The female athlete.

Annotation: The female athlete remains less well understood and less well studied compared with male athletes, especially in the areas of performance factors, repetitive stress, and acute injuries. Logical reasons for this include: (a) a limited two-generation span of the high-profile elite female; (b) fewer females involved in coaching, research, and sports medicine; and (c) limited areas of female youth sports historically (gymnastics, swimming, dance). Notwithstanding these reasons, the new millennium demands an increased emphasis on gender equity and the female athlete in all respects.

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The female athlete has special issues that the physician will address. Differences in physical and physiologic characteristics affect performance and risk of injury. Title IX of the Educational Amendment Act of 1972 mandated equal opportunity for women in educational institutions receiving federal funding, and effectively increased competitive female athletic participation in the United States. The disparity in performance and injury patterns between males and females has become less pronounced as women have become more active in sports at a younger age, and with training and conditioning techniques appropriately applied to the female athlete.

Performance Factors

Anatomy and physiology

The prepubertal female is equal in strength, aerobic power, heart size, and weight to her male counterpart. With the onset of puberty, the female body undergoes physiologic changes under the influence of the female sex hormones which affect bone mass, lean body mass, circulation, and metabolism.

The typical female physique is portrayed with a wider pelvis, femoral anteversion, genu valgum, and external tibial torsion. However, pelvic shapes vary widely among both men and women. Center of gravity differences are minimal, approximately one inch, and actually correlate better with height and body type than gender. (1) Adult females generally have smaller bones, with smaller articular surfaces, and shorter leg length as a proportion of height. Shorter long-bone length effectively results in a smaller lever arm and decreased force achievable with various maneuvers.

Throughout childhood, girls and boys have approximately equal body fat. At puberty, boys gain muscle mass and lose body fat under the influence of androgens, while girls gain both lean mass and fat mass. Adult women have approximately 10% more body fat than men on average. The average teenage girl has 20 to 25% body fat, whereas the body fat of an athletic girl may be lower than 10%. (2) The basal metabolic rate is lower in females by approximately 10%, which becomes important when designing nutritional plans for the female athlete. The difference is primarily due to the metabolic activity of adipose versus muscle tissue. The presence of estrogen and progesterone promotes greater reliance on fat metabolism at a given relative exercise intensity, enhances glycogen uptake and storage, and enhances glycogen utilization. (3-7)

Differences in muscle strength are not due to fiber type, but rather muscular hypertrophy and percentage of muscle mass. (8) Androgen secretion leads to increased protein synthesis and hypertrophy of skeletal and cardiac muscle. Males have approximately 40% muscle mass versus approximately 23% in females. Average muscle fiber cross-sectional area in females is 60 to 85% that of men. However, resistance training can result in similar relative gains in strength and hypertrophy. (8)

The changes in body composition and circulatory parameters at puberty result in greater cardio-respiratory capacity (20% greater) in men. Adult men, due to the effect of androgens on protein synthesis, have higher hemoglobin and hematocrit concentrations, resulting in a higher oxygen-carrying capacity relative to women. Controlling for the same body weight and level of conditioning, women have a smaller heart and lung mass, lower stroke volume, and lower maximal cardiac output, resulting in decreased effectiveness in anaerobic and aerobic activities. Training overcomes some of the discrepancy by increasing maximum oxygen uptake (V[O.sub.2]max). (9) Studies to date disagree as to whether performance and V[O.sub.2]max are affected by menstrual cycle phase, and which phase, and studies often have not appropriately documented menstrual cycle phase with blood or urine testing. (10-12) Recent studies have linked hyperventilation and airway reactivity of asthma with hormonal status, ie, pregnancy and the luteal phase. (5, 13-15) Oral contraceptives (OCPs) may attenuate the effect. (16)

Psychology

Psychologic effects on performance can be real, but whether or not the premenstrual syndrome and its associated mood swings truly affects performance or contributes to injury risk remains unproven. Studies to date have been contradictory and were completed during the female sports revolution, often with improperly conditioned athletes and inaccurate extrapolations of menstrual cycle staging. (17-24) Premenstrual dysphoric disorder, which should be differentiated from molimina, is recognized by the American Psychiatric Association in the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. (25) Serotonin levels are thought to be the link between levels of estrogen and progesterone and mood disorders. (26,27) Psychological aspects of eating disorders can indirectly affect bone health and risk of injury through poor nutritional intake.

Biochemistry

In vitro and in vivo studies show that estrogen decreases collagen content, reduces ligament tensile force, and increases joint elasticity, while progesterone has the opposite effect, increasing collagen content. (28) Relaxin has been shown to downregulate collagen synthesis and stimulate the activity of collagenase. (29) However, joint laxity in pregnancy does not correlate with serum relaxin levels. (30) Receptors for estrogen, progesterone, and relaxin are found on the anterior cruciate ligament. (31)

Further studies are needed to delineate whether the increased rate of injury seen in ovulating women is due to hormonal effects on tissues, neuromuscular coordination, or mood and decision making.

Obstetric and Gynecological Issues

Menstrual disorders

Many unique parameters of medical care in female athletes relate to the menstrual cycle. Menstrual-related disorders, including amenorrhea, oligomenorrhea, delayed menarche, luteal phase deficiency, and anovulation, are often associated with intense training, low body weight, low body fat, poor nutrition, decreased caloric intake, an immature hypothalamic-pituitary-gonadal/adrenal axis, and elevated levels of circulating glucocorticoids from stress and exercise. [beta]-endorphins, androgens, and cortisol, secreted in response to stress, negatively feed back on gonadotropin-releasing hormone. In addition, leptin, a hormone made by the fat cell, is postulated to be the link between body fat percentages or nutritional status and menstrual cycle irregularity, via feedback mechanisms on the hypothalamus. (32-34) Irregular menses and anovulation more frequently occur in athletes (up to 60%) compared with nonathletes (approximately 5%), (35) with the percentage of those affected being sport dependent. Irregular menses are reported in up to 20% of casual runners and 50% of elite runners and professional dancers. (2) The average female undergoes menarche at age 12 to 13, while menarche may be delayed until age 15 in elite athletes.

In the adolescent, delayed menarche and amenorrhea result in a state of relative hypoestrogenism, which affects bone metabolism by a lower rate of bone accretion versus resorption during remodeling. Manifestations of hypoestrogenism on bone include an increased incidence of osteopenia, scoliosis, stress fractures, and lower peak bone mass.

Primary and secondary amenorrhea should be evaluated in a systematic fashion to exclude medical causes of menstrual dysfunction other than "athletic amenorrhea". These include thyroid disease, adrenal disease, ovarian failure, polycystic ovarian disease, chromosomal abnormalities, pituitary dysfunction, prolactinoma, malnutrition, and pregnancy. In the athlete with amenorrhea or oligomenorrhea, a progestin challenge test should be performed with ten milligrams of medroxyprogesterone orally for 5 to 10 days. This should induce withdrawal bleeding if adequate levels of circulating estrogen are present. Menstrual disorders may be treated by decreasing or modifying training, improving nutrition, increasing body weight, and hormone replacement therapy (HRT). Progesterone may be sufficient if the female is euestrogenic. If hypoestrogenic with a serum estradiol <50 pg/mL, oral contraceptive pills are recommended. The American Academy of Pediatrics advises that females within 3 years of menarche do not take hormonal therapy. However, it also recommends estrogen if stress fractures have occurred. (36)

Iron deficiency anemia 

Up to 80% of female athletes may be iron deficient. Women lose about 1 mg of iron per day through excretory functions and an additional 0.5 mg per day during menses. The typical American diet does not always replace these losses, and over time, iron stores are depleted. Daily supplementation is recommended, especially for long-distance runners, as low iron stores, evidenced by low serum ferritin levels, can be associated with a significant decline in aerobic performance capacity. (32,37)

Pregnancy

Exercise in moderation does not affect fertility, but excessive exercise may result in an anovulatory cycle. Most women can begin or continue to exercise during pregnancy. (38) An increase in injury rates in pregnant women has not been documented. The physiologic adaptations of pregnancy allow for safe sports participation. Cardiac output, heart rate, blood volume, venous capacity, and heat dissipation increase. Benefits of exercise during pregnancy include shorter labor, decreased medical intervention during delivery, and quicker postpartum recovery. Exercise that begins in mid-trimester has not been associated with birth weight abnormalities. Birth weight can be affected by exercise in the third trimester, but this is actually due to a reduction in fetal fat mass, and a slight decrease in the duration of gestation, with little impact on head circumference or lean body mass. (39) A physician should monitor fetal growth and weight gain throughout the pregnancy. Performance may be affected by limited diaphragmatic excursion.

Risks to the fetus include hypoxia (at altitude) and hyperthermia (teratogenic threshold is 39.2[degrees]C for first trimester neural tube defects). Theoretically, shear forces on the mobile uterus may cause premature rupture of membranes, placental separation, premature labor, or umbilical cord entanglement. However, data do not support these concerns. Meanwhile, the incidence of meconium, abnormal fetal heart rate patterns, cord entanglement, and low Apgar scores is reduced in those who continue exercise. (40-42) There are no reports of utero-placental insufficiency among exercising women. (43) However, in the untrained woman, fetal bradycardia, indicating fetal hypoxemia, can result from a rapidly progressive exercise routine. (44) The normal fetal response to exercise is a 10 to 25 beats-per-minute increase in fetal heart rate. Supine exercise should be avoided in the second and third trimesters, as compression of the vena cava decreases venous return and cardiac output.

The American College of Obstetricians and Gynecologists has published guidelines for exercise during pregnancy. (45) Current recommendations state that healthy women may safely begin or maintain an exercise program during pregnancy under close monitoring. Hydration, caloric intake, rectal temperature (<38.7[degrees]C), body weight, and fetal heart rate response to exercise should be monitored. Sports that put the uterus and fetus at significant risk for blunt trauma or hyperbaric injury should be avoided.

Absolute contraindications to exercise during pregnancy include: pregnancy-induced hypertension, premature rupture of fetal membranes, preterm labor in current or previous pregnancies, incompetent cervix, persistent second or third trimester bleeding, intrauterine growth retardation, uncontrolled hypertension, renal disease or diabetes mellitus, and hemodynamically significant heart disease or anemia. However, women with gestational diabetes mellitus often see improved control of blood glucose with exercise. (46,47) Relative contraindications include: multiple gestations, history of miscarriage, breech in third trimester, history of precipitous labor, malnutrition, arrhythmia, previous sedentary lifestyle, or active thyroid disease. The recommendations state that the pregnant female should exercise at 65 to 85% of maximum predicted heart rate three times a week for no longer than 45 minutes. However, elite athletes have been known to exercise daily and rigorously up until days before delivery, without adverse effects on the fetus. (48,49) Exercise should be stopped if the woman experiences extreme shortness of breath, dizziness, headache, chest pain, or contractions. Weight training with light weights and moderate repetitions should not pose a significant risk for injury.

In the postpartum period, women may resume activity approximately 1 to 2 weeks after a normal vaginal delivery. After a Caesarean section, the recommended interval is 6 to 8 weeks. (32) After a dilation and curettage, exercise can be started within 2 days and water sports within 1 week. Lactating women will have increased energy and nutrient requirements.

Oral contraceptives

OCPs may have effects on bone metabolism, risk of injury, and performance. (12,50,51) OCPs are used for contraception, cycle manipulation, control of premenstrual symptoms, control of dysmenorrhea and menorrhagia, and hormone replacement therapy.

The level of estrogen in OCPs can exceed that of HRT, which has been shown to increase bone density in postmenopausal females. Estrogen inhibits bone resorption, however, so this effect may not significantly alter bone mass in amenorrheic athletes, where the problem lies with bone accretion. However, in one study, women who exercised and utilized OCPs had higher bone mineral density. (52) OCP use correlates with a decrease in the risk of stress fractures in some studies, but not in others. (53) It is difficult to interpret and apply the current literature to medical practice, as dosage and type of estrogen and progestin varies widely.

OCP use has also been associated with a decrease in the risk of traumatic injury. (22) It is unclear if this is due to hormonal effects directly on the tissues or an effect on psychological performance and neuromuscular coordination. (22,23,54) The hormones in OCPs seem to have some direct tissue effects, as OCP use correlates with decreased knee laxity scores. (54,55)

It is clear that OCPs decrease PMS symptoms and decrease menstrual blood loss, thereby resulting in potentially improved aerobic capacity. However, OCP use has reportedly reduced aerobic capacity. (56) OCPs can also affect substrate metabolism by increasing fatty acid metabolism and sparing carbohydrate use. (12,57) Newer studies show no significant changes in strength with OCP use or stage of the menstrual cycle. (10,20,58)

Depo-Medroxyprogesterone Acetate

Use of Depo-Provera (Pharmacia & Upjohn, Peapack, NJ) has been associated with bone demineralization. (59,60) There is a paucity of studies exploring the effects of progestin derivatives on bone density, injury, and performance.

Menopause

Ovarian failure results in cessation of menses and indirectly leads to osteoporosis. Before participation, postmenopausal women should have bone density testing to assess fracture risk. Postmenopausal women also see a rise in cardiovascular risk, and as a result, women over age fifty with two or more risk factors for coronary artery disease, or symptoms thereof, need a graded exercise stress test before moderate activity. (61)

Osteoporosis

Each year, over one million fractures are attributed to osteoporotic bone. Maximum content and rate of decline is affected by genetics, nutrition, hormones, and exercise. Traditional risk factors for osteoporosis include white or Asian ethnicity, low body weight, family history, smoking, alcoholism, oral corticosteroid use, inadequate calcium and vitamin D intake, estrogen deficiency, and inactivity.

Osteoporosis may result from inadequate bone formation or premature bone loss. Maximum bone mineral content is achieved in the second decade of life. Females who exercise regularly can maintain bone mass into the third decade, and see a slower rate of decline thereafter. Athletic women generally have greater bone density than inactive women. However, excessive exercise may negatively affect bone density through negative feedback on secretion of the sex hormones. Increased osteoclastic activity is seen with low estrogen levels. In addition, poor nutritional status may affect bone metabolism via the centrally mediated effects of leptin. (32) Bone mineral density (BMD) values in amenorrheic athletes can be similar to postmenopausal women. Generally, BMD can only be partially restored. Bone demineralization is compounded in athletes taking corticosteroids in the long term, anabolic steroids, or thiazide diuretics.

Dual-energy x-ray absorptiometry is useful in estimating BMD. Scores are obtained by comparing subjects with age- and sex-matched populations. The World Health Organization diagnostic guidelines (62) for postmenopausal females indicate a diagnosis of osteopenia between a t score of -1.0 and -2.5 SD, and a diagnosis of osteoporosis when the t score is less than -2.5 SD. BMD may also be calculated with computed tomography technology, peripheral bone scanning, or quantitative ultrasound.

Medical therapy should be initiated to reduce fracture risk in women with one or more risk factors having BMD t scores below -1.5 SD. Weight-bearing exercise and resistance training can improve bone mass. (2) Women at risk for osteoporosis should consume at least 1,500 mg dietary calcium per day in addition to vitamin D supplementation. (63) Hormone replacement therapy, though controversial, is usually recommended for amenorrheic and postmenopausal females. (64-66) In amenorrheic athletes, the combined effect of calcium and estrogen supplementation can increase bone mass up to 4% in one year. (10) HRT should not be prescribed for younger women who have not completed their growth, as estrogens can cause physeal closure. Alternative agents to HRT that have reduced fracture risk in postmenopausal females include bisphosphonates, calcitonin, parathyroid hormone, and selective estrogen receptor modulators (SERMs). Of these, bisphosphonates and SERMs have also been shown to increase bone mass. Note that use of these alternative agents and their effects have not been studied in young females with osteoporosis and are not recommended at this time.

Female Athletic Triad

The female athletic triad is known as a syndrome including disordered eating, altered menstrual function, and deficiencies in bone mineralization, resulting in amenorrhea and osteopenia. (67,68) The triad is more common in sports where lean physique and low body weight are an advantage, such as in gymnastics, skating, dancing, and running. The Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition delineates the profiles seen in the eating disorders of anorexia and bulimia. Factors leading to disordered eating include sports-specific psychological profile, body image or weight or strength expectations, and underlying depression and tendencies toward control. Disordered eating is prevalent among athletes, up to 60% in some studies. (69) The athlete with an eating disorder may also frequently abuse laxatives and diuretics, and is at increased risk for dehydration and electrolyte disturbances. The mortality rate in treated anorectic females reaches 18%. (70,71)

Excessive exercise or weight loss can lead to menstrual irregularity via feedback mechanisms on the hypothalamus. Deficiency of the sex hormones and malnutrition leads to osteopenia, with an increased risk of stress fractures. (72) Amenorrheic athletes see a continuing decline in BMD, while resumption of menses correlates with increased bone density scores. (73) However, regular menstrual cycling induced by OCP use has not been proven to increase bone density.

Screening during the preparticipation history and examination is vital to discovering an athlete at risk. Questions covering menstrual history, nutrition, ideal body weight, and exercise history should be included. The modified Eating Attitudes Test (EAT-26) may be a useful adjunct to detect eating disorders in the preparticipation screening history and examination. (74,75) BMD screening is recommended for females with a history of >6 months of abnormal menses or disordered eating and in those with stress fractures. (32) Treatment involves addressing behavioral factors, developing support systems, nutritional and psychologic counseling, instituting weight training and resistance exercises, and supplemental vitamins, minerals, and hormones.

Gender-specific Orthopaedic Injuries

The female sports revolution, occurring from the 1970s to the present, has resulted in increased participation, but greater emphasis on equipment, training, and coaching principles tailored to females is necessary. In the 1980s, lack of conditioning was probably responsible for increased injury rates seen in women. As women have improved training and conditioning, injury rates have become more evenly distributed. Though most injuries are not unique to females, a few injuries in particular may be associated with the effects of hormones on bone or soft tissue. OCPs have been shown to decrease the risk of overall injury, (55) and may play a preventative role in the future.

Breast and gynecologic injuries are rare. Protective devices, such as bras with plastic cups, are obsolete. Sports bras are recommended to support Cooper ligaments. The American Academy of Pediatrics states that no restrictions are necessary for female athletes with a single ovary. (76)

Overuse injuries, such as stress fractures, are especially problematic for female athletes. Inadequate strength, flexibility, footwear, equipment, and training methods all play a role in the incidence of these injuries. Hypoestrogenic women, with decreased bone mass, are at increased risk. In dancers, prevalence of fractures reaches 60%, while incidence of fractures and scoliosis are increased with each year of delayed menarche. (77)

Back pain may represent several distinct processes in females. Women are predisposed to having lumbosacral muscular pain because of increased lumbar lordosis, which is associated with pregnancy, tight hamstring muscles, and poor abdominal strength. Ligament laxity can lead to sacroiliac joint dysfunction from pelvic instability. Spondylolysis, a stress fracture to the pars interarticularis of the spine, is seen in gymnasts and dancers as a result of repeated hyperextension and impact loading. Idiopathic scoliosis is ten times more common in females.

Shoulder injuries are also common, a result of a combination of increased ligament and joint laxity, relatively weaker upper body strength, and shorter long bone length. For example, female swimmers must increase stroke repetitions to achieve comparable speed and distance.

Women have an increased tendency to develop patellofemoral knee pain. Lateralization of patellar tracking occurs at increased rates in females due to ligamentous laxity, deficiency of vastus medialis obliquus, genu valgum, increased Q angle, and excessive pronation with associated external tibial torsion.

Inappropriate footwear has lead to many complaints of foot pain. Women's athletic shoes are often designed to be too narrow, while dress shoes frequently have a pointy toe box. Wearing high-heeled shoes causes relative tightening of the Achilles tendon and increased load bearing through the forefoot.

The Anterior Cruciate Ligament

The National Collegiate Athletic Association (NCAA) Injury Surveillance System studied basketball and soccer injuries from 1989 to 1993 and found that women are still at increased susceptibility for injury of the anterior cruciate ligament (ACL). (78,79) Female soccer players had a 2.4:1 risk, while female basketball players had a 4:1 risk of ACL injury. Gender disparity in this injury has been attributed to multiple factors, including poor muscular protection of the knee, hormonal effects on ligamentous tissue (laxity), and landing techniques. (23,31,54,80-85) Increased Q angle has not been proven to significantly correlate with an increased incidence of injury in females. (86) Despite previous beliefs, ligament size, intercondylar notch width, and notch width index, all factors involved in risk of ACL tear, are not more prevalent in women. (87) Joint laxity has been linked to increased risk of injury; however, the joint laxity seen in pregnancy has not. (88) Gender differences in knee laxity between males and ovulating females are significant, but whether the effect occurs in a cyclical fashion with the menstrual cycle requires further studies. (55,83,84,89) Study results are conflicting as to which phase of the menstrual cycle is associated with ACL injury. (22,83,90) Therefore, interpretation of findings is difficult. OCP use correlates with decreased knee laxity scores, which may explain the protective effect documented in some studies. (22,55)

Preventing these season-ending injuries is the focus of current sports medicine research. Variables that can be addressed to alter risk profile include strength and agility training, proprioception and balance training, and, though controversial, use of OCPs. Teaching women a modified style of planting, cutting, and pivoting with the knees in a flexed position resulted in an 89% reduction of ACL injuries in a 1989 study by Griffis et al. (91) A plyometric training program can also reduce risk factors and incidence of injury four-fold. (92) Improvement of hamstring/quadriceps strength and hamstring recruitment is another area of focus. (84,93-95)

Future Research Questions

Female sports have come a long way. Women's success in Olympic sports and the development of women's professional sport teams is evidence of the closing gender gap in athletics. Future research will focus on improving female performance in athletics, and on reducing risk of injury. These new studies must differentiate results seen in ovulating versus nonovulating females, as the effects of hormones on tissues and neuropsychology are vast. Racial differences must also be considered. Further investigations are warranted into the effects of oral contraceptives and progestin derivatives on bone health and risk of soft tissue injury.

Accepted May 21, 2004.

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Jolie C. Holschen, MD

From the University of Michigan, Departments of Orthopaedic Surgery and Emergency Medicine, Ann Arbor, MI.

Reprint requests to Jolie C. Holschen, MD, Medsport, 24 Frank Lloyd Wright Drive, Ann Arbor, MI 48106.