What is Osteoporosis?
Osteoporosis is the most common human bone disease and is characterized by low bone mass or bone mineral density (BMD) and loss of bone tissue [3]. Bone is living tissue and it is constantly undergoing remodeling where old bone is replaced by new bone. Osteoporosis develops when the bone that is lost is not replaced by new bone. This results in a decreased bone mass and the increased risk for fractures. Osteoporosis is defined by the amount of BMD at any skeletal site. “Normal” is defined as having a BMD within 1 standard deviation of a “young normal” adult. Osteopenia is having a BMD between 1 and 2.5 standard deviations below a “young normal” adult. Osteoporosis is having a BMD 2.5 standard deviations or more below a “young normal” adult. Severe or established osteoporosis occurs in osteoporotic women who have already had one or more fractures. The many common causes of osteoporosis range from lack of physical stress (exercise) on the bones, malnutrition, lack of estrogen, and old age [4]. Osteoporosis is seen as a disease that primarily concerns women as they enter their postmenopausal years because of their decreasing levels of estrogen. Estrogen causes increased osteoblastic (bone formation) activity and after menopause, no estrogen is secreted from the ovaries [4]. But since the recognition of the development of The Female Athlete Triad, osteoporosis, osteopenia, and stress fractures are now a concern for much younger women.

How Osteoporosis Is Involved in The Female Athlete Triad
Emotional stress, disordered eating, and energy deficits can affect the hypothalamus in women and cause a decrease in gonadotropin-releasing hormone (GnRH) [1]. The decrease in GnRH results in a decrease in all of the hormones that are necessary for menstruation and this leads to functional hypothalamic amenorrhea (FHA). These low concentrations of estrogen in amenorrheic athletes are associated with reduced bone mass and increased rates of bone loss. The estrogen levels of amenorrheic athletes is similar to that of postmenopausal women [5]. In a comparison of BMD in amenorrheic and eumenorrheic (normally menstruating) athletes, vertebral mineral density was significantly lower in the amenorrheic group than in the eumenorrheic group. The amenorrheic group had a lower mean estradiol concentration (amenorrheic group, 38.58 pg per milliliter; eumenorrheic group, 106.99 pg per milliliter) and progesterone peak (amenorrheic group, 1.25 ng per milliliter; eumenorrheic group, 12.75 ng per milliliter) than the eumenorrheic women. A three-day dietary history showed no significant differences in nutritional intake, including calcium, with and without supplements. The two groups were similar in percentage of body fat, age at menarche, years of athletic participation, and frequency and duration of training but differed in number of miles run per week (amenorrheic group, 41.8 miles; eumenorrheic group, 24.9 miles) [6]. In another study on amenorrheic and eumenorrheic runners, bone mass was found to be reduced by 20% in the amenorrheic group [7].

Factors Affecting Bone Mass
Of course, not all amenorrheic athletes have a low bone mass [1]. Many factors can affect bone mass like peak bone mass reached before amenorrhea, the length and severity of menstrual irregularity, the type of loading during exercise, the frequency and intensity of exercise, nutritional status, weight, and genetics. A concern with amenorrheic adolescents is that they are losing bone mass at a crucial time in their lives. It is well known that bone mass increases during childhood and accelerates during adolescence. Bone mass was assessed in a study of 207 healthy caucasian boys and girls, aged 9-18 yr. In females, but not in males, a dramatic reduction in bone mass growth was observed after 15 years of age. This sharp reduction occurred between the second and fourth years after menarche. The researchers demonstrated that almost all of the maximal adult bone density is reached by 15-16 years of age in female adolescents [8]. Therefore, if an adolescent is amenorrheic at a time when bone mass accumulation is optimal, they may be predisposing themselves to osteoporosis in their later years, regardless of menstrual status, nutrition, or exercise [9].
The relationship of prior menstrual irregularities and current menstrual status to bone density showed that vertebral bone density was significantly related to menstrual patterns. Women with no history of menstrual cycle irregularity had higher lumbar densities than those with a history of oligomenorrhea (irregular menstruation) and amenorrhea. These data suggest that extended periods of oligomenorrhea/amenorrhea may have a residual effect on lumbar bone density [10].

Consequences of Osteoporosis
Although exercise is considered to be protective on bone density, excess exercise is associated with bone loss and the risk of fractures [11]. Athletes with stress fractures are more likely to have lower bone density, lower dietary calcium, current menstrual irregularity, and lower oral contraceptive use [12]. Additionally in amenorrheic women, the physiochemical signal that stimulates bone to mineralize seems to be absent. This suggests that even the quality of bone is affected [9]. Unfortunately, the bone damage from amenorrhea may not be reversible. In a study involving athletes who regained menses after an increase in weight and decrease in training distance, their bone density increased 6% after 14 months, slowed to 3% in the second year, and then plateaued at a level that was below normal for their age. After four years, they still had not reached normal bone mass [13].

Untangling the Web of The Female Athlete Triad
All of the evidence points to prevention as the key to untangling the web of The Female Athlete Triad. Early recognition and therapy require a multidisciplinary approach that can prevent serious complications, and perhaps, even death. Overall, a majority of women receive significant health benefits from regular exercise and should be encouraged to adopt regular physical activity in their lives [1]. This series of articles is not meant to discourage athletic participation, rather it is to educate and inform about a growing trend, and hopefully, prevent or stop the trend from becoming an athletic woman’s epidemic.

References
1. Otis, C.L., et al., American College of Sports Medicine position stand. The Female Athlete Triad [see comments]. Med Sci Sports Exerc, 1997. 29(5): p. i-ix.
2. West, R.V., The female athlete. The triad of disordered eating, amenorrhoea and osteoporosis. Sports Med, 1998. 26(2): p. 63-71.
3. National Osteoporosis Foundation Physician's Guide To Prevention and Treatment of Osteoporosis. 1998: http://www.nof.org.
4. Guyton, A.C. and J.E. Hall, Textbook of Medical Physiology. Nineth ed. 1996, Philadelphia: W.B. Saunders Company.
5. Reeder, M.T., et al., Stress fractures. Current concepts of diagnosis and treatment. Sports Med, 1996. 22(3): p. 198-212.
6. Drinkwater, B.L., et al., Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med, 1984. 311(5): p. 277-281.
7. Cann, C.E., et al., Decreased spinal mineral content in amenorrheic women. Jama, 1984. 251(5): p. 626-629.
8. Bonjour, J.P., et al., Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab, 1991. 73(3): p. 555-563.
9. Warren, M.P., Health issues for women athletes: exercise-induced amenorrhea. J Clin Endocrinol Metab, 1999. 84(6): p. 1892-1896.
10. Drinkwater, B.L., B. Bruemner, and C.H.d. Chesnut, Menstrual history as a determinant of current bone density in young athletes. Jama, 1990. 263(4): p. 545-548.
11. Marcus, R., et al., Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med, 1985. 102(2): p. 158-163.
12. Myburgh, K.H., et al., Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med, 1990. 113(10): p. 754-759.
13. Drinkwater, B.L., et al., Bone mineral density after resumption of menses in amenorrheic athletes. Jama, 1986. 256(3): p. 380-382.