Bone Health in Highly Trained Female Athletes:

A review of the current state of knowledge.

Introduction

Highly trained female athletes are often at peak cardiovascular fitness but face important threats to their skeletal health. Women who train intensively may produce abnormally low levels of estrogen, which may lead to weakened bones. Low bone strength, or "osteopenia", is a risk factor for stress fractures (1,2,3). Young adults with osteopenia are also more likely to develop osteoporosis later in life (4).

Exercise, estrogen-deficiency, and menstrual irregularity.

Regular vigorous exercise is associated with decreased estrogen levels in the blood (5,6,7). In one study (6), healthy women who began training for a marathon reduced their estrogen levels by over 50%. Low estrogen levels result in menstrual irregularity in a large proportion of intensively training athletes. Irregularities can include a late onset of menstrual periods, infrequent or absent periods, or more subtle abnormalities, such as shortened luteal phase and anovulatory cycles. We recently surveyed competitive collegiate cross country runners and found that 56% missed several menstrual periods a year or had no periods at all. The cause of estrogen-deficiency and menstrual irregularity in athletes is not known with certainty, but risk factors include earlier onset of training, more intense training, psychological stress, nutritional inadequacy, low body weight, low body fat mass, and changes in body composition (8).

Estrogen and bone

Estrogen is essential for maintaining bone health in women. Events that result in rapid declines in a woman's estrogen level, such as menopause and ovariectomy (the removal of the ovaries), also result in rapid losses in her bone mass and bone strength. These losses can be prevented by estrogen treatment (9,10,11). Young women who develop hormonal conditions that cause estrogen deficiency, such as hyperprolactinemia, gonadal failure, and premature ovarian failure, also stop menstruating and lose bone (12-15). The extent of the bone loss in these women is directly proportional to the length of time that they have been without a period (15). Various estrogen replacement therapies have been shown to increase bone in these women (16-18).

Diet and bone

It is likely that poor nutrition and disordered eating adds to the risk of bone health problems in female athletes. Low body weight and a lean physique are desirable attributes in many sports, such as gymnastics, dancing, figure skating, and running. Athletes striving to excel in these sports may develop disordered eating patterns that contribute to both their menstrual irregularities and to the weakened state of their bones. Proper nutrition is essential for normal menstruation and for healthy bone; non-athletic women who are malnourished, such as women with anorexia nervosa, will develop amenorrhea (the absence of a menstrual period), osteopenia, and even osteoporosis (19,20,21). The combination of disordered eating, amenorrhea, and osteoporosis has been termed the "female athlete triad" (22).

Exercise-associated menstrual irregularity and bone

Because exercise is normally beneficial to bone, it has been hypothesized that women athletes may escape bone loss even if they develop menstrual irregularities. However, studies show that this is not the case for most sports. Nineteen studies have been conducted in which the bone strength (measured as bone density) of normally menstruating women was compared to the bone strength of athletes with irregular or absent periods ("amenorrheic" or "oligomenorrheic" athletes). Fifteen of these studies showed that bone density was significantly lower in amenorrheic and/or oligomenorrheic athletes (23-37). Three of the four remaining studies (38-41) showed a trend towards lower bone density in amenorrheic/oligomenorrheic athletes that was not statistically significant (38-40).

Women in late adolescence and early adulthood should still be building bone. Studies that measure athletes at a single time point cannot tell us if osteopenic athletes simply halt this building process or if they also break down existing bone. However, three studies have been conducted in which amenorrheic/oligomenorrheic athletes were measured yearly (42-44). These studies found that amenorrheic athletes in their late teens and early twenties not only fail to gain, but actually begin to lose bone.

The magnitude of bone loss is serious. Amenorrheic/oligomenorrheic athletes have 8-31% lower bone density than normally-menstruating athletes, and 3-24% lower bone density than non-exercising, normally-menstruating controls (23-37). Alarmingly, many of these women have extremely low bone mass; some have bone densities comparable to women in their 70's and 80's (32,36).

Most studies have considered athletes with infrequent or absent periods (oligomenorrhea or amenorrhea) and have not evaluated athletes with more subtle menstrual disturbances. However, one study found that runners who menstruate monthly but who have anovulatory cycles and/or shortened luteal phase also lose bone (45). This study is of particular interest because it demonstrates that highly training females who appear to be menstruating normally may still be at risk for osteopenia; asymptomatic hormonal changes and menstrual disturbances may be sufficient to cause bone loss.

Several studies show that the lower an athlete's estrogen level falls and the longer that her menstrual irregularity persists, the greater the deficits in her bone (26,27,34,36). These observations suggest a direct relationship between a low estrogen state and bone loss. In theory, then, the establishment of normal estrogen levels should prevent and even reverse bone loss. Oral contraceptives (birth control pills) provide estrogen and regulate the menstrual cycle; thus, it has been hypothesized that oral contraceptives can be used to strengthen the bones of women athletes. However, this hypothesis has never been formally tested.

Stress fractures and menstrual irregularity

Stress fractures plague young female athletes. In our recent survey of competitive collegiate cross country runners, 44% had experienced at least one stress fracture and 21% had suffered multiple stress fractures. Stress fractures may be related to estrogen deficiency and menstrual irregularity. Several studies report an association between current menstrual irregularity and stress fracture incidence among female athletes (5,23,25,46,47). Two studies (2,48) also found that a history of menstrual irregularity is a risk factor for stress fractures. These studies found that stress fracture risk was 2-4 times greater for amenorrheic/oligomenorrheic athletes than for normally-menstruating athletes.

Oral contraceptive use and stress fractures

Oral contraceptives may be protective against stress fractures. Four retrospective studies found that female athletes who took oral contraceptives had suffered 2-4 times fewer stress fractures than non-users (1,5,47,48). These studies suggest that oral contraceptive use reduces stress fracture incidence. However, these studies cannot establish a cause and effect relationship. For example, the women who chose to take oral contraceptives may have had greater bone mass before they started taking oral contraceptives. A randomized trial is urgently needed to establish if oral contraceptives can prevent bone problems in female athletes.

Reversibility of bone loss

Few studies have evaluated long-term outcomes for athletes with menstrual irregularities and low bone density. Three studies that followed amenorrheic athletes over time found that some recovery of bone mass can occur (42-44); athletes who gained weight, decreased training, and resumed menses (concomitant with increased estrogen levels) had bone density gains of 3-9% over the first year. However, formerly amenorrheic athletes still had significantly lower bone density compared to controls, suggesting that bone health may be permanently compromised if intervention is initiated too late. The longest study to follow previously amenorrheic/oligomenorrheic athletes lasted eight years (42). Despite the return of regular menstrual periods for several years, the bone density of formerly amenorrheic/oligomenorrheic athletes remained 15% less than the bone density of athletes who had never been amenorrheic. This suggests that some bone loss may be irreversible and that
early intervention is crucial.
 

Glossary

amenorrhea - The absence of a menstrual period, or less than 4 periods per year.

anovulatory cycle - A disturbance of the menstrual cycle in which ovulation (the release of an egg from the ovary to the fallopian tube) does not occur.

bone density - A measure of bone strength.

eumenorrhea - Having a normal number of menstrual periods per year (10 -13).

oligomenorrhea - Infrequent menstruation, 4 -9 periods per year.

osteopenia - Having abnormally low bone mineral density for one's age.

ovariectomy - Surgical removal of the ovaries.

randomized trial - A type of study in which subjects are randomly assigned to either a treatment or control group and then are monitored over time as to their progress. This type of study can be used to establish causality between a treatment and an effect.

shortened luteal phase - A type of menstrual irregularity in which the luteal phase of a woman's menstrual cycle lasts for an abnormally short amount of time.
 

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