A patient referred to the eating disorders clinic has lost 35 pounds in 3 months

J Gen Intern Med. 2000 Aug; 15(8): 577–590.

The Role of the Primary Care Physician

Abstract

OBJECTIVE

To describe how primary care clinicians can detect an eating disorder and identify and manage the associated medical complications.

DESIGN

A review of literature from 1994 to 1999 identified by a medlinesearch on epidemiology, diagnosis, and therapy of eating disorders, including anorexia nervosa and bulimia nervosa.

MEASUREMENTS AND MAIN RESULTS

Detection requires awareness of risk factors for, and symptoms and signs of, anorexia nervosa (e.g., participation in activities valuing thinness, family history of an eating disorder, amenorrhea, lanugo hair) and bulimia nervosa (e.g., unsuccessful attempts at weight loss, history of childhood sexual abuse, family history of depression, erosion of tooth enamel from vomiting, partoid gland swelling, and gastroesophageal reflux). Providers must also remain alert for disordered eating in female athletes (the female athlete triad) and disordered eating in diabetics. Treatment requires a multidisciplinary team including a primary care practitioner, nutritionist, and mental health professional. The role of the primary care practitioner is to help determine the need for hospitalization and to manage medical complications (e.g., arrhythmias, refeeding syndrome, osteoporosis, and electrolyte abnormalities such as hypokalemia).

CONCLUSION

Primary care providers have an important role in detecting and managing eating disorders.

Keywords: eating disorders, primary care, medical complications

Eating disorders are common in young women. Although the evaluation and treatment of eating disorders has typically been thought to be the realm of the psychiatrist, the primary care physician plays an important role. In the era of managed care, the primary care physician may be the first to detect an eating disorder and is responsible for coordinating care, including management of complications and determining the need for hospitalization. In addition, a patient may need to see a primary care physician first in order to be referred to a mental health clinician. The primary care physician must work with a multidisciplinary team, including a nutritionist and a mental health specialist to provide well-integrated care for patients with eating disorders. Finally, particularly for those patients who have milder forms of disordered eating and may not be seeing a mental health specialist regularly, the primary care physician may have primary responsibility for ongoing care and for management of complications. The following questions will be addressed in this review: What signs and symptoms should lead the primary care physician to suspect an eating disorder? Are there high risk groups at particular risk for eating disorders? What laboratory tests should be part of the evaluation of a patient with a suspected eating disorder? What are common medical complications among patients with eating disorders? What are the data on current treatments for patients with eating disorders?

METHODS

Three authors did a medline search on epidemiology, diagnosis, and therapy of eating disorders, anorexia nervosa, bulimia nervosa, and disordered eating. Search terms included anorexia nervosa, bulimia nervosa, disordered eating, and female athlete triad. Other search terms included eating disorders (anorexia nervosa and bulimia nervosa) and epidemiology, eating disorders (anorexia nervosa and bulimia nervosa) and detection or screening, eating disorders (anorexia nervosa and bulimia nervosa) and medical complications, eating disorders (anorexia nervosa and bulimia nervosa) and treatment or therapy, eating disorders (anorexia nervosa and bulimia nervosa) and osteoporosis, and disordered eating and diabetes. When assessing treatment modalities, we specifically sought randomized clinical trials when available.

We confined our search to the English literature. We also reviewed the bibliographies of retrieved articles to find articles which had not been previously identified by the medline search. The medline search focused on 1994 to 1999; significant earlier articles identified through bibliographic searches were also included.

EPIDEMIOLOGY

The DSM-IV diagnostic criteria for anorexia nervosa and bulimia nervosa are listed in Table 1. New features of the DSM-IV criteria are that both anorexia nervosa and bulimia nervosa have restricting and binge eating/purging subtypes.

Table 1

Eating Disorder Definitions

Anorexia Nervosa

The majority (95%) of patients with anorexia nervosa are female. The prevalence of anorexia nervosa has been estimated to be about 1% in adolescent girls, although it may be subclinical in up to 10% of young women aged 16 to 25. Although anorexia nervosa is typically considered a disease of Caucasians, eating disorders and body dissatisfaction seem to be common in African-American, Asian, and Hispanic populations as well.1–3 Other risk factors for anorexia nervosa include being a middle- to upper-class female, participation in activities valuing thinness (e.g., ballet, gymnastics, modeling), and a family history of an eating disorder. An episode of anorexia nervosa is typically precipitated by a stressful situation.4 Anorexia nervosa may be associated with other psychiatric diagnoses, including an estimated 25% lifetime prevalence of obsessive compulsive disorder and a 50% to 75% prevalence of dysthymia.5 About 40% to 45% of anorectics recover completely, 30% improve, and 25% have a chronic course. The mortality rate is about 10% to 15%, the highest of any psychiatric disorder. Causes of death include starvation, suicide, and medical complications. Mortality is increased in those with a late age of onset, long duration of illness, and severe weight loss.4 Overall, a poorer prognosis is associated with lower initial weight, disturbed family relationships, being male, the presence of vomiting, longer duration of symptoms or failure to respond to earlier treatment.6,7

Bulimia Nervosa

The estimated prevalence of bulimia nervosa is 3% to 10% of adolescent and college age women in the United States; however, because bulimics look healthier, the disease can be harder to detect. Bulimia typically begins after an unsuccessful attempt at weight loss or when the patient discovers that purging, fasting, and exercise can compensate for bingeing. Factors associated with developing bulimia include a history of childhood or sexual abuse, a history of psychoactive substance abuse or dependence, and a family history of alcoholism or depression.4,7–9 Depression and mood disorders are common in bulimics. The prognosis in bulimia is generally better than with anorexia: more than 50% recover, and few become anorectic. About 30% maintain a “nonspecified eating disorder.” Of those who recover, 25% retain some abnormal eating habits. Factors associated with an increased mortality rate in bulimia include both premorbid and paternal obesity.9

Many patients identified by the primary care physician may not meet full DSM criteria for a diagnosis of anorexia or bulimia nervosa, but will exhibit significantly disordered eating and exercise patterns, including either restrictive and/or binge eating with or without purging behaviors (eating disorder not otherwise specified). When identified in the younger patient, this may represent milder disease, which is more difficult to detect, but in which the outcome is likely to be better; conversely, in the older patient, it may represent the chronic sequelae of partial recovery from a full-blown eating disorder. In this latter group, psychiatric and nutritional treatment options may have been exhausted, and the primary care physician will be responsible for monitoring the course of a chronic illness.

Other high risk groups include female athletes (see Female Athlete Triad in Table 1) and diabetics. It has been estimated that the prevalence of disordered eating in athletes ranges from 15% to 62%.10,11 Up to one third of young women with insulin-dependent diabetes mellitus (IDDM) have eating disturbances.12,13 Patients with either of these syndromes also have medical complications that require treatment and monitoring by the primary care clinician.

DETECTION AND EVALUATION

Anorexia Nervosa

Since patients often do not present with a chief complaint of an eating disorder, the primary care physician must be alert to that possibility, particularly in young women. Low weight, progressive weight loss, or concern expressed by family members may also raise suspicion. Symptoms common in anorexia nervosa include amenorrhea, abdominal discomfort, bloating or constipation, and cold intolerance. When a clinician suspects anorexia nervosa, he/she should ask about previous weight and weight loss pattern, menstrual history, daytime hyperactivity and insomnia, and exercise habits. Two questions which may help in determining her eating habits include “What did you eat yesterday?” and “Do you ever binge eat (eat more than you want) or use laxatives, diuretics, or diet pills?” Attitude toward body weight or shape may be elicited by asking, “Do you think you are thin (too thin)?”

On physical examination, the patient may be hypotensive and bradycardic with significant orthostatic signs. The skin may be yellow, and lanugo hair may be present. Physical examination findings may include irregular cardiac rhythm and peripheral edema. Mitral valve prolapse is common in anorexia nervosa, as weight loss leads to a size disproportion between the left ventricle and the mitral valve. In one study, it was present in 37% of anorectics compared with 4% of controls.14 This prolapse does seem to be reversible with weight gain.15

Laboratory evaluation of the anorectic should include a complete blood count, electrolytes, magnesium, calcium, phosphorus, urea nitrogen, creatinine, glucose, and albumin. Measuring FSH, LH, TSH and prolactin can be helpful in evaluating the cause of the amenorrhea. An electrocardiogram is especially important in patients who are bingeing and purging, and who may have metabolic abnormalities. Bone densitometry should be considered to assess severity of bone loss, especially if the results will affect the treatment.

Bulimia Nervosa

Bulimia nervosa may be more difficult to detect than anorexia. Two questions which have been shown to be very sensitive when used in the primary care setting for the detection of bulimia nervosa are “Do you ever eat in secret?” and “How satisfied are you with your eating habits?”16 These screening questions can easily be included on initial history forms and as part of a routine health maintenance assessment. Another screening tool, the SCOFF questionnaire, was recently evaluated and may ultimately be useful in screening for eating disorders. The questions include the following: (1) Do you make yourself Sick because you feel uncomfortably full? (2) Do you worry you have lost Control over how much you eat? (3) Have you recently lost more that One stone (14 pounds) in a 3-month period)? and (4) Do you believe yourself to be Fat when others say you are too thin? Would you say Food dominates your life? In a group of 116 patients with eating disorders and 96 controls, the positive answer to 2 of the SCOFF questions had 100% sensitivity for detecting anorexia nervosa or bulimia nervosa and 87.5% specificity.17 This test has yet to be validated prospectively in a broader population.

Clinicians should also ask about previous maximum and minimum weight, menstrual history, exercise habits, use of alcohol or other drugs, and whether the patient ever binges, or uses laxatives, diuretics, or diet pills. Other factors associated with bulimia nervosa include a personal history of rape, sexual assault, childhood abuse, or depression. A family history of depression or alcohol abuse is also common.

On physical examination, the bulimic generally looks healthy. She may have erosion of teeth enamel and/or many fillings, due to vomiting. Other physical examination signs include parotid gland hypertrophy, hoarse voice due to gastroesophageal reflux, Russell's sign (hypertrophy of the knuckles from inducing vomiting), peripheral edema, and rectal prolapse or bleeding due to chronic constipation. Laboratory evaluation is essentially the same as for the anorectic, with careful attention to the binge- and purge-induced electrolyte abnormalities (hypokalemia, hypochloremic metabolic alkalosis).

The role of the primary care clinician is to identify patterns of disordered eating. More important for the primary care clinician than making the exact diagnosis (which can ultimately be made by the treating mental health professional) is management and treatment of the complications caused by the disordered eating.

TREATMENT ISSUES

General Treatment Issues

Treatment of the patient with an eating disorder should involve a multidisciplinary team, including the primary care physician, nutritionist, and a mental health professional, all of whom should communicate and confer regularly. The role of the primary care physician is to coordinate treatment, to manage the medical complications, and to help determine the need for inpatient hospitalization. If the patient is unwilling or unable to see a mental health professional or nutritionist, the role of the primary care physician is to monitor weight, nutritional intake, and physical condition, while using contract setting regarding weight and food intake as a tool to help the patient see the need for treatment.

The immediate treatment interventions for both anorexia and bulimia are aimed at nutritional normalization and recovery of normal eating patterns. The best early results occur with weight restoration and individual and family psychotherapy as soon as the patient is medically able to participate. Effective psychotherapy cannot occur when the patient is in a starvation mode.4

A trial of outpatient management is often a requirement of insurance companies.18 Day programs and outpatient treatment are most effective in the motivated patient; the multidisciplinary team establishes criteria at which outpatient treatment is no longer appropriate. These include failure to follow-up, a “basement” weight, continued weight loss or inadequate weight gain, number of binge/purge episodes, or specified laboratory values or physical signs. The patient and all members of the team must agree on the limits, which are shared in writing and then firmly applied. For patients who refuse therapy, the goal of medical or nutritional follow-up should be to help the patient realize the seriousness of the situation and to work with her to accept treatment and minimize medical danger. Food diaries, monitored by a nutritionist, are an essential part of treatment. Food diaries are used for 2 purposes: to assess nutritional adequacy (i.e., protein, calcium, iron, and fat) and to record all food eaten (including mood and physical sensations before and after eating). When a nutritionist is not available, review of food diaries for nutritional adequacy also becomes the responsibility of the primary care physician. For the anorectic, an exact record of food consumption enables the treating professionals to suggest changes that result in a slow, steady weight gain and improvement of food tolerance. For bulimics, food diaries can be an important part of cognitive behavioral therapy.

Anorexia Nervosa

In addition to the general principles described above, some specific management strategies are important for patients with anorexia nervosa. It is important for the primary care physician, along with the patient and other members of the team, to set a target weight. An appropriate target weight is often a weight at which the patient previously menstruated. The patients become very frightened about weight gain, so generally the weight gain should be very gradual, and does not usually exceed 1/2 to 1 pound per week. Anorectics should be weighed by the primary care provider at every visit, generally weekly, ideally at the same time of day. Weighing techniques include ensuring that the patient has an empty bladder, no shoes, and one layer of clothing, preferably an exam gown. If necessary, urine specific gravity can be assessed to detect water loading. Weights should be reported to the practitioner rather than through patient report. Patients may misrepresent weights in order to meet a contract weight or to avoid hospitalization. All patients should receive multivitamins with iron and calcium. Zinc supplementation at 50 mg daily (14 mg elemental zinc) is well tolerated and may facilitate weight gain and improve affective symptoms.19,20 Metoclopramide may be helpful if the patient complains of abdominal bloating. Cisapride was assessed in another study: although the cisapride group improved subjectively, there was no association between subjective improvement and gastric emptying.21

Contract setting, done in collaboration with the entire team, is important for patients with eating disorders. Components of the contract include indications for hospitalization; agreement to appropriate follow-up and to keep a food diary, an exercise log, and a record of purges, if indicated; and agreement that weight loss or failure to gain agreed upon weight would mandate more intensive treatment.

Assessment of food diaries by the nutritionist should include a review of nutritional adequacy, especially protein, fat, and calories; a demonstration of portion sizes; a review of intervals between eating; goal setting for foods to be added; and a review of emotional and physical hunger when eating. If the primary care physician is providing nutritional counseling, food models are available to demonstrate serving sizes to patients.

Determining the need for hospitalization is an important role for the primary care physician. Criteria for inpatient hospitalization include rapid progressive weight loss, weight loss of more than 30% of ideal body weight, arrhythmia or bradycardia, signs of inadequate cerebral perfusion, and lack of response to outpatient treatment.4

The medical complications of anorexia nervosa are listed in Table 2. Cardiac complications include arrhythmias and sudden death, related to QT prolongation and electrolyte abnormalities.22 The refeeding syndrome is cardiovascular collapse due to repletion of circulatory volume while left ventricular mass is still reduced. It is potentiated by hypokalemia, hypocalcemia, and hypomagnesemia. To avoid this, refeeding is best done orally and slowly with electrolyte monitoring. Dermatologic complications include dry skin, yellowing of the skin (carotenodermia),23 lanugo hair, and starvation-associated pruritis. Gastrointestinal complications include delayed gastric motility, constipation, and refeeding pancreatitis.24,25 There is an increased risk of infertility in patients with eating disorders, although whether a history of an eating disorder is a risk factor for infertility remains unclear.26 Pelvic ultrasound demonstrates reduced size of both ovaries and the uterus which reverses with weight gain and normalization of eating patterns.27–29 Endocrine abnormalities include thyroid abnormalities similar to euthyroid sick syndrome,30 hypercortisolemia,31 hypercholesterolemia due to impaired cholesterol metabolism,32 hypoglycemia, neurogenic diabetes insipidus,33 and impaired temperature regulation. Pancytopenia can occur due to starvation.34,35

Table 2

Medical Complications of Anorexia Nervosa

The most significant long-term complication is the increased risk of osteoporosis associated with amenorrhea. Anorectics have hypothalamic hypogonadism which leads to a hypoestrogenemic state, reflected by lack of withdrawal bleeding after a progesterone challenge. This hypoestrogenemic state is associated with low bone density. Although bone mineral density is lower in anorectics when compared with normal weight women, it is highest among those who are physically active, suggesting a protective effect of physical activity,36 although bone loss does occur even at those sites subjected to stress during exercise.37 Bone mineral density 2 standard deviations below normal occurs in 50% of anorectics and is associated with clinical fractures of multiple sites. In a 2-year prospective study, anorectics had an increased risk of fracture (relative risk, 7.0; 95% confidence level, 3.2 to 18.5) compared with normal weight women.38 Bone mineral density may increase after resumption of normal menses, but whether it returns to baseline is not known.39

In addition to weight gain and the resumption of normal menses, treatment options for low bone density include hormone therapy and the bisphosphonates. Although observational evidence suggests that women with anorexia nervosa or exercise-associated amenorrhea who take hormone replacement therapy or oral contraceptives have increased bone mineral density,40,41 evidence from clinical trials is scanty.

In 2 small clinical trials, anorectic women who took hormonal therapy had a greater increase in bone mineral density than those who did not; the effect was more marked in those with less than 70% ideal body weight. Although bone mineral density increased with hormone therapy, resumption of normal menses and recovery from anorexia nervosa had a more significant positive effect on bone density. Whether hormone replacement therapy or oral contraceptives are the superior treatment could not be determined from either study.42,43

Bisphosphonates have been studied for the prevention and treatment of osteoporosis in postmenopausal women,44–46 but have not been studied in anorectic women. Although their positive effects on bone mineral density may be beneficial, no data on their long-term use are available. Because younger amenorrheic women could potentially be taking this medication for many years, more information on their long-term effects is critical before they are used routinely in this group.

Estrogen replacement alone may not prevent progressive osteoporosis in anorectics. Although resumption of normal menses has a more profound effect on bone density than supplemental estrogen, it is probably reasonable to prescribe supplemental estrogen until adequate weight gain for normal menstruation occurs. The primary care physician must be careful that estrogen replacement does not falsely reassure the patient regarding her future risk of osteoporosis, thus slowing weight gain. Currently there is inadequate evidence to recommend either oral contraceptives or replacement-dose estrogen as the superior treatment. Whether or not a patient desires contraception, other noncontraceptive benefits and risks of oral contraceptives should be considered in the choice for each patient. In addition, all anorectic women should receive calcium supplementation.

Psychological Treatments

Abnormal eating behaviors in anorexia are often viewed as an attempt to gain and maintain control. Unlike bulimia nervosa, no single psychotherapeutic model as emerged as the standard of treatment. Both family therapy and individual therapy have been shown to be of benefit, with family therapy being most indicated in younger patients.47–51

Medications

In general, psychotropic medications have been less successful in anorexia nervosa than in bulimia. In one study, cryptoheptadine had some value.52 Few controlled studies on medications have been done, although many medications are used empirically. Several small studies of fluoxetine have not shown conclusive results.53–55 Anxiolytics can be helpful in treating the fear of loss of control, fear of weight gain and can be given before meals to reduce the anxiety associated with eating. Depression is often due to starvation and improves with the resumption of normal eating habits; if depression persists, antidepressants may be helpful.56,57

Bulimia Nervosa

The medical complications of bulimia nervosa are listed in Table 3. Several treatment issues are unique to patients who binge and purge.

Table 3

Medical Complications of Bulimia Nervosa

Gastrointestinal complications can occur at any part of the gastrointestinal tract from the mouth to the colon. Dental erosion from gastric acid may occur and may be irreversible.58,59 Brushing the teeth after a binge can worsen the problem, but rinsing with baking soda after vomiting seems to alleviate some of the acid-related complications. Parotid gland swelling can occur from repeated vomiting.60–62 Other gastroesophageal complications include reflux due to chronic relaxation of the sphincter and esophageal rupture from vomiting.63 Acute gastric dilitation and rupture is rare but is associated with a mortality rate of 80% when it occurs.64–66 Other gastrointestinal complications include postbinge pancreatitis and constipation due to laxative abuse.67 Cathartic colon with toxic degeneration of Auerbach's plexus due to overuse of stimulant laxatives can render the colon unable to perform normal peristalsis without large doses of laxatives.68,69 Pulmonary and mediastinal complications include aspiration pneumonitis and pneumomediastinum.70,71 Cardiac complications include arrhythmias due to electrolyte imbalances, palpitations and hypertension due to diet pills, and mitral valve prolapse. Emitene (ipecac syrup), which is designed for one-time use, has been associated with cardiomyopathy and death when used repeatedly to induce vomiting.72–74 Endocrine and metabolic complications include hypoglycemia and electrolyte imbalances, particularly hypokalemia. Dehydration leads to aldosterone-induced renal potassium losses, and sodium loss in the stool causes activation of renin-angiotensin resulting in sodium retention and loss of potassium. Finally, in a chronic low potassium environment, a kaliopenic nephropathy occurs when tubular dysfunction leads to decreased urine-concentrating ability. Vomiting leads to loss of hydrochloric acid and a metabolic alkalosis, whereas laxative abuse leads to a loss of bicarbonate and a metabolic acidosis.75–77 Bulimics also may have hypothalamic hypogonadism, even at normal weights. If a progesterone challenge does not lead to withdrawal bleeding, hypoestrogenism is present and is associated with low bone mineral density. Use of estrogen replacement is probably indicated until the binge-purge pattern is eliminated.

Goal setting is important in bulimia and is focused on elimination of binge/purge behaviors, normalization of eating patterns, and resumption of normal menses. Contract setting between the patient and all members of the treatment team includes agreement on monitoring interval; agreement to keep food, exercise, and binge/purge diaries; and agreement on what parameters will be followed and how frequently they will be followed. Although most bulimics can be managed as outpatients, advance discussion about what would mandate more intensive treatment (e.g., severe electrolyte imbalances, need for withdrawal from laxatives or diuretics) is appropriate and should be clearly specified in a written contract shared by the patient and all members of the team. Chronicity of symptoms is not rare. Relapse is more frequent in those who are more symptomatic at onset.

Criteria for inpatient hospitalization in bulimia include severe depression and suicidality; marked fluid and electrolyte imbalances; the need for withdrawal from laxatives, diuretics, emetics, or diet pills; and significant substance abuse.4

Psychological Treatment.

Cognitive behavioral therapy (Table 4)) has emerged as the most effective therapy for bulimia nervosa when compared to other psychological treatments and to medications (antidepressants).9,78–84 Nondepressed bulimics are generally treated first with cognitive behavioral therapy; medication is added if they continue to binge or purge. Walsh et al. compared cognitive behavioral therapy with psychodynamically oriented supportive psychotherapy and also assessed whether adding medication to cognitive behavioral therapy produced additional benefits. They found that cognitive behavioral therapy was superior to supportive psychotherapy in reducing the number of binge/purge episodes and in increasing the percentage of individuals becoming binge/purge free. Adding medication (either fluoxetine or imipramine) to cognitive behavioral therapy was superior to cognitive behavioral therapy alone.85 Several other studies have also suggested that combined treatment may have additional benefits.79,86,87 Two recent randomized trials suggest that self-care manuals can reduce the therapist contact hours required for cognitive behavioral therapy while achieving comparable efficacy.80,88

Table 4

Cognitive Behavioral Therapy*

Medications

Early studies suggested that imipramine was helpful in the treatment of bulimia nervosa.86,87 More recently, fluoxetine has emerged as an effective medication in bulimia nervosa. Two randomized trials support the superiority of fluoxetine over placebo, although the dose of fluoxetine which was effective (60 mg) was significantly higher than the dose typically used for depression (20 mg).89,90

Several investigators have noted a seasonal pattern among some bulimics, with distinct winter worsening of symptoms in 10% to 42% of individuals.91–93 Three small randomized, controlled trials have examined the effect of bright light therapy on bulimic symptoms. All the studies included small numbers of women and patients were generally not selected for the presence of seasonal symptoms. In one study, bright light of 10,000 lux for 30 minutes in the morning was superior to 500 lux of red light (placebo) on all measures of mood and eating outcomes.94 In another study, bright light–treated women bulimics noted improvement in depression scores but no significant change in bulimic symptoms,95 while a third study did note a significant decrease in bingeing.96

HIGH RISK GROUPS

Not all patients with patterns of disordered eating meet the criteria for a full-blown eating disorder. Patients with disordered eating patterns who do not meet eating disorder criteria are still at risk for complications. Two groups at particularly high risk are diabetics and female athletes.

Disordered Eating in Diabetics

Up to one third of women with IDDM have eating disturbances,12,13,97 and up to 40% of young patients with IDDM will have microvascular complications.98

In a recent prospective study, 91 women with IDDM were followed for 4 to 5 years and assessed for the presence of disordered eating, including binge eating, omission or underdosing of insulin to promote weight loss, self-induced vomiting, or use of laxatives. After 4 years of follow-up, 86% of women with highly disordered eating had retinopathy, compared with 43% and 24% of women with moderately or nondisordered eating, respectively. Despite the limitations of this study (no baseline measures of retinopathy, no interim assessments of glycemic control, and no measures of severity of retinopathy), the impaired metabolic control associated with disordered eating behavior in patients with IDDM does seem to be associated with an increased risk of diabetic retinopathy.99 Physicians should remain alert for patterns of disordered eating in patients with IDDM.

Female Athlete Triad

Many female athletes exhibit disordered eating patterns. Although these athletes may not meet criteria for anorexia nervosa or bulimia nervosa and typically do not have disturbances in body image, behaviors and complications similar to those seen in full-blown eating disorders are seen.

The female athlete triad (disordered eating, amenorrhea, and osteoporosis) was described initially in 1992.100 Disordered eating is described as a spectrum of abnormal patterns of eating, including bingeing, purging, food restriction, prolonged fasting, use of diet pills, diuretics, and laxatives, and other abnormal eating behaviors. Amenorrhea, both primary and secondary, is more common in women athletes than in their more sedentary peers. Osteoporosis occurs and is secondary to hypoestrogenism. Half of all amenorrheic athletes have bone densities at least 1 standard deviation below the mean. These athletes have an increased risk of stress fractures, and bone density may be decreased even in those sites subjected to impact loading during exercise. Some of this bone loss may be irreversible. The female athlete triad is more common in appearance- and endurance-based sports such as gymnastics, ballet, and long-distance running. It also seems to be more common in athletes who are training seriously and who have an overcontrolling parent or coach. Estimates of the prevalence of disordered eating in athletes range from 15% to 62%, and amenorrhea may occur in 3% to 66% of athletes. The prevalence of premature osteoporosis is not known.10,11

At present, there is little evidence regarding treatment of the female athlete triad. It is likely that strategies used for other eating disorders, such as counseling, cognitive behavioral therapy, and possibly exercise restriction, would be helpful. Open communication with coaches and trainers will enable common goal setting (e.g., weight at which exercise must be restricted). The desire to participate in sports and the lure of performance-enhancing diet may motivate some patients. Clinicians should maintain a high index of suspicion in all female athletes and should remain alert for the syndrome in young women who come in for a preperformance physical examination.

Eating Disorders in Males

Although eating disorders occur predominantly in females, they do occur in males. They tend to be more common in those who are gay or bisexual, and premorbid obesity is more common. There is an increased frequency in those in jobs where there is high pressure to be thin, such as acting or modeling. Men with eating disorders have a higher incidence of substance abuse than men who eat normally, and a family history of alcohol use or an affective disorder is more common. Of 135 males seen in an eating disorders clinic, 46% were bulimic, 22% were anorectic, and the rest had unspecified eating disorders.101

SUMMARY AND CONCLUSIONS

Eating disorders are common in young women of all ethnic groups, and clinicians must maintain a high index of suspicion. Primary care physicians must be able to detect eating disorders, determine the need for hospitalization, and manage the medical complications of eating disorders. The primary care physician is part of a multidisciplinary team including a nutritionist and a mental health professional. Common goal setting, open communication, and firm adherence to agreed-upon contracts are essential aspects of the team approach. Treatments for anorexia nervosa and bulimia nervosa are summarized in Table 5.

Table 5

Summary of Studies on Treatment of Anorexia Nervosa and Bulimia Nervosa*

Nutritional management based on food diaries includes indicated supplementation (iron, calcium, multivitamins) and assessment of both eating patterns and nutritional adequacy, especially protein, fat, and calories. Amenorrheic patients with eating disorders should receive estrogen therapy.

Psychotherapy is imperative for patients with eating disorders, although effective psychotherapy cannot occur while the patient is in a starvation mode. All patients with bulimia nervosa should receive some form of psychotherapy, preferably cognitive behavioral therapy. Individuals who continue to have difficulty with bulimic behaviors despite therapy or who are clinically depressed should be treated with selective serotonin reuptake inhibitors; fluoxetine has the most evidence. Light therapy may be considered, particularly in seasonal bulimics.

Diabetics are at risk for disordered eating, and disordered eating increases the risk of microvascular complications. Clinicians should maintain a high index of suspicion for disordered eating in female athletes. Finally, although eating disorders are more common in females, clinicians must remain alert for eating disorders in males.

REFERENCES

1. leGrange D, Telch CF, Tibbs J. Eating attitudes and behaviors in 1,435 South African Caucasian and non-Caucasian college students. Am J Psychiatry. 1998;155:250–4. [PubMed] [Google Scholar]

2. Field AE, Colditz GZ, Peterson KE. Racial/ethnic and gender differences in concern with weight and in bulimic behaviors among adolescents. Obes Res. 1997;5:447–54. [PubMed] [Google Scholar]

3. Robinson TN, Killen JD, Litt IF, et al. Ethnicity and body dissatisfaction: are Hispanic and Asian women at increased risk for eating disorders? J Adoles Health. 1996;19:384–93. [PubMed] [Google Scholar]

4. American Psychiatric Association. Practice Guidelines for Eating Disorders. Am J Psychiatry. 1993;150:2–28. [Google Scholar]

5. Halmi KA, Eckert E, Marchi P, Sampugnaro V, Apple R, Cohen J. Comorbidity of psychiatric diagnoses in anorexia nervosa. Arch Gen Psychiatry. 1991;48:712–8. [PubMed] [Google Scholar]

6. Eckert ED, Halmi KA, Marchi P, Grove W, Crosby R. Ten year follow-up of anorexia nervosa: clinical course and outcome. Psychol Med. 1995;25:143–55. [PubMed] [Google Scholar]

7. Comerci GD, Graydanus DE. Eating disorders: anorexia nervosa and bulimia. In: Hoffman ED, Graydanus DE, editors. Adolescent Medicine. Stamford, Conn: Appleton and Lange; 1997. [Google Scholar]

8. Bulik CM, Wullivan PF, Rorty M. Childhood sexual abuse in women with bulimia. J Clin Psych. 1989;50:460–4. [PubMed] [Google Scholar]

9. Fairburn CG, Agras WS, Wilson GT. The research on the treatment of bulimia nervosa: practical and theoretical implications. In: Anderson GH, Kennedy SH, editors. The Biology of Feast and Famine: Relevance to Eating Disorders. New York, NY: Academic Press; 1995. pp. 317–40. [Google Scholar]

10. Steen SN. The competitive athlete. In: Rickert VI, editor. Adolescent Nutrition: Assessment and Management. New York, NY: Chapman and Hall; 1996. pp. 223–47. [Google Scholar]

11. Tofler IR, Stryer BK, Micheli LJ. Physical and emotional problems of elite female gymnasts. N Engl J Med. 1996;335:281–3. [PubMed] [Google Scholar]

12. Rodin G, Craven J, Littlefield C, Murray M, Daneman D. Eating disorders and intentional insulin undertreatment in adolescent females with diabetes. Psychosomatics. 1991;32:171–6. [PubMed] [Google Scholar]

13. Steel JM, Young RJ, Lloyd GG, Clarke BF. Clinically apparent eating disorders in young diabetic women: associations with painful neuropathy and other complications. BMJ. 1987;294:859–62. [PMC free article] [PubMed] [Google Scholar]

14. Johnson GL, Humphries LL, Shirley PB, et al. Mitral valve prolapse in patients with anorexia nervosa and bulimia. Arch Intern Med. 1986;146:1525–9. [PubMed] [Google Scholar]

15. Meyers DG, Starke H, Pearson P, Wilken MK. Mitral valve prolapse in anorexia nervosa. Ann Intern Med. 1986;105:384–6. [PubMed] [Google Scholar]

16. Freund KM, Graham SM, Lesky LG, Moskowitz MA. Detection of bulimia in a primary care setting. J Gen Intern Med. 1993;8:243–8. [PubMed] [Google Scholar]

17. Morgan JF, Reid F, Lacey JH. The SCOFF questionnaire: assessment of a new screening tool for eating disorders. BMJ. 1999;319:1467–8. [PMC free article] [PubMed] [Google Scholar]

18. Sigman G. How has the care of eating disorder patients been altered and upset by payment and insurance issues? Let me count the ways. J Adolesc Health. 1996;19:317. [PubMed] [Google Scholar]

19. Katz RL, Keen CL, Hurley LS, Kellams-Harrison KM, Glader LJ. Zinc deficiency in anorexia nervosa. J Adolesc Health Care. 1987;8:400–6. [PubMed] [Google Scholar]

20. Birmingham CL, Goldner EM, Bakan R. Controlled trial of zinc supplementation in anorexia nervosa. Int J Eating Disord. 1994;15:251–5. [PubMed] [Google Scholar]

21. Szmuckler GI, Young GP, Miller G, Lichenstein M, Binns DS. A controlled trial of cisapride in anorexia nervosa. Int J Eating Disorders. 1995;17:347–57. [PubMed] [Google Scholar]

22. Isner JM, Roberts WC, Heymsfield SB, Yager J. Anorexia nervosa and sudden death. Ann Intern Med. 1985;102:49–52. [PubMed] [Google Scholar]

23. Bhanji S, Mattingly D. Anorexia nervosa: some observations on “dieters” and “vomiters.” Brit J Psych. 1981;139:238–41. [PubMed] [Google Scholar]

24. Rampling D. Acute pancreatitis in anorexia nervosa. Med J Aust. 1980;74:126–32. [Google Scholar]

25. Saleeh JW, Lebwohol P. Metoclopromide-induced gastric emptying in patients with anorexia nervosa. Amer J Gastroenterol. 1980;74:127–32. [PubMed] [Google Scholar]

26. Stewart DE, Robinson E, Goldbloom DS, Wright C. Infertility and eating disorders. Am J Obstet Gynecol. 1990;163:1196–9. [PubMed] [Google Scholar]

27. Sobanski E, Hiltmann WD, Blanz B, Klein M, Schmidt MH. Pelvic ultrasound scanning of the ovaries in adolescent anorectic patients at low weight and after weight recovery. Eur Child Adolesc Psychiatry. 1997;6:207–11. [PubMed] [Google Scholar]

28. Lai KY, de Bruyn R, Lask B, Bryant-Waugh R, Hankins M. Use of pelvic ultrasound to monitor ovarian and uterine maturity in childhood onset anorexia nervosa. Arch Dis Child. 1994;71:228–31. [PMC free article] [PubMed] [Google Scholar]

29. Treasure JL, Wheeler M, King EA, Gordon PA, Russell GF. Weight gain and reproductive function: ultrasonographic and endocrine features in anorexia nervosa. Clin Endocrinol. 1988;29:607–16. [PubMed] [Google Scholar]

30. Croyan MS, Ibbertson HK. Low serum T3 and hypothyroidism in anorexia nervosa. J Clin Endocrinol Metab. 1977;44:167–72. [PubMed] [Google Scholar]

31. Gold PW, Gwirtsman H, Avgerinow PC, et al. Abnormal hypothalamic-pituitary-adrenal function in anorexia nervosa: pathophysiologic mechanism in underweight and weight-corrected patients. N Engl J Med. 1986;314:1335–42. [PubMed] [Google Scholar]

32. Nestel PJ. Cholesterol metabolism in anorexia nervosa and hypercholesterolemia. J Clin Endocrinol Metab. 1979;38:325–9. [PubMed] [Google Scholar]

33. Gold P, Kaye W, Robertson GI, Ebert M. Abnormalities in plasma and CSF arginine vasopressin in patients with anorexia nervosa. N Engl J Med. 1983;308:1112–23. [PubMed] [Google Scholar]

34. Silverman JA. Anorexia nervosa: clinical observations in a successful treatment plan. J Pediatrics. 1974;84:68–73. [PubMed] [Google Scholar]

35. Reiger W, Brady JP, Weisberg E. Hematologic changes in anorexia nervosa. Am J Psychiatry. 1978;135:984–5. [PubMed] [Google Scholar]

36. Rigotti NA, Nussbaum SR, Herzog DB, Neer RM. Osteoporosis in women with anorexia nervosa. N Engl J Med. 1984;311:1601–6. [PubMed] [Google Scholar]

37. Rencken ML, Chesnut CH, Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes. JAMA. 1996;276:238–40. [PubMed] [Google Scholar]

38. Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR. The clinical course of osteoporosis in anorexia nervosa: a longitudinal study of cortical bone mass. JAMA. 1991;265:1133–8. [PubMed] [Google Scholar]

39. Drinkwater BL, Nilson K, Chestnut CH, Bremner WJ, Shainholtz S, Southworth MB. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med. 1984;311:277–81. [PubMed] [Google Scholar]

40. Cumming DC. Exercise-associated amenorrhea, low bone density and estrogen replacement therapy. Arch Intern Med. 1996;156:2193–5. [PubMed] [Google Scholar]

41. Recker R, Davies KM, Hinders SM, Heaney RP, Stegman R, Kimmel DB. Bone gain in young adult women. JAMA. 1992;268:2403–8. [PubMed] [Google Scholar]

42. Klibanski A, Biller BMK, Schoenfeld DA, Herzog DB, Saxe VC. The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab. 1995;80:898–904. [PubMed] [Google Scholar]

43. Hergenroeder AC, O'Brian Smith E, Shypailo R, Jones LA, Klish WJ, Ellis K. Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone or placebo over 12 months. Am J Obstet Gynecol. 1997;176:1017–25. [PubMed] [Google Scholar]

44. Black DM, Cummings SR, Karpf DB, et al. Randomized trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Lancet. 1996;348:1535–41. [PubMed] [Google Scholar]

45. Hosking D, Chilvers CED, Christiansen C, et al. Prevention of bone loss with alendronate in postmenopausal women under 60 years of age. N Engl J Med. 1998;338:485–92. [PubMed] [Google Scholar]

46. McClung M, Clemmensen B, Daifotis A, et al. Alendronate prevents postmenopausal bone loss in women without osteoporosis. Ann Intern Med. 1998;128:253–61. [PubMed] [Google Scholar]

47. Robin AL, Siegel PT, Koepke T, Moye AW, Tice S. Family therapy versus individual therapy for adolescent females with anorexia nervosa. J Dev Behav Pediatr. 1994;15:111–6. [PubMed] [Google Scholar]

48. Eisler I, Dare C, Russell GF, Szmukler G, leGrange D, Dodge E. Family and individual therapy in anorexia nervosa. A 5-year follow-up. Arch Gen Psychiatry. 1997;54:1025–30. [PubMed] [Google Scholar]

49. Gowers S, Norton K, Halek C, Crisp AH. Outcome of outpatient psychotherapy in a random allocation treatment study of anorexia nervosa. Int J Eating Disord. 1994;15:165–77. [PubMed] [Google Scholar]

50. Treasure J, Todd G, Brolly M, Tiller J, Nehmed A, Denman F. A pilot study of a randomised trial of cognitive analytical therapy vs educational behavioral therapy for adult anorexia nervosa. Behav Res Ther. 1995;33:363–7. [PubMed] [Google Scholar]

51. Fairburn CG, Shafran R, Cooper Z. A cognitive behavioral theory of anorexia nervosa. Behav Res Ther. 1999;37:1–13. [PubMed] [Google Scholar]

52. Halmi KA, Eckert E, LaDu TJ, Cohen J. Anorexia nervosa: treatment efficacy of cyproheptadine and amitriptyline. Arch Gen Psychiatry. 1986;43:177–81. [PubMed] [Google Scholar]

53. Gwirtsman HE, Guze BH, Yager J, Gainsley B. Fluoxitene treatment of anorexia nervosa: an open clinical trial. J Clin Psychiatry. 1990;51:378–82. [PubMed] [Google Scholar]

54. Kaye WH, Weltzin TE, Hsu LK, Bulik CM. An open trial of fluoxetine in patients with anorexia nervosa. J Clin Psychiatry. 1991;52:464–71. [PubMed] [Google Scholar]

55. Attia E, Haiman C, Walsh BT, Flater SR. Does fluoxetine augment the inpatient treatment of anorexia nervosa? Am J Psychiatry. 1998;155:548–51. [PubMed] [Google Scholar]

56. Garfinkel PE, Garner DM. The Role of Drug Treatments for Eating Disorders. New York, NY: Brunner/Mazel; 1987. [Google Scholar]

57. Wells LA, Logan KM. Pharmacologic treatment of eating disorders: a review of selected literature and recommendations. Psychosomatic. 1987;28:470–9. [PubMed] [Google Scholar]

58. House RC, Grisius R. Periomolysis: unveiling the surrepitious vomiter. Oral Surg. 1981;6:152–5. [PubMed] [Google Scholar]

59. Clark DC. Oral complications of anorexia nervosa and/or bulimia: with a review of the literature. J Oral Med. 1985;40:134–8. [PubMed] [Google Scholar]

60. Dawsen J, Jones C. Vomiting induced hypokalemic alkalosis and parotid swelling. Practitioner. 1977;28:267–8. [PubMed] [Google Scholar]

61. Levin PA, Falko JM, Dixon K, Gallup EM, Saunders B. Benign parotid enlargement in bulimia. Ann Intern Med. 1980;93:827–9. [PubMed] [Google Scholar]

62. Walsh BT, Croft CB, Katz JL. Anorexia nervosa and salivary gland enlargement. Int J Psychiatry Med. 1981;11:255–61. [PubMed] [Google Scholar]

63. Larsen K, Skov Jensen B, Axelsen F. Perforation and rupture of the esophagus. Scand J Thorac Cardiovas Surg. 1983;17:311–6. [PubMed] [Google Scholar]

64. Saul SH, Dekker A, Watson CG. Acute gastric dilatation with infarction and perforation. Report of fatal outcome in patient with anorexia nervosa. Gut. 1981;22:978–83. [PMC free article] [PubMed] [Google Scholar]

65. Mitchell JE, Pyle RL, Miner RA. Gastric dilatation as a complication of bulimia. Psychosomatics. 1982;23:96–7. [PubMed] [Google Scholar]

66. Breslow M, Yates A, Shisslak C. Spontaneous rupture of the stomach: a complication of bulimia. Int J Eating Disorders. 1986;5:137–42. [Google Scholar]

67. Mitchell JA, Boutacoff LI. Laxative abuse complicating bulimia: medical and treatment implications. Int J Eating Disorders. 1986;5:325–34. [Google Scholar]

69. Cooke WT. Laxative abuse. Clin Gastroenterol. 1977;6:659–73. [PubMed] [Google Scholar]

70. Al-Mufty NS, Bevan DH. A case of subcutaneous emphysema, pneumomediastinum and pneumoretroperitoneum associated with functional anorexia. Brit J Clin Pract. 1977;31:160–1. [PubMed] [Google Scholar]

71. Donley AJ, Kemple TJ. Spontaneous pneumomediastinum complicating anorexia nervosa. Br J Med. 1978;11:1604–5. [PMC free article] [PubMed] [Google Scholar]

72. Brotman MC, Forbath N, Garfinkel PE, Humphrey JG. Myopathy due to ipecac syrup poisoning in a patient with anorexia nervosa. Can Med Assoc J. 1981;125:453–4. [PMC free article] [PubMed] [Google Scholar]

73. Adler AG, Walinsky P, Krall RA, et al. Death resulting from ipecac syrup poisoning. JAMA. 1983;243:1977–8. [PubMed] [Google Scholar]

74. Palmer EP, Guay AT. Reversible myopathy secondary to abuse of ipecac in patients with major eating disorders. N Engl J Med. 1986;313:1457–9. [PubMed] [Google Scholar]

75. Brotman AW, Rigotti N, Herzog DB. Medical complications of eating disorders: outpatient evaluation and management. Compr Psychiatry. 1985;26:258–72. [PubMed] [Google Scholar]

76. Mitchell JE, Pyle RI, Eckert ED, Hatsukami D, Lentz R. Electrolyte and other physiological abnormalities in patients with bulimia. Psychol Med. 1983;13:273–8. [PubMed] [Google Scholar]

77. Mitchell JE, Seim HC, Colon E, Pomeroy C. Medical complications and medical management of bulimia. Ann Intern Med. 1987;107:71–7. [PubMed] [Google Scholar]

78. Fairburn CG, Jones R, Peveler RC, Hope RA, O'Connor M. Psychotherapy and bulimia nervosa: the longer-term effects of interpersonal psychotherapy, behavior therapy and cognitive behavior therapy. Arch Gen Psychiatry. 1993;50:419–28. [PubMed] [Google Scholar]

79. Goldbloom DS, Olmsted M, Davis R, et al. A randomized controlled trial of fluoxetine and cognitive behavioral therapy for bulimia nervosa: short term outcome. Behav Res Ther. 1997;35:803–11. [PubMed] [Google Scholar]

80. Treasure J, Schmidt U, Troop N, Tiller J, Todd G, Turnbull S. Sequential treatment for bulimia nervosa incorporating a self-care manual. Br J Psychiatry. 1996;168:94–8. [PubMed] [Google Scholar]

81. Lewandowski LM, Gebing TA, Anthony JL, O'Brien WH. Meta-analysis of cognitive-behavioral treatment studies for bulimia. Clin Psychol Rev. 1997;17:703–18. [PubMed] [Google Scholar]

82. Thackwray DE, Smith MC, Bodfish JW, Meyers AW. A comparison of behavioral and cognitive-behavioral interventions for bulimia nervosa. J Consult Clin Psychology. 1993;61:639–45. [PubMed] [Google Scholar]

83. Garner DM, Rockert W, Davis R, Garner MV, Olmsted MP, Eagle M. Comparison of cognitive behavioral and supportive expressive therapy for bulimia nervosa. Am J Psychiatry. 1993;150:37–46. [PubMed] [Google Scholar]

84. Fairburn CG, Norman PA, Welch SL, O'Connor ME, Doll HA, Peveler RC. A prospective study of outcome in bulimia nervosa and the long-term effects of three psychological treatments. Arch Gen Psychiatry. 1995;52:304–12. [PubMed] [Google Scholar]

85. Walsh BT, Wilson GT, Loeb KL, et al. Medication and psychotherapy in the treatment of bulimia nervosa. Am J Psychiatry. 1997;154:523–31. [PubMed] [Google Scholar]

86. Mitchell JE, Pyle RL, Eckert ED, Hatsukami D, Pomeroy C, Zimmerman R. A comparison study of antidepressants and structured group psychotherapy in the treatment of bulimia nervosa. Arch Gen Psychiatry. 1990;47:149–57. [PubMed] [Google Scholar]

87. Agras WS, Rossiter EM, Arnow B, et al. Pharmacologic and cognitive-behavioral treatment for bulimia nervosa: a controlled comparison. Am J Psychiatry. 1992;149:82–7. [PubMed] [Google Scholar]

88. Thiels C, Schmidt U, Treasure J, Garthe R, Troop N. Guided self-change for bulimia nervosa incorporating use of a self-care manual. Am J Psychiatry. 1998;155:947–53. [PubMed] [Google Scholar]

89. Fluoxetine Bulimia Nervosa Collaborative Study Group. Fluoxitene in the treatment of bulimia nervosa: a multi-center placebo-controlled double blind trial. Am J Psychiatry. 1992;49:139–47. [PubMed] [Google Scholar]

90. Goldstein DJ, Wilson MG, Thompson VL, Potvin JH, Rampey AH., Jr Long term fluoxetine treatment of bulimia nervosa. Fluoxetine Bulimia Nervosa Research Group. Br J Psychiatry. 1995;166:660–6. [PubMed] [Google Scholar]

91. Fornari VM, Sandberg DE, Lachenmeyer J, Cohen D, Matthews M, Montero G. Seasonal variations in bulimia nervosa. Ann NY Acad Sci. 1989;575:509–11. [Google Scholar]

92. Lam RW, Solyom L, Tompkins A. Seasonal mood symptoms in bulimia nervosa and seasonal affective disorder. Compr Psychiatry. 1991;32:552–5. [PubMed] [Google Scholar]

93. Levitan RD, Kaplan AS, Rockert W. Chracterization of the “seasonal” bulimic patient. Int J Eating Dis. 1996;19:187–92. [PubMed] [Google Scholar]

94. Lam RW, Goldner EM, Soplyom L, Remick RA. A controlled study of light therapy for bulimia nervosa. Am J Psychiatry. 1994;151:744–9. [PubMed] [Google Scholar]

95. Blouin AG, Blouin JH, Iversen H, et al. Light therapy in bulimia nervosa: a double-blind, placebo controlled study. Psychiatry Res. 1996;60:1–9. [PubMed] [Google Scholar]

96. Braun D, Sunday S, Fornari V, Halmi K. Bright light therapy decreases winter binge frequency in women with bulimia nervosa: a double-blind, placebo controlled study. Compr Psychiatry. 1999;40:442–8. [PubMed] [Google Scholar]

97. Rodin GM, Johnson LE, Garfinkel PE, Daneman D, Kenshole AB. Eating disorders in female adolescents with insulin-dependent diabetes mellitus. Int J Psychiatry Med. 1986;16:49–57. [PubMed] [Google Scholar]

98. Krowlewski AS, Warram JH, Cristlieb AR, Busick EJ, Kahn CR. Risk of proliferative diabetic retinopathy in juvenile-onset type I diabetes: a 40 year follow-up study. Diabetes Care. 1985;9:443–52. [PubMed] [Google Scholar]

99. Rydall AC, Rodin GM, Olmsted MP, Devenyi RG, Daneman D. Disordered eating behavior and microvascular complications in young women with insulin-dependent diabetes mellitus. N Engl J Med. 1997;336:1849–54. [PubMed] [Google Scholar]

100. American College of Sports Medicine. The female athlete triad: disordered eating, amenorrhea, osteoporosis: call to action. Sports Med Bulletin. 1992;27 [Google Scholar]

101. Carlat DJ, Camargo CA, Herzog DB. Eating disorders in males: a report on 135 patients. Am J Psychiatry. 1997;154:1127–32. [PubMed] [Google Scholar]

Articles from Journal of General Internal Medicine are provided here courtesy of Society of General Internal Medicine