaedic and Sports Physical Therapy, Rocky Mountain University of Health Professions, Provo, UT (MJR)
2 Supported by grants from the National Athletic Trainers Association and the San Diego State University, Department of Exercise and Nutritional Sciences Fred Kasch Endowment. 3 Reprints not available. Address correspondence to MT Barrack, School of Exercise and Nutritional Sciences, San Diego State University, San Diego, CA 92182-7251. E-mail: michellebarrack{at}gmail.com.
| ABSTRACT |
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Objective: We aimed to determine the relation between Eating Disorder Examination Questionnaire (EDE-Q) subscale scores, pathologic behaviors, MI, and low BMD in adolescent female runners.
Design: Participants were 93 female competitive cross-country runners 13–18 y old. The EDE-Q, composed of subscales for weight concern, shape concern, eating concern, and dietary restraint, was used to assess DE. Menstrual history was determined by using a questionnaire derived from a medical history form administered before participation in high school athletics. The International Society for Clinical Densitometry and the World Health Organization criterion of
–2 or
–1 SD, respectively, was used to categorize runners as having low BMD.
Results: Runners with elevated restraint had a significantly (P < 0.001) greater incidence of low BMD than did runners with elevated weight and shape concern. After adjustment for possible confounding variables (including menstrual history), lumbar spine BMD, bone mineral content, and BMD z score values were lowest in runners with elevated restraint. In addition, total-body BMD and total-body BMD z scores were significantly (P < 0.05) lower in runners with elevated restraint than in those with elevated weight or shape concern. Elevated EDE-Q scores for weight or shape concern, pathologic behaviors, or any combination of the 3 without concurrent dietary restraint were not significantly associated with low bone mass.
Conclusion: These findings suggest that, in adolescent female runners, dietary restraint may be the DE behavior most associated with negative bone health effects.
Key Words: Adolescent female runners eating disorder examination questionnaire eating attitudes and behaviors disordered eating menstrual irregularity
| INTRODUCTION |
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Subclinical abnormal eating attitudes and behaviors have primarily been assessed in athletes and nonathletes with the use of the Eating Disorder Inventory, the Eating Attitudes Test–26 (EAT-26), the Eating Disorder Examination Questionnaire (EDE-Q), the Bulimia Inventory Test Edinburgh, and the Three Factor Eating Questionnaire (TFEQ). Among endurance runners, elevated Eating Disorder Inventory (9), EAT-26 (10), and EDE-Q (11) values have been associated with menstrual irregularity (MI), whereas elevated Bulimia Inventory Test Edinburgh scores have not shown a relation with MI (10). In young adult nonathletes, elevated TFEQ scores have been associated with menstrual disturbances in 2 studies (12, 13), but another report (14) did not observe this relation. In adolescent athletes, one study reported a higher EDE-Q restraint and global score in oligomenorrheic or amenorrheic athletes with DE than in eumenorrheic athletes with DE (15), but another assessment did not observe an association between elevated EAT-26 values and menstrual function (16).
Equally diverging reports have emerged from studies assessing DE and bone mass. In female collegiate and postcollegiate elite athletes, elevated Eating Disorder Inventory values have been associated with lower spine bone mineral density (BMD) values in eumenorrheic but not oligomenorrheic or amenorrheic subjects (9). In young adult women, elevated TFEQ scores predicted lower total-body BMD and bone mineral content (BMC) values after adjustment for height, weight, and exercise (14), whereas 2 studies of a similar population did not observe a relation between elevated TFEQ values and low BMD (17, 18). In one study of adolescent athletes, elevated EDE-Q values were not significantly associated with lower total-body or lumbar spine BMD or BMD z scores (15); however, another assessment of adolescent nonathletes observed a relation between high oral control, measured by the children's EAT-26 scores, and low BMC (19).
These disparities may be partially related to the use of various questionnaires or certain subscales of each questionnaire, which may target different DE attitudes or behaviors. The comparison of different DE behaviors may become problematic, because each behavior may vary in its effect on energy availability, hormone concentrations, and stress levels. It seems necessary, then, to identify the DE attitudes or behaviors that are most associated with negative menstrual and bone health effects. Observing high school runners may be particularly relevant, because few studies have concurrently assessed DE and low BMD in adolescents, long-distance running has been associated with a greater risk of MI and low BMD (9, 10, 20-22), and adolescents are in a period of rapid bone mineral accrual (23, 24). Therefore, our purpose was to examine the associations among various DE attitudes and behaviors, MI, and low BMD in adolescent female competitive cross-country runners.
| SUBJECTS AND METHODS |
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Parental written informed consent and subject assent were obtained after a study orientation session held before team practice during the third week of the track season. The study was approved by the Institutional Review Board of San Diego State University.
Data collection
The runners completed questionnaires regarding menstrual history and eating behaviors. For each 6–8 runners, 1 research assistant reviewed the EDE-Q response scale and, for questions deemed more difficult to interpret, defined terminology—eg, binge episode—and then remained in the room to assist runners who requested further clarification as they individually completed the questionnaires. Two to 4 wk after the administration of the questionnaire, the subjects underwent a dual-energy X-ray absorptiometric scan [(DXA) Lunar DPX-NT densitometer; Lunar/GE Corp, Madison, WI] to measure BMD. Before scanning, height and weight were measured while the subjects were barefoot. Data from runners who reported taking any medications known to affect bone mass were excluded from analysis.
Eating attitudes and behaviors
At the end of the first month of the cross-country season, each runner completed the EDE-Q, a self-report questionnaire composed of 4 subscales (ie, weight concern, shape concern, eating concern, and dietary restraint); the global score is the composite mean score of the 4 subscales (3). The EDE-Q is considered the gold standard for assessment of DE because of the instrument's internal consistency (25), reliability, temporal stability, and investigator-based design (3). This DE measure has been validated in clinical, adult, and adolescent populations (4, 25, 26) and has been reported to have high test-retest and interrater reliability in adolescent athletes (15). A mean cutoff of
3.0 was used to categorize runners as having an elevated value for each subscale. We chose this cutoff because it indicated that a specific attitude or behavior was reported on
14 of the previous 28 d and because it corresponded with the highest 6–18% of scores for each subscale. The numbers of runners with elevated scores for 0, 1, 2, or 3 subscales of the EDE-Q are shown in Table 1
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2 of the previous 28 d. We identified binge eating as the consumption of an unusually large amount of food and a loss of control over eating. Excessive exercise was recognized as exercise in addition to practice or competition that was performed with the sole intention of controlling one's weight or shape. Vomiting was considered pathologic if it was self-induced as a means to control weight or shape (or both).
We divided the runners into 3 groups according to their EGE-Q responses: 1) normal EDE-Q, which included runners who did not report any elevated subscale scores or pathologic behaviors (n = 67); 2) elevated weight or shape concern but not elevated restraint (n = 13); and 3) elevated dietary restraint, which included runners also reporting elevated weight or shape concern (n = 5). We also reported the descriptive and bone mass values for runners with normal EDE-Q subscale scores but
1 pathologic behavior (n = 8). Weight and shape concern referred to an excessive fear of gaining weight or becoming fat, exhibiting an abnormal preoccupation with food or allowing shape or weight to influence one's self-worth (27, 28). Dietary restraint described the intent to limit calorie intake, whether or not the effort was successful (3). We grouped together runners who reported only elevated weight or shape concern, because these subscales identified similar constructs, were frequently reported together, and described athletes with similar descriptive traits. In assessing BMD z scores of runners reporting pathologic behaviors, we grouped runners admitting pathologic behaviors and elevated EDE-Q subscale scores (n = 5) with runners reporting pathologic behaviors and normal EDE-Q subscale scores (n = 8), because we did not identify differences in BMD z scores between these groups.
Menstrual status
After the administration of the EDE-Q, the runners completed a menstrual status and history questionnaire, which was derived from a medical history form required for participation in high school athletics (29). The criteria for classifying athletes with MI were primary amenorrhea (no onset of menarche by age 15 y), secondary amenorrhea (absence of 3 consecutive menstrual cycles in the past year), or oligomenorrhea (cycle length < 21 or > 35 d in the past year) (2, 30). Runners who met any of the above criteria were combined into a single (oligomenorrheic or amenorrheic) group and compared with runners who had normal menses (eumenorrheic).
Bone measures
We assessed areal BMD (g·cm–2) and BMC (g) at the spine (L1–L4), proximal femur, and total body and assessed body composition (percentage fat and lean tissue mass) by using DXA. Quality assurance tests were performed each morning of testing. The CVs in BMD in our laboratory are 0.6% for the total hip, 1.2% for the spine (L1–L4), and 0.99% for total body.
We used the criteria of the World Health Organization (WHO; 31) and International Society for Clinical Densitometry (ISCD; 32) to define low bone mass. Runners were categorized as having low BMD if their values at the spine or total body were
1 SD (WHO criterion) or
2 SD (ISCD criterion) below the age-matched, sex-specific reference data from the pediatric GE/Lunar database (z score:
–1 or
–2, respectively). At the time of data collection, z scores for the hip were not available for children.
Statistical analysis
We used analysis of variance (ANOVA) with Bonferroni correction to determine mean differences for physical and performance characteristics between EDE-Q groups. After we split our sample by menstrual status, we conducted Pearson's partial correlations between each EDE-Q subscale and total-body, total hip, and lumbar spine BMD. Using Fisher's r-to-z transformation, we converted r values to z values and used a z test to compare the correlation coefficients between runners with normal menses (NM) and MI. ANOVA and analysis of covariance with Bonferroni correction were used to assess BMD z score differences between runners reporting binge eating and excessive exercise and runners who reported no pathologic behaviors. ANOVA and analysis of covariance with Bonferroni correction were used to assess mean differences in BMD, BMC, and BMD z scores among 4 groups of runners: those with a normal EDE-Q, elevated weight or shape concern values, elevated restraint scores, or no elevated subscale but a reported pathologic behavior. Chi-square tests were used to identify associations between our EDE-Q subscale groups and the incidence of MI, low BMD, and pathologic behaviors. The data were analyzed with the use of SPSS software (version 12.0; SPSS Inc, Chicago, IL).
| RESULTS |
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Descriptive traits
Compared with runners who had a normal EDE-Q, runners who had elevated weight or shape concern had significantly (P < 0.05) higher BMIs, body weight, and percentage body fat, and they reported running significantly (P < 0.05) fewer miles per week during the track season and over the previous 3 summer months (Table 2
). In addition, runners with elevated weight or shape concern ran significantly (P < 0.05) fewer miles per week during the current cross-country season than did those with elevated dietary restraint (Table 2
).
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3) eating concern scores. This runner had elevated scores for each subscale, admitted self-induced vomiting, reported only one menstrual cycle in the past year, and had lumbar spine and total-body BMD z scores of –3.5 and –2.1, respectively. These observations may warrant further assessment of the relation between the eating concern EDE-Q subscale and MI or low BMD. | DISCUSSION |
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Dietary restraint
To our knowledge, this report is the first documentation of reduced BMD, BMC, and BMD z score values in adolescent runners with elevated dietary restraint. Whereas some studies have not confirmed this finding in adults (17, 33), others have recognized a similar relation between dietary restraint and low BMC or BMD in premenopausal women (14, 34). Another report recognized an association between elevated restraint and stress fracture incidence in adult female runners (35), whereas still another identified reduced bone turnover in young adults reporting elevated restraint (18).
Because BMI, body weight, and percentage body fat values varied among EDE-Q groups, and because we observed that menstrual function interacted with the relation between abnormal eating attitudes and behaviors and BMD, we adjusted, in our bone mass analyses, for BMI, lean tissue mass, chronological age (except in z score assessments), gynecological age, and the number of menstrual cycles in the past year. Therefore, our findings suggest that dietary restraint has a negative effect on BMD and BMC independent of other factors known to affect bone mass, particularly at the lumbar spine, in adolescent female competitive cross-country runners.
Consequently, it does not appear that clinical menstrual irregularity was associated with the low BMD in our sample of high school runners with elevated dietary restraint. Consistent with our findings, previous research studies also reported a negative association between dietary restraint and bone health, independent of menstrual irregularity (14, 18, 35). Thus, subclinical menstrual disturbances not associated with an abnormal cycle length, such as luteal phase disturbances or anovulatory cycles, may have occurred in our runners with elevated restraint. Supporting this claim are previous reports of a greater prevalence of anovulatory cycles and shortened luteal length in women with high dietary restraint scores than in those with low scores (13, 17). In addition, as we found in the high school runners with elevated restraint who were enrolled in the present study, women with subclinical menstrual disturbances have been shown to exhibit bone loss (36). Therefore, it appears reasonable to speculate that our sample of high school runners with elevated restraint concurrently had subclinical menstrual abnormalities that may have negatively affected bone mass.
Other factors also may have accounted for the low bone mass we observed in these high school runners with dietary restraint. Previous studies reported higher urinary and salivary concentrations of cortisol in young women with elevated dietary restraint (14, 37), and excess cortisol negatively affects bone formation, bone resorption, calcium absorption, and calcium excretion (14, 37, 38); therefore, elevated cortisol may have contributed to this low bone mass. In addition, it is recognized that a certain threshold of low energy availability alters luteinizing hormone pulsatility, reduces markers of bone deposition, and increases markers of bone resorption (39, 40). Therefore, low energy availability may have also contributed to the low bone mass in these runners. This hypothesis is particularly convincing because restrained eaters attempt to restrict food intake and because long-distance running is a highly energy-demanding sport. However, dietary restraint is the intent to limit food intake (3), and a person's attempts to restrict food may not always be successful. The fact that this sample of runners reporting restraint did not have low body weight, BMI, percentage body fat, or lean tissue mass may suggest that their energy availability did not differ from that of the other EDE-Q groups.
Weight or shape concern
Runners who reported elevated weight or shape concern had higher BMI, body weight, and percentage body fat than did runners with normal EDE-Q scores. Previous research studies also reported higher body mass and percentage body fat values in endurance runners and adolescent nonathletes with DE (9, 15, 41, 42). It has been suggested that girls who have average or slightly above-average weight may be most sensitive to the social pressure to obtain a thin body type, and that lean girls may not practice unhealthy weight-control behaviors, given that they already fit the society's ideal body type (42). This observation appears consistent with our findings, because these high school runners with elevated weight and shape concern were heavier than the other members of the cohort, and they also had the greatest prevalence of pathologic binge eating. Runners with elevated weight and shape concern subscale scores also reported running fewer miles per week during the current season and over the previous 3 summer months. Consequently, runners with elevated weight and shape concerns may be less likely to exhibit low energy availability than would runners with a normal EDE-Q, which is a possible explanation for the lower prevalence of low BMD in the runners in the present study who had elevated weight and shape concerns.
Weight or shape concern, dietary restraint, and pathologic behaviors
In terms of bone health, the concurrent presence of weight or shape concern and dietary restraint appeared to be associated with negative bone health effects more than were weight or shape concern and pathologic behaviors such as binge eating. However, the combination of weight or shape concern, restraint, and pathologic behavior seemed to be the most detrimental combination—the one runner who fit this profile had an extremely low lumbar spine BMD z score of –3.5. The higher total-body and lumbar spine BMD z scores in runners reporting binge eating may be due to the tendency of these girls to consume large quantities of food during a given period of time. This behavior, especially if practiced frequently, may reduce their risk of developing a chronic energy deficit and the resulting decrease in bone deposition or increase in bone resorption (39).
Limitations
Despite our efforts to maximize understanding of the questionnaire and to ensure the confidentiality of the participant (given the self-reporting nature of the EDE-Q), some runners may have presented inaccurate responses. Furthermore, given the cross-sectional design of our study and the relatively small number of runners with elevated EDE-Q subscale scores or pathologic behaviors (or both), longitudinal studies assessing a larger sample may be more beneficial in understanding each DE attitude and behavior and its relation with menstrual function and bone mass.
Conclusions
Although runners with elevated weight and shape concerns, elevated dietary restraint, and pathologic behaviors displayed abnormal eating attitudes and behaviors, dietary restraint appeared to be the DE behavior most associated with low bone mass. It is interesting that the dietary restraint–associated negative bone health effects occurred independently of other factors known to affect BMD. Future studies assessing luteal phase length, ovulation, cortisol, energy availability, and relevant hormones in adolescent endurance runners may prove beneficial in identifying the factors that are associated with low bone mass in persons with dietary restraint. Because our dietary restraint assessment consisted of only 5 questions, the EDE-Q restraint subscale may be useful in clinical and other athletic research settings.
| ACKNOWLEDGMENTS |
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The authors' responsibilities were as follows: MTB, JFN, MJR, and H-SB: study design; MTB, JFN, and MJR: subject recruitment and management; MTB, H-SB, and JFN: data collection and data entry; MTB: data analysis and writing of the manuscript; and JFN and MJR: review and editing of the manuscript. None of the authors had personal or financial conflicts of interest.
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