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3 Effects of Caloric Intake, Physical Activity and Hormonal Factors on Bone Health CALORIC/HORMONAL FACTORS Women in the military may be placed in situations or under conditions that are not optimal for the accrual or maintenance of peak bone mass. Conditions that induce estrogen deficiency from any cause, whether hormonal or due to caloric insufficiency, may adversely affect the skeleton. In military women, there is cause for concern about hypothalamic amenorrhea due to physical or emotional stress, excessive exercise and/or eating disorders, therapy with gonadotropin-releasing hormone (GnRH) agonists for the treatment of endometriosis, and the use of contraceptives that prevent menstruation; all of these factors may lower BMD and increase the risk for stress fractures. A decrease in hypothalamic GnRH leads to anovulation and increased bone resorption due to decreased estradiol secretion. Because military women are now eligible for most military occupational specialties, an increase in the time they spend in arduous, physically demanding situations may increase the
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incidence of hypothalamic amenorrhea. Women may eventually be eligible for participation in the Ranger training program1, in which soldiers are subjected to severe energy restriction. Concern about adhering to existing military standards for body weight and composition also may lead to disordered eating patterns2 that are known to adversely affect women's long-term bone health. Although exact numbers are not available for the military population, dietary energy restriction to maintain ''optimal" body weight is common in the civilian population, and young women entering the military may already be involved in chronic dietary practices that may negatively influence their nutrient and hormonal status and thereby their bone health (IOM, 1998). Effects of Low Energy Intake on Hormonal Levels and Bone Health The impact of low energy intake on the hormonal milieu in young women of military age is well documented. Kurzer and Calloway (1985) showed that a decrease in energy intake to 43 percent of need for only 1 month resulted in menstrual abnormalities in two of six subjects, with decreases in circulating estrogen and progesterone. Hypoestrogenemia or luteal suppression (shortened luteal phase of the menstrual cycle with reduction in progesterone secretion) was also found in female athletes (ACSM, 1997), in whom high energy outputs are often coupled with lower than expected energy intakes (Mulligan and Butterfield, 1990). Female athletes who are amenorrheic also demonstrated suppressed insulin release (Laughlin et al., 1994), elevated growth hormone (Laughlin et al., 1994), mildly elevated cortisol levels (Loucks, 1989) in conjunction with low tri-iodothyronine (T3) (Loucks et al., 1992), and high levels of IGF-1 binding protein (Laughlin et al., 1994), all of which may adversely affect bone turnover and the accrual of peak bone mass. Several investigators have documented low bone mass in young women athletes, especially those who are amenorrheic (Drinkwater et al., 1984) and have low energy intakes (Marcus et al., 1985). The complete etiology of the hormonal changes that may accompany strenuous athletic activity is unknown. (The decrease in luteal phase length has been associated with a reduction in luteinizing hormone [LH] pulsatility and an increase in pulse height, a response thought to originate at the level of the hypothalamus [Loucks, 1996] via changes in the pulsatile secretions of GnRH.) However, the interactions resulting in decreased GnRH pulsatility are unknown. Loucks and colleagues (1989) have shown that the disrupted LH pulsatility is present in normally menstruating female athletes as well as those who are amenorrheic and have proposed the concept of decreased energy availability to explain this and other aspects of the syndrome. They speculate that the disruption in menstrual function that accompanies exercise is akin to that 1 The U.S. Army Ranger training program is a physically and psychologically demanding program used by the Army to screen male officers and enlisted soldiers for entry into special operations units. The training consists of three 3-wk phases conducted at widely varying sites with differing physical demands: military base training, mountain training, and swamp training. 2 Disordered eating describes a wide spectrum of harmful behaviors in a continuum between over- and undereating where abnormal measures are taken to control weight (e.g., bingeing, purging, dieting, and restricting food intake) (ACSM, 1997).
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associated with fasting or starvation, where energy intake is insufficient to meet metabolic demands (Loucks, 1996). The concept of energy availability is based on the understanding that mammals divide their energy intake among a variety of energy-requiring functions, including cellular maintenance, thermoregulation, motor activity, growth, reproduction, and storage, with this order representing the hierarchy of function (Wade and Schneider, 1992). When energy intake is limited, functions at the top of the hierarchy are performed at the expense of those at the bottom. Thus, optimal menstrual function requires a minimal amount of available energy. When activity is high, the energy available for menstrual function may be compromised unless energy intake is appropriately adjusted. At the workshop, Loucks (1997) presented data illustrating her attempts to dissect the relationship between activity level and energy intake in order to explain this phenomenon. In a series of short-term and acute studies (4–5 days in duration) in eumenorrheic sedentary women (Loucks and Callister, 1993) and eumenorrheic active women (Loucks et al., 1994), in whom exercise and energy intake were manipulated to limit energy availability, even this short period of low energy availability resulted in changes in LH pulsatility and suppression of T3 levels. She has also demonstrated that exercise has no further effect beyond that of decreasing energy availability (Loucks and Callister, 1993). The suppression of T3 and the changes in LH pulsatility occurred at a threshold level of energy availability (operationally defined as dietary energy intake minus exercise energy expenditure) of 20 to 25 kcal/kg lean body mass in women (Loucks and Heath, 1994). Unpublished data presented at the workshop suggested that a similar low energy availability in men resulted in no change in LH pulsatility, although other endocrine changes were similar to those seen in women. In additional experiments on physically active women, Williams et al. (1995) have shown similar results. Active eumenorrheic women experienced suppressed LH pulsatility after only 3 days of training when dietary energy intake was reduced. This condition reversed itself when the dietary intake was appropriately increased. Further support for the concept that the hormonal changes accompanying amenorrhea in female athletes derive from low energy availability comes from the report of Dueck et al. (1996). In a pilot study, they evaluated LH pulsatility and cortisol secretion in three eumenorrheic women athletes as compared with the same parameters in an amenorrheic athlete. This athlete was treated by increasing energy intake by approximately 350 kcal/d and decreasing training by 1 d/wk, with an increase in net energy availability of about 250 kcal/d. At the end of 15 weeks, all athletes were again tested. In the previously amenorrheic athlete, LH pulsatility had returned to match the normal pattern, cortisol secretion had fallen to within normal limits, and normal menstrual function had returned. Effect of Dieting and Weight Loss on Bone Health Independent of menstrual dysfunction, weight loss may decrease BMD. Substantial weight loss due to reduced energy intake in overweight postmenopausal women was associated with a significant loss of total-body BMD (Compston et al., 1992; Jensen et al., 1994; Sevendsen et al., 1993). In young women, moderate dieting at a level of 27 percent energy restriction resulted in a
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3.4 kg weight loss, a 0.7 percent decrease in total-body BMD, and a 0.5 percent decrease in lumbar spine BMD (Ramsdale and Bassey, 1994). However, the above studies examining the effect of weight loss on bone mineral should be interpreted cautiously, because changes in total-body bone mineral measured by older software versions of DXA instruments may have been erroneous if considerable change in soft tissue composition occurred (Svendsen et al., 1993). Incidence of Caloric Restriction and Disordered Eating Patterns in Military Women Because stress fractures occur primarily during basic training, it would be useful to know the dietary practices of women who enter into the military to determine if caloric restriction and disordered eating patterns are related to the incidence of stress fractures. Most reports of diagnosed eating disorders in the civilian population place the incidence of anorexia nervosa at 0.5 to 1 percent by the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV, 1994) criteria and that of bulimia nervosa at 1 to 4 percent of the women studied. Others have suggested that subclinical eating disorders are significantly more prevalent in the 18- to 24-year old age group (Beals and Manore, 1994; Sundgot-Borgan, 1993). Clinical eating disorders appear to be rare among military women, but representative data are not available on the prevalence of disordered eating patterns among these women. Interpretation of data from the military is complicated by the policy that, until recently, defined eating disorders as grounds for dismissal (IOM, 1998). Thus, attempts to assess disordered eating of any kind in the past have been inadequate and probably have underestimated the problem. However, the emphasis on appearance, which is formalized in DoD documents (U.S. Department of Defense Directive 1308.1, 1995; U.S. Department of Defense Directive 1308.3, 1995, U.S. Department of the Army AR 600-9, 1986), is a risk factor for development of such conditions. The Perception of Wellness and Readiness Assessment (POWR'95) of Navy and Marine Corps personnel, conducted in 1995, employed questions from the Eating Disorders Inventory, a validated tool that has been shown to have predictive value in assessing risk of disordered eating (Garner and Olmstead, 1991). POWR'95 revealed that 11 percent of women respondents used diet pills to lose or maintain weight, 13 percent ate in secret, and 50 percent were dissatisfied with their weight. These three factors are most predictive of disordered eating (especially bulimia) (Hourani, 1996). Respondents to this same survey indicated a 1.5 percent incidence of bulimia at some time in their lives and a 1.2 percent incidence at the time of the survey. In a recent report by Lauder (1997), 33.6 percent of 423 active-duty women in the Army were judged to be at risk for disordered eating, and 8 percent fulfilled the criteria for disordered eating. Fewer than 1 percent had anorexia nervosa or bulimia. As mentioned above, these data may significantly underestimate the incidence of these eating patterns in the military. A similar study of Navy midshipmen answering similar questions suggested that 10 percent of the women and 3.5 percent of the men were at risk for disordered eating patterns (Drake, 1996). Results of these surveys as well as others (Survey of Health Related Behaviors among Military Personnel, 1995; Survey of Nutrition Knowledge of Active-Duty Navy Personnel, 1990) have suggested that the prevalence of overweight among active-duty women is at least comparable to that of a similar population of civilian women. Service-wide, 25 to 50 percent of the women
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surveyed reported that they exceeded the weight standards set for their own branch of the service. However, the surveys also demonstrated that the percentage of active-duty women who are dieting and/or dissatisfied with their weight3 (40-80% in the regular forces) is significantly higher than the percentage of women who are actually overweight. In young recruits participating in basic training or in the U.S. Military Academy at West Point, the percentage of women dieting was equally high (60% and 74%, respectively), which suggests an early establishment of a food intake pattern that might jeopardize bone health (Klicka et al., 1993). The requirement to meet military weight standards every 6 months may induce "crash" or chronic dieting and weight cycling (repetitive episodes of weight loss followed by weight gain). In addition, the activity level that accompanies, first, basic training and, then, the day-to-day activities of a fighting soldier (Army women have been estimated to expend 1,300 kcal/d in exercise [Hourani, 1996]) may put the female soldier at continued risk of amenorrhea. Drake (1996) reported that 10 to 15 percent of female midshipmen become oligomenorrheic within the first year at the U.S. Naval Academy, and 5 to 6 percent develop full amenorrhea. Lauder (1997) reported that among 423 active-duty women, 2.2 and 3.3 percent were amenorrheic and oligomenorrheic, respectively, excluding women on hormonal birth control. Hypothalamic Amenorrhea and Bone Health Premature bone demineralization occurs in women with hypothalamic amenorrhea and oligomenorrhea associated with eating disorders and strenuous physical activity. This complex syndrome has been referred to as the female athlete triad (ACSM, 1997; Bennell et al., 1995). In young women with amenorrhea associated with weight loss, BMD loss occurs soon after amenorrhea develops. Hypoestrogenic amenorrhea has been correlated with the age of onset of menstruation, the duration of amenorrhea, and low body fat mass. Although fat stores are an important component of energy balance, there is no convincing evidence that body fat has a direct causal role in regulating ovulation (Loucks, 1996). In a randomized trial, 24 young women with hypothalamic amenorrhea or oligomenorrhea were treated with oral contraceptives, medroxyprogesterone, or a placebo for 12 months (Hergenroeder et al., 1997). In amenorrheic subjects receiving oral contraceptives, lumbar spine, and total BMC and BMD were higher at 12 months compared with those on medroxyprogesterone, or the placebo. In oligomenorrheic subjects treated with medroxyprogesterone, no detectable improvement in BMD was seen. In another randomized trial, 48 amenorrheic young women with anorexia nervosa received estrogen and progestin, or no replacement, and were re-evaluated 18 months later (Klibanski et al., 1995). No significant change was seen in BMD in the treated versus the placebo group; however, a 4 percent increase in BMD was observed in treated patients whose initial body weight was less than 70 percent of ideal. Despite this partial protection, estrogen and progestin administration did not reverse the osteopenia seen in these young, amenorrheic women, which emphasizes the multifactorial etiology of the anorexia syndrome. Energy restriction, low body weight, body fat 3 Based on self-reported weights and heights (IOM, 1998), the prevalence rates for underweight (BMI < 19.0) ranged from 3.6 percent for Navy women to 6.8 percent for Marine Corps women.
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depletion, and nutritionally dependent hormones (i.e., hormones such as thyroid, cortisol, GH, and IGF-1 whose synthesis or secretion is dependent on energy-protein intake) together with the steroid hormones interact to influence BMD. Possible Effects of Excessive Exercise on Bone Health In general, exercise promotes bone mineralization, but the beneficial effect of exercise on BMD can be lost, and significant bone loss can result if exercise training is excessive (Hergenroeder, 1995). Regular recreational exercise at or above a basic conditioning level does not increase infertility or disturb the menstrual cycle, but abrupt, large changes in exercise frequency or intensity, or excessive exercise resulting in weight loss, can disturb menstrual function, resulting in hypoestrogenic amenorrhea, anovulatory cycles, and luteal phase deficiency (Clapp and Little, 1995). A strenuous running program in untrained women with normal cycles induced menstrual disturbance within 1 month in the majority of subjects (Bullen et al., 1985). Although not a prerequisite for bone loss, the additional stress of body weight loss, superimposed during the training program, increased the severity and frequency of menstrual changes. Estrogen production, not progesterone, appears to be the most important hormone in maintaining bone mass in women with menstrual cycle disturbances, such as short luteal cycle (De Souza, 1997). Subtle disturbances associated with running such as decreased follicular phase estradiol also appear to be related to bone loss. Reductions in circulating estrogens characteristic of the female athlete triad are of clinical concern. The extent to which amenorrhea limits the skeletal response to mechanical loading is not clear. In postmenopausal women, resistance training combined with hormone replacement therapy led to substantial and unprecedented rises in vertebral BMD (Notelovitz et al., 1991). In another study of amenorrheic runners, those receiving hormone replacement therapy increased bone density during training, while those not receiving treatment did not experience an increase in bone density (Cumming, 1996). Vigorous exercise, hypogonadism, and leanness in women with athletic amenorrhea may not be associated with generalized osteoporosis. Young and colleagues (1994) studied 44 ballet dancers with amenorrhea or oligomenorrhea, 18 sedentary amenorrheic girls with anorexia nervosa, and 23 girls with regular menstrual cycles. BMD was normal or elevated at weight-bearing sites (trochanter) in dancers, and it was normal or reduced at these sites in sedentary amenorrheic girls. BMD at non-weightbearing sites was reduced in dancers, similar to sedentary amenorrheic girls. Weight-bearing exercise may offset effects of hypogonadism at predominantly cortical weight-bearing sites such as proximal femur. Nonweight-bearing sites with substantial trabecular bone, such as lumbar spine, may be adversely affected by hypogonadism. Resumption of menses in athletes results in a gain in bone density; however, their values are still less than that of eumenorrheic counterparts. As the length of the amenorrheic period is prolonged, bone loss can occur at weight-bearing sites that are largely cortical bone (Rencken, 1996).
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SUMMARY Conditions that induce estrogen deficiency from any cause, such as energy insufficiency either as a result of dieting or excessive physical activity, may adversely affect bone health. Whether continued disruption leads to the phenomenon of athletic amenorrhea is not known; however, normal reproductive hormone secretion can be reinstated in amenorrheic women athletes simply by increasing the energy intake. Some of the hormonal changes of athletic amenorrhea are similar to those created by imposing a state of low energy availability on sedentary or active women, namely, suppression of T3 secretion and alteration in LH pulsatility. In addition, it has been shown that abnormal cortisol secretion associated with the amenorrhea (which may negatively influence bone health) can also be corrected by increasing energy intakes. Oral contraceptives may also afford protection from loss of bone minerals in some women The extent to which amenorrhea limits the skeletal response to mechanical loading is not clear. In general, exercise promotes bone mineralization, but the beneficial effect of exercise on BMD can be lost, and significant bone loss can result if exercise training is not matched by adequate caloric intake. The prevalence of overweight among active-duty women is at least comparable to that of a similar population of civilian women. A large percentage of military women surveyed reported that they exceeded weight standards, and even a larger percentage reported they are dieting or dissatisfied with their weight (IOM, 1998). Premature bone demineralization occurs in women with hypothalamic amenorrhea and oligomenorrhea associated with eating disorders as well as with strenuous physical activity. Eating disorders are rare among military women; however, representative data are not available on the prevalence of disordered eating patterns among military women. In a recent report, one-third of the Army active-duty women studied were documented to be at risk of disordered eating, and 8 percent fulfilled the criteria for disordered eating.
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