help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sundgot-Borgen, J.
Right arrow Articles by Schneider, L. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sundgot-Borgen, J.
Right arrow Articles by Schneider, L. S.
The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 9 3144-3149
Copyright © 1998 by The Endocrine Society

Original Studies

Normal Bone Mass in Bulimic Women

J. Sundgot-Borgen, R. Bahr, J. A. Falch and L. Sundgot Schneider

Address all correspondence and requests for reprints to: Jorunn Sundgot-Borgen, Ph.D., University of Sport and Physical Education, P.O. Box 4014, Ullevål Hageby, 0806 Oslo, Norway. E-mail: jorunn{at}brage.idrettshs.no


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The aim of this study was to examine the relationship among exercise, menstrual function, and bone mineral density (BMD) in different groups of age-matched patients with eating disorders. Dieting and eating disorder history, physical activity history, and menstrual history were assessed by clinical interview in 43 bulimic and 13 anorectic young women as well as in 17 healthy control subjects (18–29 yr). BMD was assessed by dual x-ray absorptiometry. All the anorectics but only 30% of the bulimics exercised regularly from the onset of their eating disorder (P < 0.01), mainly using aerobic dancing and running. All of the anorectics had been amenorrheic since the start of their symptoms, and 68% of the bulimics had a history of menstrual dysfunction. Within the exercise subgroups of bulimic patients, there was no significant relationship between BMD and current or previous menstrual function. Anorectic patients had lower BMD than bulimics and controls in all skeletal regions studied (P < 0.01). Bulimic patients who had exercised regularly during their illness had higher total body BMD than bulimics classified as sedentary (P < 0.01). Bulimics who had exercised regularly or intermittently since the onset of their eating disorder had higher BMD than sedentary bulimics in the lumbar vertebrae, femoral neck, and legs (P < 0.05). It appears that weight-bearing exercise can prevent or attenuate bone loss at specific skeletal sites in normal weight bulimic patients, but not in anorectics.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
DIETING, like exercise, has become part of our contemporary culture. These activities alter energy balance by controlling the energy consumed in food and expended through exercise. They can act synergistically, creating an anorectic cycle consisting of severe dietary restriction and an intense commitment to an exercise regimen (1). Exercise has been defined as a trigger mechanism for the development of anorexia nervosa (2) and as a significant feature of and perpetuating factor for eating disorders (1). Excessive exercise has also been described as a purging technique in bulimic patients (1).

A number of studies have shown that healthy athletes have better than average bone mass, and that exercise increases bone mineral density (BMD) (3, 4, 5, 6, 7, 8). On the other hand, amenorrheic athletes have been shown to have vertebral BMD values 9–31% lower than those of eumenorrheic women (7). Lloyd et al. (6) found that collegiate athletes who missed more than 50% of their expected menses had vertebral densities that were 69% those of normally menstruating athletes. Rutherford (7) also found a significantly lower lumbar and total spine BMD in amenorrheic vs. eumenorrheic athletes, but these two groups did not differ in total body BMD.

Amenorrhea is one of the diagnostic criteria for anorexia nervosa, but it is not a diagnostic criterion for bulimia nervosa (1). However, menstrual irregularities are described in about 50% of women with bulimia nervosa (9).

Many anorectic patients have asymptomatic osteopenia, and some develop fractures (10, 11, 12, 13, 14, 15). However, results of the effects of exercise on bone mass in anorectic patients are conflicting. Rigotti et al. (14) reported that anorectics who were highly active had greater radial cortical bone density than those who were less active. Joyce et al. (13) found in their anorectic patients that moderate exercise was protective, whereas strenuous exercise was detrimental to bone mass. Bachrach et al. (16, 10) and Kooh et al. (17) reported no relationship between bone mass and exercise in their anorectic patients. The discrepancy between these studies could be explained by a lack of control for exercise history, training volume, and type of training.

There is little information available on changes in BMD in subgroups of patients with eating disorders (18). The division of anorexia nervosa into food-restricting and bulimic subtypes, and the proposed division of bulimia into subgroups have been accepted in the fourth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) (1). Just as the psychiatric course of the illness differs between subgroups of eating disorders, so may the medical complications, such as a reduced bone mass. Therefore, the aims of this study were to examine BMD and to examine the association among exercise, menstrual function, and BMD in different groups of patients with eating disorders.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
This study took place in three phases: 1) an initial screening by questionnaire, 2) a detailed clinical interview, and 3) a medical examination, including measurement of peak oxygen consumption, percent fat tissue, and BMD. In addition to the Eating Disorder Inventory (19), a questionnaire was developed to assess weight history, menstrual history, physical activity history, dietary history, nutritional habits, and frequency of bingeing and purging (20).

Physicians and psychologists in private practice and psychiatric out-patient clinics in the Oslo area were invited by letter to refer eating disorder patients to the study. Patients who met the DSM-IV criteria for anorexia nervosa (without a history of bulimia) or bulimia nervosa (without a history of anorexia nervosa), who had no other psychiatric or somatic disorders that could have triggered the eating disorder, who had not been receiving treatment for eating disorders during the last 6 months, who did not use any medication, who were motivated for treatment, and who were between 18–29 yr of age were potential subjects.

Fourteen of the 70 patients referred did not meet the inclusion criteria and were therefore not included in the study. The reason for excluding these patients were history of other eating disorders (n = 4), additional personality disorders (n = 3), use of medication (including birth control pills; n = 5), and involvement in treatment during the last 6 months (n = 2). In all, 56 patients (13 anorectic and 43 bulimic) were included in the study.

The need for a control group in this study was announced at an information board at the University of Oslo. The following inclusion criteria were listed in this announcement: eumenorrhea, regular participation in weight-bearing exercise (1–2 h/week) in addition to the mandatory 2–3 h/week of the mandatory physical education lesions from age 7–18 yr, no history of somatic or psychiatric disorders, no use of medication (including birth control pills), and willingness to complete a dietary registration, a fitness test, a medical exam, clinical interviews, and measurement of bone mass and tissue fat. Twenty-five signed up for the study, but 8 were excluded due to symptoms of eating disorders (n = 3), menstrual irregularities (n = 2), vegetarian dietary habits (n = 2), and competitive running (n = 1). Thus, 17 healthy females were included in the control group. These students matched the patients by age and the body weight of the bulimics (Table 1Go). No attempt was made to find students who could match the anorectic patients in weight.


View this table:
[in this window]
[in a new window]
  		Table 1. Characteristics of the three subject groups: anorectic patients, bulimic patients, and control subjects

 
Permission to undertake the study was provided by the Data Inspectorate and the regional ethical committee of the Norwegian Research Council. All subjects gave their written informed consent to participate in the study.

Interview and clinical examination

All patients and controls underwent a clinical examination, including an interview and physical examination. Body weight and height were recorded with subjects wearing underwear and no shoes. Body mass index (BMI) was calculated as the body weight (kilograms) divided by the squared height (meters).

The interview protocol was developed as part of the Diagnostic Survey for Eating Disorders (21) and has been described previously (20). DSM-IV criteria (1) were used to define anorexia nervosa and bulimia nervosa. For consistency, each examination or interview was conducted by the same researcher.

Menstrual dysfunction

The subjects were classified according to their menstrual history (menstrual function during the period since developing an eating disorder) and menstrual status (the number of cycles during the last 12 months). Eumenorrhea was defined as menstrual cycles of less than 35 days, but longer than 23 days (22). Menstrual dysfunction was defined as secondary amenorrhea (lack of more than three consecutive cycles) or oligomenorrhea (menstrual cycles of between 35–90 days).

Assessment of previous and present physical activity

Previous physical activity pattern (since onset of symptoms) and present training volume (including the average number of training hours per week during the last 12 months) were assessed by a self-report questionnaire followed by an interview to improve accuracy. The questionnaire included information on all activities common for children, teenagers, and young adults in Norway. Questions about frequency and regularity (in addition to the mandatory physical education lessons) from age 12 yr were included.

For part of the analysis the subjects were divided into 3 different groups depending on their reported degree of exercise regularity since the onset of their eating disorder (except for the last 6 months): regular, intermittent, and sedentary. Regular exercise was defined as weight-bearing aerobic exercise for at least 2 h/week. Intermittent was defined as more or less regular weight-bearing exercise (never exercising regularly for >2 months). The sedentary group included those who did not exercise during their illness. Six of 18 subjects in the sedentary group had not participated in mandatory physical education lesions since the onset of symptoms.

Fitness assessment

Aerobic capacities were expected to vary widely. Therefore, peak oxygen uptake was assessed using a walking test. A modified Balke protocol (23) was used. The major modifications were as follows: the participants warmed up for 10 min, and the inclination of the treadmill was increased every minute, not every second minute. The test was terminated when the participants were close to exhaustion according to the Borg scale (>18) or when the oxygen uptake leveled off and the respiratory exchange ratio was above 1.05.

BMD and fat mass tissue assessment

BMD and soft tissue composition of the total body and major subregions were measured with dual energy x-ray absorptiometry (DXA; Lunar DPX-l, Lunar, Madison, WI). For the purpose of this study, the BMD values of the lumbar vertebrae (L2–L4), femoral neck, and total body were measured. From the total body scans, the BMDs of the arms and legs could be evaluated separately. Fat mass as a percentage of total body mass was calculated from the total body scans. In our laboratory, the reproducibility of the DXA measurements were as follows: L2–L4, 1.0%; femoral neck, 2.5%; total body, 0.7%; and percent fat, 1.9%. The reproducibility was estimated by scanning 25 middle-aged women twice within 2 weeks.

Statistical analysis

All analyses were performed using SPSS software (SPSS, Evanston, IL). Differences between more than two groups were determined by one-way ANOVA (Kruskal-Wallis) and Student’s t test between pairs of groups for continuous ordinal variables. Pearson’s correlation test was employed to determine the association between continuous variables. All tests were two tailed. Contingency table were used to test for association between categorical variables. Stepwise linear regression was used to determine how the dependent (response) variable (BMD) changed as a function of the independent (explanatory) variables: duration of eating disorders, body weight, BMI, peak oxygen uptake, tissue fat, menstrual history, and exercise history. P < 0.05 was considered statistically significant. Results are presented as the mean and SD unless otherwise noted.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The anorectic group had lower weight, BMI, percent ideal body weight, and percent tissue fat than bulimic patients and controls (Table 1Go). No difference was observed when body weight (P = 0.74), BMI (P = 0.22), percent ideal body weight (P = 0.17), or tissue fat (P = 0.70) was compared between bulimics and controls or when bulimic groups with different exercise histories (regular, intermittent, or sedentary) were compared using the same variables (body weight, P = 0.93; BMI, P = 0.99; percent of ideal body weight, P = 0.15; tissue fat, P = 0.06). The bulimic patients reported a mean weight loss of 1.1 kg (0.5–3.6 kg) after onset of symptoms.

Physical exercise

Sixty-six percent of the eating disorder patients and 61% of the controls were physically active in addition to mandatory physical education classes before the age of symptom debut (mean, 16 yr; range, 13–21 yr). There was no difference between the regularly exercising, intermittent, and sedentary bulimic groups with respect to physical activity before developing symptoms of eating disorders. After onset of symptoms, a significantly higher proportion of anorectic patients exercised on a regular basis, had a higher current training volume, and had a higher peak oxygen uptake than the bulimic and control groups (Table 2Go).


View this table:
[in this window]
[in a new window]
  		Table 2. Exercise history, current training volume, and peak oxygen uptake for the three subject groups: anorectic patients, bulimic patients, and control subjects

 
In the bulimic group, no significant differences in present training volume or peak oxygen uptake were observed among the regular exercise group (n = 13; 3.5 ± 3.6 h/week; 46.4 ± 6.5) L/kg·min), the intermittent group (n = 12; 2.0 ± 1.6 h/week; 44.2 ± 6.9 L/kg·min), and the sedentary group (n = 18; 1.9 ± 2.7 h/week; 40.2 ± 5.5 L/kg·min). Results from the questionnaire and the clinical interview revealed that 93% of the subjects included in the regular exercise group reported the same degree of regularity and training volume in the questionnaire and the clinical interview, 63% of the subjects in the intermittent group overreported both the degree of regularity and training volume, and 89% of those in the inactive group defined themselves as inactive. The correlations between present training volume and peak oxygen consumption were r = 0.67, r = 0.62, and r = 0.54 for the regular, intermittent, and sedentary groups, respectively. The main activities reported were aerobic dancing and jogging.

Menstrual history and status

All anorexia nervosa patients had been amenorrheic since the start of their eating disorders. A history of menstrual irregularity was reported by 68% of the bulimic patients (14 amenorrheic and 16 oligomenorrheic), and 74% (15 amenorrheic and 17 oligomenorrheic) reported menstrual irregularities within the last 12 months. In the bulimic group, the menstrual histories of the different bulimic groups were as follows: regular exercisers, 6 amenorheic, 6 oligomenorrheic, and 1 eumenorheic; intermittent exercisers, 5 amenorheic, 2 oligomenorrheic, and 5 eumenorheic; and sedentary, 3 amenorheic, 8 oligomenorrheic, and 7 eumenorheic. None of the controls had a history of menstrual dysfunction.

BMD

BMD was significantly lower in the anorectic group compared with the those in the bulimic and control groups for all regions examined, including total body BMD (P < 0.01; Table 3Go).


View this table:
[in this window]
[in a new window]
  		Table 3. Mineral density (grams per cm2) in females with anorexia nervosa, bulimia nervosa, and healthy controls

 
No differences in BMD were observed between the bulimic group and the control group for total body BMD or any of the regions examined. Regularly and intermittent exercising bulimics and healthy controls had higher BMD than sedentary bulimics (P < 0.01) in the lumbar spine, femoral neck, and legs, whereas total body BMD values were different between controls and sedentary bulimics only (P < 0.01). Regularly exercising bulimics had higher lumbar values than intermittent exercisers, healthy controls, and sedentary bulimics (P < 0.05; Fig. 1Go). Total body BMD was lower when the anorectic group was compared with the three subgroups of bulimic patients (Fig. 1Go).



View larger version (43K):
[in this window]
[in a new window]
  		Figure 1. Regional BMD values in different groups: sedentary bulimics (sb), cyclic exercisers (cb), regular exercisers (rb), anorectics (a), and controls (c). BMDs in four regions (total BMD, lumbar vertebrae L2–L4, femoral neck, and legs and arms) in relation to training history are shown. Anorectic patients are shown as filled bars (all regular exercisers), and bulimic patients as hatched bars. The bulimic patients have been separated into three groups according to their exercise habits during the symptomatic period (regular exercisers, intermittent exercisers, and a sedentary group). Controls (mixed exercise history) are shown separately with open bars. The mean and SD are shown. The value of the group represented in each bar is significantly different from the abbreviation(s) on top.

 
Within each subgroup of bulimic patients, there appeared to be no relationship between BMD and menstrual function in any of the skeletal regions examined. As an example, the lumbar values for all bulimic patients are shown in Fig. 2Go.



View larger version (34K):
[in this window]
[in a new window]
  		Figure 2. Bulimic patients have been separated into three groups according to their menstrual histories during the symptomatic period (eumenorrheic, oligomenorrheic, or amenorrheic). Values are given as the mean and SD.

 
Bulimic patients who had L2–L4 BMD values below 80%, 80% or greater, less than 90%, between 90–100%, and 100% or greater of healthy control values were compared for tissue fat (percentage), degree of regularity in training history, history of menstrual dysfunction, average number of training hours over the last year, and number of menstrual cycles during the last year (Table 4Go).


View this table:
[in this window]
[in a new window]
  		Table 4. The percentage of tissue fat, training history, training volume, menstrual history, and number of menstrual cycles in patients with bulimi nervosa representing groups with different BMD lumbar values

 
An overall difference in tissue fat, training history, and training volume was observed. No difference in body weight or eating disorder history was observed.

In the univariate correlation analysis for the bulimic group, an association was found between lumbar BMD and exercise history, peak oxygen uptake, BMI, tissue fat, and menstrual dysfunction (P < 0.01–0.05). After adjusting for correlation between explanatory variables, only exercise history, peak oxygen consumption, BMI, and tissue fat were associated with lumbar BMD (P < 0.01–0.05; Table 5Go). Of the total variance, 86% could be explained by these variables. The same trend was found for the other skeletal regions studied.


View this table:
[in this window]
[in a new window]
  		Table 5. Explanatory variables for lumbar bone mineral density for the bulimic group

 
For the anorectic and control groups, only tissue fat was associated with lumbar BMD. In these two groups, 34% and 45% could be explained by the tissue fat.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The main findings of the present study were that 1) BMD was significantly different in subgroups of eating disordered patients; 2) anorectic patients, all of them regular exercisers, had lower BMD values for all regions studied compared with bulimic patients and controls with a mixed exercise background; 3) bulimics who had been exercising during their illness had higher BMD values in weight-bearing regions than sedentary bulimics regardless of menstrual function; and 4) bulimics with the highest lumbar value had a higher number of training hours during the last year, a higher degree of regularity in their exercise history, and a higher percentage of tissue fat than bulimics with lower L2–L4 BMD.

It should be noted that although the anorectics in our study had been excessive exercisers since the onset of the eating disorder, 9 of 13 anorectics had BMD values more than 2.5 SD below control values, which corresponds to the WHO’s definition of osteoporosis. The anorectic group had lumbar BMD values that were 65% of control values and significantly lower values than bulimics and controls in all regions studied; there was no trend toward higher values in weight-bearing regions. This supports other recent studies with amenorrheic athletes, indicating that the deficit appears to be generalized throughout the skeleton (24, 25, 26).

Rigotti et al. (14) reported that anorectics who were highly active had greater radial cortical bone density than those who were less active. Furthermore, Joyce et al. (13) studied groups of anorectics who also exercised at various levels (<1 to >6 h/week). All of their subjects demonstrated a significant decreased vertebral BMD compared with normal values. In contrast to the results from Rigotti’s study (14), the results from our study show that anorectics are not able to maintain normal bone mass even if they exercise regularly. Therefore, the combination of a high volume of exercise combined with malnutrition, abnormal cortisol secretion (27), and estrogen deficiency (13) may explain the decrease in BMD in these subjects.

As expected, bulimic patients who were defined as intermittent exercisers overreported both the degree of regularity and the number of training hours per week. Bulimic patients who did not exercise regularly or were sedentary seem to follow their bulimic eating pattern (28). This overreport of exercise should be kept in mind for those treating bulimic patients. The relatively low correlation between peak oxygen uptake and the reported hours of exercise per week could be explained by differences in genetics, training methods, and nutritional status (29). In addition, the average time since onset of symptoms for the bulimic patients was 5.7 (3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14) yr, indicating that some of these patients were too exhausted to keep the intensity needed to maintain or enhance their aerobic capacities.

Bulimics who had been exercising regularly or periodically since acquiring the eating disorder had higher lumbar spine BMD than sedentary bulimics and anorectic patients in weight-bearing skeletal sites. However, there was no difference in arm BMD between exercisers and nonexercisers. The difference observed in the effects of exercise on BMD between bulimic and anorectic patients could be explained by the suggestion made by Koch et al. (17) that nutritional deprivation may have a more deleterious effect on bone than either the duration of amenorrhea or the serum levels of sex hormones.

The eating disorder patients in this study who had been performing aerobic dancing and jogging more or less regularly during the eating disorder history may have benefited from the mechanical stress placed on the different weight-bearing skeletal regions measured (lumbar spine, femural neck, and legs). It is therefore not surprising that there was no exercise effect for arm BMD. The DXA method used for determining BMD in this study averages BMD for the entire extremity. It may be that differences would have been found if specific sites in the lower leg had been examined as well. This is supported by the finding that the bulimic patients with the highest L2–L4 BMD values had the highest degree of regularity in their exercise history and the highest number of training hours per week. Furthermore, the groups with the higher BMD values also had higher percentages of fat tissue.

In contrast to previous findings indicating that trabecular bone is not protected by exercise (6, 7, 12, 13, 30), results from this study indicate that there is an exercise effect for bulimic patients. Therefore, it may be that hormonal imbalance is not the major factor explaining reduced bone mass in sedentary bulimic patients. As anorectics and bulimic patients both have menstrual dysfunction, it is tempting to argue that the energy intake and contents plays significant roles. Although menstrual dysfunction was associated with bone mass, it was not one of the variables in the multiple regression model explaining reduced bone mass in the bulimic groups.

Most researchers (2, 6, 19) report that prior menstrual history is the best predictor of current BMD and that women with a history of amenorrhea have lower BMD than those who have always been cyclic. On the other hand, it has been reported that not all physically active females suffering from menstrual dysfunction have low bone mass (4, 5, 31). Their skeletal status depends upon the length and severity of the menstrual irregularity as well as factors that influence their BMD before the onset of menstrual dysfunction: type of skeletal loading during activity, nutritional status, and genetic components (5).

The established difference in energy and nutrient intake between active anorectic and bulimic patients (28) could partly explain why exercising bulimics, in contrast to the anorexics, may experience the positive effect of weight-bearing exercise (aerobic dancing and jogging) on bone mass.

It is interesting to note that there appeared to be no difference in BMD within the different exercise subgroups of bulimic patients when they were separated based on menstrual function or history. Again, more data are needed to determine whether mechanical stress and weight-bearing exercise can effectively prevent or attenuate bone loss at specific skeletal sites in normal weight, eating disorder patients with menstrual dysfunction. More research is needed in many areas related to women, exercise, nutrition, and bone mass. Prospective longitudinal studies should include females at different ages, with diverse activity histories (type and volume), representing the total spectrum of weight, eating disorders, and menstrual function.

Received September 18, 1997.

Revised May 12, 1998.

Accepted May 19, 1998.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. American Psychiatric Association. 1994 Diagnostic and statistical manual of mental disorders, 4th ed. Washington DC: American Psychiatric Association.
  2. Epling WF, Pierce WD, Stefan A. 1983 A theory of activity based anorexia. Int J Eating Disord. 3:27–46.
  3. Davee AM, Rosen CJ, Adler RA. 1990 Exercise pattern and trabecular bone density in college women. J Bone Miner Res. 5:245–260.[Medline]
  4. Drinkwater BL, Bruemner B, Chesnut CH. 1990 Menstrual history as a determinant of current bone density in young athletes. JAMA. 263:545–548.[Abstract/Free Full Text]
  5. Drinkwater BL, Nilson K, Chesnut CH, Bremner WJ, Shainholtz S, Southworth MB. 1984 Bone mineral content of amenorrheic and uemenorrheic athletes. N Engl J Med. 311:277–281.[Abstract]
  6. Lloyd T, Myers C, Buchanan JR, Demers LM. 1988 Collegiate women athletes with irregular menses during adolescence have decreased bone density. Obstet Gynecol. 72:639–642.[Medline]
  7. Rutherford OM. 1993 Spine and total body bone mineral density in amenorrheic endurance athletes. J Appl Phys. 74:2904–2908.[Abstract/Free Full Text]
  8. Teegarden D, Proulx WR, Kern M, et al. 1996 Previous physical activity relates to bone mineral measures in young women. Med Sci Sports Exerc. 28:105–113.[Medline]
  9. Pirke K, Schweiger M, Laersle U, Dickhaut R. 1986 Dieting influences the menstrual cycle: vegetarian vs. nonvegetarian diet. Fertil Steril. 46:1083–1088.[Medline]
  10. Bachrach LK, Katzmann DK, Litt IF, Gudo D. 1991 Recovery from osteopenia in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab. 72:602–606.[Abstract/Free Full Text]
  11. Biller BW, Saxe V, Herzog DB, Rosenthal DI, Holzman S, Klibanski A. 1989 Mechanisms of osteoporosis in adult and adolescent women with anorexia nervosa. J Clin Endocrin Metab. 68:548–554.[Abstract/Free Full Text]
  12. Cann CE, Martin MC, Genant HK, Jaffe RB. 1984 Decreased spinal mineral content in amenorrheic women. JAMA. 251:626–629.[Abstract/Free Full Text]
  13. Joyce JM, Warren DL, Humphries LL, Smith AJ, Coon JS. 1990 Osteoporosis in women with eating disorders. Comparison of physical parameters, exercise, and menstrual status with SPA and DPA evaluation. J Nucl Med. 31:325–331.[Abstract/Free Full Text]
  14. Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR. 1991 The clinical course of osteoporosis in anorexia nervosa: a longitudinal study of cortical bone mass. JAMA. 265:1133–1138.[Abstract/Free Full Text]
  15. Treasure J, Fogelman I, Russell GFM. 1986 Osteopenia of the lumbar spine and femoral neck in anorexia nervosa. Scott Med J. 31:206–207.[Medline]
  16. Bachrach LK, Guido D, Katzman D, Litt IF, Marcus R. 1990 Decreased bone density in adolescent girls with anorexia nervosa. Pediatrics. 86:440–447.[Abstract/Free Full Text]
  17. Koch SW, Noriega E, Leslie K, Muller C, Harrison JE. 1996 Bone mass and soft tissue composition in adolescents with anorexia nervosa. Bone. 19:181–188.[Medline]
  18. Andersen AE, Woodward PJ, France MLA. 1995 Bone mineral density of eating disorder subgroups. Int J Eating Disord. 18:335–342.[Medline]
  19. Garner DM, Olmsetd MP, Polivy J. 1984 Manual of eating disorder inventory. Odessa, FL: Psychological Assessments Resources; 2–18.
  20. Sundgot-Borgen J. 1993 Prevalence of eating disorders in elite female athletes. Int J Sport Nutr. 3:29–40.[Medline]
  21. Johnson C. 1985 Initial consultation for patients with bulimia nervosa and anorexia nervosa. In: Garner DM, Garfinkel PE, eds. Handbook of psychotherapy of anorexia nervosa and bulimia. New Yourk: Guildford Press; 19–54.
  22. Rippon C Nash J, Myburgh KH. 1988 Abnormal eating attitude test scores predict menstrual dysfunction in lean females. Int J Eating Disord. 7:617–624.[CrossRef]
  23. Balke B. 1954 Optimale Korperliche Leistungsfahigkeit, ihre Messung und Veranderung infolge Arbeitsermudung. Arbeidsphysiologie. 15:311–323.
  24. Myburg KH, Bachrach LK, Lewis B, Kent K, Marcus R. 1993 Bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Exerc. 25:1197–1202.
  25. Rencken MB, Drinkwater L, Chestnut III CH. 1993 Decreased bone density in the lower extremity of amenorrheic athletes. J Bone Miner Res. 8(Suppl 1):S254.
  26. Rencken MB, Chesnut CH, Drinkwater BL. 1996 Bone density at multiple skeletal sites in amenorrheic athletes. JAMA. 276:238–240.[Abstract/Free Full Text]
  27. Gold PW, Gwirtswan H, Avgerinos PC.1986 Abnormal hypothalamic-pituitary-adrenal function in anorexia nervosa. N Engl J Med. 314:1335–1342.
  28. Sundgot-Borgen J. 1993 Nutrient intake of female elite athletes suffering from eating disorders. Int J Sport Nutr. 3:431–442.[Medline]
  29. McArdle WD, Katch FI, Katch VI. 1991 Body composition, energibalance, and weight control. Philadelphia: Lea and Febiger; 599–740.
  30. Ott SM. 1991 Methods of determining bone mass. J Bone Miner Res. 6(Suppl 2): 571–576.
  31. Kirchner EM, Lewis RD, O’Connor P. 1996 Effects of past gymnastics participation on adult bone mass. J Appl Physiol. 80:226–232.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Br. J. Sports. Med.Home page
J. Sundgot-Borgen and M. K. Torstveit
The female football player, disordered eating, menstrual function and bone health
Br. J. Sports Med., August 1, 2007; 41(suppl_1): i68 - i72.
[Abstract] [Full Text] [PDF]

Home page
 Eur J EndocrinolHome page
S. Naessen, K. Carlstrom, R. Glant, H. Jacobsson, and A. L. Hirschberg
Bone mineral density in bulimic women - influence of endocrine factors and previous anorexia.
Eur. J. Endocrinol., August 1, 2006; 155(2): 245 - 251.
[Abstract] [Full Text] [PDF]

Home page
 Family and Consumer Sciences Research JournalHome page
J. M. Beiseigel and S. M. Nickols-Richardson
Anthropometrics, Bone Mineral Density, and Dietary Intake in a Group of Young Adult Females
Family and Consumer Sciences Research Journal, March 1, 2002; 30(3): 404 - 423.
[Abstract] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
S. Zipfel, M. J. Seibel, B. Lowe, P. J. Beumont, C. Kasperk, and W. Herzog
Osteoporosis in Eating Disorders: A Follow-Up Study of Patients with Anorexia and Bulimia Nervosa
J. Clin. Endocrinol. Metab., November 1, 2001; 86(11): 5227 - 5233.
[Abstract] [Full Text] [PDF]

Home page
 QJMHome page
T.M. O'CONNOR, D.J. O'HALLORAN, and F. SHANAHAN
The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia
QJM, June 1, 2000; 93(6): 323 - 333.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sundgot-Borgen, J.
Right arrow Articles by Schneider, L. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sundgot-Borgen, J.
Right arrow Articles by Schneider, L. S.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals