Recognition and rehabilitation of the female athlete triad/tetrad: a multidisciplinary approach.

While the benefits of physical activity are numerous, the female athlete triad poses a significant health risk to young athletes. Emerging research links the triad to endothelial dysfunction--a sentinel event in cardiovascular disease--suggesting that this complex interplay of metabolic and endocrine factors may be described more accurately as a tetrad. Effective treatment of the triad/tetrad requires a multidisciplinary approach. Emphasis must be placed on prevention, recognition, and treatment of triad for the promotion of healthy nutritional and activity profiles in female athletes across their lifespans.

Female athlete triad screening in National Collegiate Athletic Association Division I athletes: is the preparticipation evaluation form effective?

OBJECTIVE: To evaluate the screening practices and preparticipation evaluation (PPE) forms used to identify college athletes at risk for the female athlete triad (triad). DESIGN: Phone and/or e-mail survey. SETTING: National Collegiate Athletic Association (NCAA) Division I universities. PARTICIPANTS: All 347 NCAA Division I universities were invited to participate in a survey, with 257 participating in the survey (74%) and 287 forms collected (83%). MAIN OUTCOME MEASURES: Information about the nature of the PPE was requested from team physicians and certified athletic trainers during a phone or e-mail survey. In addition, a copy of their PPE form was requested to evaluate for inclusion of the 12 items recommended by the Female Athlete Triad Coalition for primary screening for the triad. RESULTS: All 257 universities (100%) required a PPE for incoming athletes; however, only 83 universities (32%) required an annual PPE for returning athletes. Screening was performed on campus at 218 universities (85%). Eleven universities (4%) were using the recently updated fourth edition PPE. Only 25 universities (9%) had 9 or more of the 12 recommended items included in their forms, whereas 127 universities (44%) included 4 or less items. Relevant items that were omitted from more than 40% of forms included losing weight to meet the image requirements of a sport; using vomiting, diuretics, and/or laxatives to lose weight; and the number of menses experienced in the past 12 months. CONCLUSIONS: The current PPE forms used by NCAA Division I universities may not effectively screen for the triad.

Challenges of the pregnant athlete and low back pain.

Low back pain during pregnancy is a common problem with a high prevalence among pregnant athletes. The etiology of pregnancy-related low back pain remains unclear, although more evidence is supporting a biomechanical/musculoskeletal origin. This article will review the causes of low back pain in athletes and pregnant women, differentiate low back from pelvic girdle pain, and discuss the treatment and prevention of pregnancy-related low back and pelvic girdle pain.

Association between the female athlete triad and endothelial dysfunction in dancers.

OBJECTIVE: To determine the prevalence of the 3 components of the female athlete triad [disordered eating, menstrual dysfunction, low bone mineral density (BMD)] and their relationships with brachial artery flow-mediated dilation in professional dancers. DESIGN: Prospective study. SETTING: Academic institution in the Midwest. PARTICIPANTS: Twenty-two professional ballet dancers volunteered for this study. INTERVENTIONS: The prevalence of the female athlete triad and its relationship to endothelial dysfunction. MAIN OUTCOME MEASURES: Subjects completed questionnaires to assess disordered eating and menstrual status/history. They also completed a 3-day food record and wore an accelerometer for 3 days to determine energy availability. Serum baseline thyrotropin, prolactin, and hormonal concentrations were obtained. Bone mineral density and body composition were measured with a GE Lunar Prodigy dual-energy X-ray absorptiometry. Endothelial function was determined as flow-mediated vasodilation measured by high-frequency ultrasound in the brachial artery. An increase in brachial diameter <5% to hyperemic flow stimulus was defined a priori as endothelial dysfunction. RESULTS: Seventeen dancers (77%) had evidence of low/negative energy availability. Thirty-two percent had disordered eating (EDE-Q score). Thirty-six percent had menstrual dysfunction and 14% were currently using hormone contraception. Twenty-three percent had evidence of low bone density (Z-score < -1.0). Sixty-four percent had abnormal brachial artery flow-mediated dilation (<5%). Flow-mediated dilation values were significantly correlated with serum estrogen and whole-body and lumbar BMD. All the 3 components of the triad plus endothelial dysfunction were present in 14% of the subjects. CONCLUSIONS: Endothelial dysfunction was correlated with reduced BMD, menstrual dysfunction, and low serum estrogen. These findings may have profound implications for cardiovascular and bone health in professional women dancers.

Folic acid supplementation improves vascular function in amenorrheic runners.

OBJECTIVE: The purpose of this study was to determine if folic acid supplementation improves endothelial vascular function (brachial artery flow-mediated dilation; FMD) in amenorrheic runners. DESIGN: Prospective cross-sectional study. SETTING: Academic medical center in the Midwest. PARTICIPANTS: Ten amenorrheic and 10 eumenorrheic women runners from the community volunteered for this study. INTERVENTIONS: Each participant was treated with folic acid (10 mg/d) for 4 weeks. MAIN OUTCOME MEASURES: Brachial artery FMD was measured before and after folic acid supplementation with standard techniques. RESULTS: The brachial artery FMD response to reactive hyperemia improved after folic acid supplementation in amenorrheic women (3.0% +/- 2.3% vs. 7.7% +/- 4.5%; P = 0.02). In the eumenorrheic control group, there was no change in brachial artery FMD (6.7% +/- 2.0% vs. 5.9% +/- 2.6%; P = 0.52). CONCLUSIONS: This study demonstrates that brachial artery FMD, an indicator of vascular endothelial function, improves in amenorrheic female runners after short-term supplementation with folic acid.

Prevalence of the female athlete triad in high school athletes and sedentary students.

OBJECTIVE: To determine the prevalence of the female athlete triad (low energy availability, menstrual dysfunction, and low bone mineral density) in high school varsity athletes in a variety of sports compared with sedentary students/control subjects. DESIGN: Prospective study. SETTING: Academic medical center in the Midwest. PARTICIPANTS: Eighty varsity athletes and 80 sedentary students/control subjects volunteered for this study. INTERVENTION: Subjects completed questionnaires, had their blood drawn, and underwent bone mineral density testing. MAIN OUTCOME MEASURES: Each participant completed screening questionnaires assessing eating behavior, menstrual status, and physical activity. Each subject completed a 3-day food diary. Serum hormonal, thyroid-stimulating hormone, and prolactin levels were determined. Bone mineral density and body composition were measured by dual-energy x-ray absorptiometry. RESULTS: Low energy availability was present in similar numbers of athletes (36%) and sedentary/control subjects (39%; P = 0.74). Athletes had more menstrual abnormalities (54%) compared with sedentary students/control subjects (21%) (P < 0.001). Dual-energy x-ray absorptiometry revealed that 16% of the athletes and 30% of the sedentary/control subjects had low bone mineral density (P = 0.03). Risk factors for reduced bone mineral density include sedentary control student, low body mass index, and increased caffeine consumption. CONCLUSIONS: A substantial number of high school athletes (78%) and a surprising number of sedentary students (65%) have 1 or more components of the triad. Given the high prevalence of triad characteristics in both groups, education in the formative elementary school years has the potential to prevent several of the components in both groups, therefore improving health and averting long-term complications.

Possible relationship of folic Acid supplementation and improved flow-mediated dilation in premenopausal, eumenorrheic athletic women.

The purpose of this study was to determine if six weeks of folic acid supplementation would improve brachial artery endothelial-dependent flow-mediated dilation in eumenorrheic female runners with previously normal serum folate levels. This was a prospective, double-blinded, randomized pilot study with convenience sampling. Sixteen eumenorrheic subjects who were not taking birth control pills and who ran at least 20 miles/week were randomly assigned to 10 mg/day of folic acid supplementation or placebo for at least 6 weeks. Serum folate levels and brachial artery measurements were made during the early follicular phase of the menstrual cycle, in a sedentary state, following an 8 hour fast; a standard ultrasound technique was used. The brachial artery vasodilator response to reactive hyperemia was similar between the folic acid (6.6% ± 0.8%, mean ± SE) and placebo groups (6.5% ± 0.7%) at baseline. After six weeks, there was a significantly higher change in flow-mediated dilation for the folic acid group (3.5% ± 0.6%) compared to the placebo group (0.1% ± 0.2%) (p = 0.01). Serum folate levels also increased significantly in the folic acid group following six weeks of folic acid supplementation. This study demonstrates that brachial artery flow-mediated dilation improves significantly in eumenorrheic female runners with previously normal serum folate levels after 6 weeks of supplementation with folic acid. Key pointsFolic acid improves FMD in eumenorrheic runners.Folic acid improves FMD in women runners.

Nutritional requirements of the child and teenage athlete.

There has been an explosion in sports participation, especially for women, in the last 35 years mainly because of Title IX. In 2005-2006, nearly 3 million girls and 4.2 million boys participated in high school athletics, and many more participated in club sports and recreational activities. On the other end of the spectrum, the prevalence of obesity in the United States is at an all-time high. Proper nutrition in combination with the appropriate amount of physical activity is of paramount importance for this era of adolescents.

Factors that affect the young female athlete.

The past 35 years have seen a tremendous increase in the number of female athletes at all ages and abilities. Recent research has shown a myriad of benefits for girls and women who participate in sports. Physical activity positively influences almost every aspect of a young woman's health, from her physiology to her social interactions and mental health. As the level of girls' participation in sports increases, it is important to examine their risk factors for sports-related injuries.

The female athlete triad and cardiovascular dysfunction.

In the past 35 years, a significant increase has occurred in sports participation by women. An estimated 3 million girls and young women compete in American high school sports. Women who participate in sports and fitness programs are generally healthier and have higher self-esteem. However, an increase has also been seen in gender-specific injuries and medical problems. The female athlete triad is a syndrome of separate but interrelated conditions of disordered eating, amenorrhea, and osteoporosis. Athletic amenorrhea is known to have a hormonal profile similar to menopause characterized by decreased circulating estrogens. Menopause is known to be associated with osteoporosis and accelerated cardiovascular disease. Although enhanced risk for cardiovascular disease is theoretically possible, it has not been explored in the young athletic population. Premature cardiovascular disease first manifests as endothelial dysfunction, which can be examined noninvasively with ultrasound. This article discusses disordered eating, amenorrhea, osteoporosis, and the potential for heightened cardiovascular risk in young athletic women.

Athletic amenorrhea and endothelial dysfunction.

OBJECTIVES: To determine if menstrual status changed in amenorrheic college runners over a 2-year period and what effect this had on brachial artery flow-mediated dilation. PARTICIPANTS: Eighteen athletes first studied in our laboratory 2 years prior were available for follow-up. Nine of the 10 original women with athletic amenorrhea (mean +/- SE, age 21.3 +/- 1.2 yrs), and 9 of the 11 eumenorrheics/controls (age 20.1 +/- 0.5 yrs) were studied 2 years after baseline measurements. METHODS: Questionnaires/personal interviews and blood draws were performed to determine menstrual status. A non-invasive ultrasound technique was used to determine brachial artery flow-mediated dilation (endothelium-dependent). RESULTS: Menstrual status changed in 7 of 9 original amenorrheic subjects (2 were taking hormone replacement, 2 were taking oral contraceptives, 3 had a natural menstrual period prior to testing, and 2 remained amenorrheic). Endothelium-dependent brachial artery dilation, measured as the percent change in maximal brachial artery diameter from baseline during reactive hyperemia, was improved in the original amenorrheic subjects (a 1.1% +/- 1.0 increase in the original study versus 5.6% + 1.1 increase in the current study, P=0.01) while in the eumenorrheic/control group there was no change (6.3% +/- 1.7 versus 8.0% +/- 1.3, P=0.42). CONCLUSIONS: Menstrual status changed in 7 of the 9 original amenorrheic athletes, and this change was associated with an improvement in brachial artery flow-mediated dilation.

Hypertension during Weight Lifting Reduces Flow-Mediated Dilation in Nonathletes.

PURPOSE: The purpose of this study was to determine whether increased intraluminal pressure is the damaging factor that reduces flow-mediated dilation (FMD) in young, healthy subjects after resistance exercise to maximal exertion. HYPOTHESIS: Attenuating the rise in brachial artery pressure during weight lifting by placing a blood pressure cuff on the upper arm prevents postexercise impairment of brachial artery FMD in sedentary individuals. METHODS: Nine sedentary individuals who exercise once a week or less and six exercise-trained individuals who exercise three times a week or more performed leg press exercise to maximal exertion on two separate occasions. During one visit, a blood pressure cuff, proximal to the site of brachial artery measurement, was inflated to 100 mm Hg to protect the distal vasculature from the rise in intraluminal pressure, which occurs during resistance exercise. Brachial artery FMD was determined using ultrasonography before and 30 min after weight lifting. RESULTS: Without the protective cuff, brachial artery FMD in sedentary individuals was reduced after weight lifting (9.0% ± 1.2% prelift vs 6.6% ± 0.8% postlift; P = 0.005), whereas in exercise-trained individuals, FMD was unchanged (7.4% ± 0.7% prelift vs 8.0% ± 0.9% postlift; P = 0.543). With the protective cuff, FMD no longer decreased but rather increased in sedentary individuals (8.7% ± 1.2% prelift vs 10.5% ± 1.0% postlift, P = 0.025). An increase in FMD was also seen in exercise-trained subjects when the cuff was present (6.6% ± 0.7% prelift vs 10.9% ± 1.5% postlift, P < 0.001). CONCLUSION: Protecting the brachial artery from exercise-induced hypertension enhances FMD in sedentary and exercise-trained individuals. These results indicate that increased intraluminal pressure in the artery contributes to the reduced FMD after heavy resistance exercise in sedentary individuals.

Awareness and comfort in treating the Female Athlete Triad: are we failing our athletes?

BACKGROUND: Recognition of the Female Athlete Triad (disordered eating, amenorrhea, osteoporosis) has increased significantly since it was defined in 1992 by the American College of Sports Medicine. However, knowledge and treatment of the Female Athlete Triad is still lacking among physicians and medical personnel. PURPOSE: We surveyed physicians, physical therapists, athletic trainers, and coaches to determine their knowledge and comfort in treating the Female Athlete Triad. METHODS: A questionnaire was submitted to 240 health care professionals (physicians, medical students, athletic trainers, physical therapists, and coaches) in a metropolitan city. RESULTS: Forty-eight percent of physicians, 43% of physical therapists, 38% of athletic trainers, 32% of medical students, and 8% of coaches were able to identify all 3 components of the Female Athlete Triad. When physicians were subdivided into specialties, 69% of Physical Medicine and Rehabilitation (PM&R) physicians, 63% of orthopaedic surgeons, 53% of family physicians, 36% of pediatricians, and 17% of gynecologists were able to identify all 3 components of the Female Athlete Triad. Only 9% of physicians felt comfortable treating the Female Athlete Triad. When physicians were subdivided into specialties, 17% of orthopaedic surgeons, 13% of family practitioners, 12% of PM&R physicians, and 4% of pediatricians felt comfortable with treatment programs. CONCLUSION: Data suggest that a heightened level of awareness and education in the proper treatment of the Female Athlete Triad is needed.

Stress fractures and knee injuries in runners.

Running often can cause injuries to the knee as a result of kinetic chain dysfunctions. Addressing these dysfunctions in rehabilitation can prevent future injury. Stress fractures often occur in runners who engage in training errors. Female runners are particularly susceptible to stress fractures, especially in the setting of the female athlete triad. Proper identification and prevention of these injuries allows for athletes to return to running expeditiously.

Ghrelin gene: identification of missense variants and a frameshift mutation in extremely obese children and adolescents and healthy normal weight students.

Ghrelin induces obesity via central and peripheral mechanisms. Administration of ghrelin leads to increased food intake and decreased fat utilisation in rodents. Ghrelin levels are decreased in obese individuals. Recently, a polymorphism (Arg-51-Gln) within the ghrelin gene (GHRL) was described to be associated with obesity. We screened the GHRL coding region in 215 extremely obese German Children and adolescents (study group 1) and 93 normal weight students (study group 2) by single strand conformation polymorphism analysis (SSCP). We found the two previously described single nucleotide polymorphisms (SNP: Arg-51-Gln and Leu-72-Met) in similar frequencies in study groups 1 and 2 (allele frequencies were: 0.019 and 0.016 for the 51-Gln allele and 0.091 and 0.086 for the 72-Met allele, respectively). Hence, we could not confirm the previous finding. Additionally, two novel variants were identified within the coding region: (1) We detected one healthy normal weight individual with a frameshift mutation (2bp deletion at codon 34). This frameshift mutation affects the coding region of the mature ghrelin. Hence, it is highly likely that the normal weight student is haplo-insufficient for ghrelin. (2) An A to T transversion leads to an amino acid exchange from Gln to Leu at amino acid position 90. The frequency of the 90-Leu allele was significantly higher in the extremely obese children and adolescents (0.063) than in the normal weight students (0.016; nominal p = 0.011). Additionally, we genotyped 134 underweight students and 44 normal weight adults for this SNP. Genotype frequencies were similar in extremely obese children and adolescents, underweight students and normal weight adults (p > 0.8). In conclusion, we identified four sequence variants in the coding region of the ghrelin gene in individuals belonging to different weight extremes. A frameshift mutation was detected in a normal weight individual. None of the variants seem to influence weight regulation.

Glucose transporter 4 gene: association studies pertaining to alleles of two polymorphisms in extremely obese children and adolescents and in normal and underweight controls.

The human insulin-responsive glucose transporter 4 gene (GLUT4) has been related to non-insulin-dependent diabetes mellitus (NIDDM) in several studies. Obesity is commonly found in patients with NIDDM. Hence, genes involved in NIDDM might also be relevant for obesity. We have analyzed 212 extremely obese children and adolescents, 82 normal-weight students, and 94 underweight students for two single nucleotide polymorphisms (SNPs: promoter -30G/A; exon 4a: silent 2061T/C) in the vicinity of the GLUT4 by polymerase chain reaction with subsequent restriction fragment length polymorphism analyses (PCR-RFLP) or single-strand conformation polymorphism analyses (SSCP). Allele and genotype distributions were similar in all study groups (all p values > 0.05). Hence, we did not detect association of any of the analyzed SNP alleles in the GLUT4 to different weight extremes, so these seem not to be involved in weight regulation in our study groups.

Is there an association between athletic amenorrhea and endothelial cell dysfunction?

PURPOSE: To test the hypothesis that young females with athletic amenorrhea and oligomenorrhea show signs of early cardiovascular disease manifested by decreased endothelium-dependent dilation of the brachial artery. METHODS: Ten women with athletic amenorrhea (mean +/- SE, age 21.9 +/- 1.2 yr), 11 with oligomenorrhea (age 20.8 +/- 1.1 yr), and 11 age-matched controls (age 20.2 +/- 1.1 yr) were studied. Study subjects were amenorrheic an average of 2.3 (range 0.6-5) yr and oligomenorrheic an average of 6.2 yr. All ran a minimum of 25 miles.wk. They were nonpregnant and free of metabolic disease. Brachial artery flow-mediated dilation (endothelium-dependent) was measured with a noninvasive ultrasound technique in each group. RESULTS: Endothelium-dependent brachial artery dilation was reduced in the amenorrheic group (1.08 +/- 0.91%) compared with oligomenorrheic (6.44 +/- 1.3%; P< 0.05) and eumenorrheic (6.38 +/- 1.4%; P< 0.05) groups. CONCLUSION: Athletic amenorrhea is associated with reduced endothelium-dependent dilation of the brachial artery. This may predispose to accelerated development of cardiovascular disease.

Cardiovascular screening practices in collegiate student-athletes.

OBJECTIVE: To evaluate screening practices and preparticipation evaluation (PPE) forms used to identify, or raise suspicion of, cardiovascular abnormalities in collegiate student-athletes. DESIGN: Phone and e-mail survey. SETTING: National Collegiate Athletic Association (NCAA) Division I universities. PARTICIPANTS: All 347 NCAA Division I universities were invited to participate in 2010-2011; 257 universities (74%) elected to participate. MAIN OUTCOME MEASURES: Information about the preparticipation screening process was obtained from team physicians and/or certified athletic trainers. PPE forms were evaluated for the inclusion of the 12 specific American Heart Association (AHA) recommendations for cardiovascular screening of competitive athletes from the 2007 AHA Council on Nutrition, Physical Activity, and Metabolism consensus panel endorsed by the American College of Cardiology Foundation. RESULTS: All 257 participating universities (100%) required preparticipation screening for freshman and transfer athletes, and 83 universities (32%) required an annual PPE for returning athletes. The PPE was performed on campus at 85% of the universities, whereas 15% of universities allowed the PPE to be completed by the athlete's choice of physician before he or she arrived on campus. Eleven universities (4%) used the recently updated American College of Sports Medicine 4th edition PPE. Sixteen universities (6%) used the American College of Sports Medicine 3rd edition PPE. The remaining 260 universities (90%) did not use either of these forms. Of the 257 Division I universities, only 21 universities (8%) met the AHA recommendations by including all 12 cardiovascular screening items on their PPE forms. CONCLUSION: The majority (92%) of NCAA Division I universities do not use PPE forms that meet the AHA recommendations for cardiovascular screening; therefore, they may not be effectively screening collegiate student-athletes for cardiovascular abnormalities that could lead to sudden cardiac death.

A proximal strengthening program improves pain, function, and biomechanics in women with patellofemoral pain syndrome.

BACKGROUND: It is hypothesized that patients with patellofemoral pain syndrome (PFPS) have hip and core muscle weakness leading to dynamic malalignment of the lower extremity. Thus, hip strengthening is a common PFPS treatment approach. PURPOSE: To determine changes in hip strength, core endurance, lower extremity biomechanics, and patient outcomes after proximally focused rehabilitation for PFPS patients. STUDY DESIGN: Case series; Level of evidence, 4. METHODS: Nineteen women (age, 22.68 ± 7.19 years; height, 1.64 ± 0.07 m; mass, 60.2 ± 7.35 kg) with PFPS participated in an 8-week program to strengthen the hip and core muscles and improve dynamic malalignment. Paired t tests were used to compare the dependent variables between prerehabilitation and postrehabilitation. The dependent variables were pain; functional ability; isometric hip abduction and external rotation strength; anterior, lateral, and posterior core endurance; joint range of motion (ROM; rearfoot eversion, knee abduction and internal rotation, and hip adduction and internal rotation); and peak internal joint moments (rearfoot inversion, knee abduction, and hip abduction and external rotation) during the stance phase of running. RESULTS: Significant improvements in pain, functional ability, lateral core endurance, hip abduction, and hip external rotation strength were observed. There was also a significant reduction in the knee abduction moment during running, although there were no significant changes in joint ROM. CONCLUSION: An 8-week rehabilitation program focusing on strengthening and improving neuromuscular control of the hip and core musculature produces positive patient outcomes, improves hip and core muscle strength, and reduces the knee abduction moment, which is associated with developing PFPS.