British Medical Bullttm (19W) Vol. 48, No. 3, pp. 546-560 O The British Council 1992

Exercise, amenorrhoea and the skeleton R J Carbon Department of Sports Medicine, London Hospital Medical College, London, UK

One of the accepted benefits of regular exercise is the development of increased bone mineral density (BMD) and hence a skeleton more capable of withstanding the rigours of physical activity throughout life. However an apparent paradox is seen in the observed decrease in lumbar BMD in female athletes who experience menstrual disturbance and athletic amenorrhoea (AA). Despite high levels of activity these athletes suffer the consequences of hormonal deficiency and are at risk of not achieving peak BMD and experiencing further bone loss. It is increasingly evident however that exercise itself continues to exert a protective effect of maintaining BMD at skeletal sites under physical stress. The observed increase then of stress fractures at these sites in amenorrhoeic athletes remains unexplained.

PHYSICAL ACTIVITY AND THE SKELETON Physical activity is the primary determinant of changes in BMD in weightbearing bones.1 As a group, weightbearing athletes have increased BMD compared with the general population,2'3 and young army recruits have been shown to increase BMD over a 3 month training programme.4 Furthermore, muscle mass and strength are positively correlated with BMD. 5 Elderly patients demonstrate a decrease in the rate of bone loss in die majority of studies on physical activity as an intervention for osteoporosis,6 although diis effect is not as great as tfiat of exercise increasing BMD in youth.7 Exercise tends to exert maximal effect at those sites actively stressed. Tennis players can develop up to 35% greater bone mass in their playing arm compared with their non-dominant arm,8 and runners develop increased bone mass in the calcaneum.9

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Inactivity and immobilization have a negative impact on the skeleton, resulting in rapid and sustained loss of bone mass. Mazess and Whedon10 concluded that neither endocrine nor dietary intervention can compensate for inactivity. Patients bed-rested after spinal surgery have been shown to lose bone density at a rate as high as 2% per week11 and animal research has demonstrated loss of 50% of metacarpal bone mass after 6 months of cast immobilization in dogs.12 Astronauts subject to weightlessness lose approximately 4% of calcaneal bone mass per month and after prolonged stays in outer-space have been unable to recover to normal levels even after several years.13 PHYSIOLOGICAL RESPONSES OF BONE The capacity of bone to respond to physical stress is in accordance with Wolff's law, defined by the German anatomist one hundred years ago; every change in environment is followed by change in internal architecture,14 that is: FORM FOLLOWS FUNCTION The capability of bone tissue to respond to mechanical strain lies in the development of streaming potentials (charge separation) in response to forces imposed by muscular activity and gravity. Bone stressed in tension develops electropositivity while compression results in electronegativity. Osteoblastic bone forming cells are activated in electronegativity and osteoclastic bone resorbing cells are activated in electropositivity. Hence any bone subject to bending stress will increase bone density along the lines of compressive force. This is evident in the cortical thickness of a long bone as well as the trabecular patterns at the end of long bones. Osteoclastic resorption precedes new bone formation during remodelling.15 Excessive and repetitive mechanical stimulus, and hence resorption exceeding formation, may result in stress fracture. BONE COMPOSITION Bone is composed of a mineral, hydroxyapatite formed mostly by calcium phosphate crystals; the organic ground substance of osteoid formed primarily of collagen; and water, all in approxi-

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mately equal volumes. The skeleton is composed of 80% cortical and 20% trabecular bone. Bone quantity is currently assessed by measurement of calcium hydroxyapatite. Bone densitometry techniques such as single photon absorptiometry can measure bone mineral content (BMC g/cm) which is the total amount of calcium hydroxyapatite present in a given bone. Alternatively the amount of bone mineral per unit of cross-sectional area can be measured by dual photon absorptiometry or dual energy X-ray absorptiometry (DEXA) as the bone mineral density (BMD g/cm2). Computed tomography can also be used to measure BMD at considerably higher radiation cost (approximately 50 times greater) to the patient. Currently there are no techniques to measure the osteoid content or configuration of bone. Nor does measurement of BMD give any indication of the rate of active resorption and formation within the bone. One study has attempted to address this factor and found that similar BMD was associated with vastly different cellular function found on bone biopsy at the iliac crest.16

DETERMINANTS OF BONE DENSITY The bone density of any individual at any given age is determined by genetic, environmental and hormonal factors (Fig. 1). Genetic factors are evidenced by the familial predisposition to osteoporosis, and the increased bone mass and lower rates of osteoporosis in negroids compared with caucasions. Environmental factors include activity and nutrition. Total energy and calcium intake are limitators of optimal bone growth in that deficiency will result in decreased bone density, but excessive intake will not increase it.17 Currently recommended intake of calcium is 800 mg per day for young women and 1500 mg for postmenopausal (and amenorrhoeic) women.18 Obesity is associated with increased bone mass, although this may be related to the added weightbearing forces. Hormonal determination of bone mass includes the triad of parathyroid hormone, osteocalcin and calcitonin which all interact to control serum calcium levels. Growth hormone and testosterone define bone length as well as density and are responsible for the increased bone size and mass in men. Sex steroids are important determinants of bone density in women. Oestrogen delays bone resorption and decreases the rate of remodelling, and progesterone has also recently been shown to

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MENOPAU8E

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AVERAGE BONE DENSITY POSSIBLE CHANGES M BONE DENSITY WITH 0 REGULAR ACTIVITY

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— — H I ) LONG TERM AMENORRHOEA NOTE •> THE 8UDOEN DECLINE AT MENOPAUSE WHICH CAN BE LE88ENEO BY REGULAR ACTIVITY b) THE FRACTURE THRESHOLD OF BONE DENSITY AT WWCH FRACTURES CAN OCCUR WITH MMMAL TRAUMA

Fig. 1 Bone density in women throughout life. (Modified from the authors' chapter in: Bloomfield J, Flicker PA, Fitch KD, eds. Textbook of Science and Medicine in Sport. Oxford: Blackwell, 1992: ch. 23).

have a bone trophic function.19'20 Trabecular bone, which has a higher turnover rate, appears most sensitive to hormonal flux while cortical bone is influenced to a lesser extent in the presence of physical activity. Long-term skeletal integrity is jeopardised by loss of trabecular spicules which, once atrophied and broken cannot be reformed, although remaining spicules and cortical bone can hypertrophy.

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OSTEOPOROSIS Osteoporosis is the quantitative deficiency of bone density which predisposes an individual to fractures of minimal trauma. It develops into old age, both as a result of the age-related decline of bone density of about 1 % per year coupled with the abrupt increase in bone loss in women of up to 8% per year at the menopause. Fracture threshold is that bone mass at which minimal trauma is likely to result in fracture. Peak bone mass, achieved by the fourth decade, is important in attenuating the effects of bone loss in later life. Young people, especially girls, should be encouraged to eat well and exercise regularly throughout the growing years to optimise their BMD. This presents the apparent enigma that female athletes who experience amenorrhoea have been shown to have decreased spinal BMD despite high levels of activity. ATHLETIC AMENORRHOEA Athletic Amenorrhoea (AA) is a form of hypothalamic amenorrhoea and as such can be described as 'hypogonadotrophic hypogonadism' in which the ovaries fail as a result of decreased stimulation from pituitary gonadotrophins, which in turn are understimulated by hypothalamic releasing hormones. Regular menses are dependent on accurately timed pulses of gonadotrophin-releasing hormone (GnRH). Pulse intervals of 60-90 minutes result in a steady pulsed release of follicle stimulating hormone (FSH) and increasing pulses of luteinizing hormone (LH) from the pituitary gland during the follicular phase of the cycle. Appropriate oestrogen secretion and formation of an ovarian follicle is dependent on the correct ratio of FSH to LH with the mid-cycle LH surge resulting in ovulation. The remaining corpus luteum secretes progesterone and a luteal phase of at least 10 days follows in preparation for fertilization and pregnancy. Alternatively, the corpus luteum degenerates and menses ensue some 28 days after the hormonal interplay began (Fig. 2). The changes of AA are currently believed to be due to an abnormal rate of pulsatile GnRH secretion. The rate of pulses may be increased or decreased. Pituitary FSH secretion is decreased and the LH surge is inadequate both in intensity and duration. Ovarian function becomes depressed with lower oestradiol (E2) secretion and an inadequate (shorter in length with lower progesterone levels) luteal phase. Ultimately the LH surge may

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Hypothalamus.

Secondary sex characteristics

Menstruation and fertility

Fig. 2 Schema of the female reproductive axis. (Reproduced from Chapter 23 of Bloomfield J, Flicker PA, Fitch KD, eds. Textbook of Science and Medicine in Sport. Oxford: BlackweU, 1992).

become ineffective in stimulating ovulation and the anovulatory cycle becomes prolonged. Menstruation may occur episodically as shedding of the inadequately progesterone-primed (secretory) endometrium or as a response to infrequent ovulation. Eventually menses may cease altogether. Altered hypothalamic/pituitary function is not unique to female athletes, as low LH pulses and testosterone levels have been recorded in male marathon runners.21 FSH, LH, E2 and progesterone are typically reduced in the amenorrhoeic athlete, though oestrogen levels rarely descend to those of postmenopausal women. Indeed, hormone profiles most commonly reflect those of the early follicular phase. While preliminary studies in older women suggest that a blood oestradiol (E2) level greater than 220 pmol/1 (60 pg/ml) is needed to maintain bone density, comparable data have not been obtained in athletes.22 Aetiology of AA The exact aetiology of AA remains unknown, however several theories have been postulated (Fig. 3).

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\

\ Stress /

Dietary Inadequacy

\ Hypothalamlc/pltultary dysfunction

Ovarian dysfunction

Inadequate luteal phase•«-»• Anovulation •«-*- Oltgomenorrhoea —-— Amtnorrhoea

Fig. 3 Influences affecting the continuum of menstrual changes in athletes. (Reproduced from Chapter 23 of Bloomfield J, Flicker PA, Fitch KD, eds. Textbook of Science and Medicine in Sport. Oxford: Blackwell, 1992).

a. Extraglandular oestrogen production

The 'fat theory' of Frisch and McArthur23 was based on a presumption of reduced conversion of oestrogen (oestrone, El) from circulating androgens in the smaller peripheral fat stores of athletes. However, El is not consistently low in AA and aromatization of androgens to oestrone also occurs in muscle. b. Acute phase hormonal changes During acute exercise insulin levels decrease, while glucagon, growth hormone, the catecholamines, prolactin, the sex steroids, dopamine and B-endorphins increase. Chronic hyperprolactinaemia as seen in pituitary tumour is a well described cause of amenorrhoea, and it has been postulated that recurrent exercise may mimic this effect.24 Increased B-endorphin and dopamine, which are secreted in very close anatomic proximity to GnRH secreting cells in the hypothalamus, may inhibit GnRH release. This is consistent with the infusion of naloxone, an opiate antagonist, significantly increasing LH and FSH pulse amplitude in amenorrhoeic runners.25 Brown26 suggests that repetitive rises in E2 levels following exercise may diminish pituitary gonadotrophin levels through feedback mechanisms to GnRH. This effect would be increased

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during the luteal phase of the cycle when the measured increase in E2 after exercise is greater, and subsequent disruption of the FSH/LH ratio results in an abnormal luteal phase and/or anovulation and amenorrhoea. The suppression of the reproductive axis in regular exercisers would lead to the observed decline in resting and exercising ovarian hormonal levels. Associated factors of AA While the direct pathogenesis of AA remains unknown there are several well identified factors associated with its occurrence in exercising women. These factors are related to both delayed menarche and secondary amenorrhoea (Table 1). Frisch et al.27 proposed that in premenarche trained swimmers and runners, menarche was delayed 5 months for each year of training. However, it is also likely that self-selection exists whereby thin, long limbed eunuchoid girls naturally experience a late menarche. Studies of sisters of athletes confirm a familial late menarche, although the athletes menstruated later than their siblings.28 /. Youth Erdelyi29 was the first to notice that younger athletes have a higher incidence of menstrual irregularity compared with older runners. 2. Prior menstrual irregularity

The majority of studies indicate that oligo/amenorrhoeic athletes are more likely to have experienced irregular menses prior to training compared with eumenorrhoeic athletes.30 However, Table 1 Factors associated with menstrual change in athletes Factors associated with menstrual regularity

Factors associated with menstrual irregularity

Maturity of reproductive axis Established ovulatory cycles Advanced gynaecological age Parity Increased bodyweight Increased body fat Gradual increase in activity Low intensity exercise

Youth Nullipariry Decreased bodyweight Decreased body fat Low energy diet High volume, high intensity exercise Rapid increase in exercise workload Psychological stress

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Bullen et al.31 recorded the onset of some form of menstrual disturbance with training in nearly all of the subjects studied, irrespective of previous menstrual history. 3. Nulliparity Women who have borne children are less likely to experience AA.32 The above three factors indicate that a mature hypothalamicpituitary-ovarian axis, commensurate with the establishment of regular menstruation, resists the onset of AA. Evidently once patterned hormonal responses are in effect they are less likely to be disrupted by external factors. 4. Sport AA is more common in runners, gymnasts, dancers and lightweight rowers and is less common in swimmers, cyclists and court sport players. 5. Weight Loss Menstrual change in athletes has been associated with low bodyweight, excessive weight loss with training, diminished per cent body fat and dietary inadequacies. Some studies, however, indicate comparable height, weight, and weight loss in AA as well as eumenorrhoeic athletes.33 The 'critical fat theory' 23 suggested that 17% body fat was necessary for menarche and 22% body fat was needed to resume menses after amenorrhoea. This dogmatic theory has not been substantiated by subsequent research; however, it is evident that there is a threshold body fat or total body mass (weight) below which menses are affected, but this threshold is different for different individuals, and may be affected by other factors such as activity and stress levels.

6. Exercise levels An association between an increased training distance in runners and the incidence of menstrual disturbance has been shown in

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many studies, including an almost linear relationship with AA when the training distance rose above 30 km per week.3* Furthermore, athletes, including dancers, are known to resume menses during a training lay-off during holidays or after injury, when there is no change in bodyweight.35 A number of studies however, show no correlation between the level of exercise and menstruation and it may be that intensity (per cent of maximal exercise sustained in training or a rapid increase in training) rather than total distance or hours, may be more important determinants of AA. 7. Stress While it is difficult to evaluate the role of stress, the observation that athletes have a higher incidence of amenorrhoea while participating in strenuous sports raises the possibility of a stress-related phenomenon. Women are known to experience menstrual irregularity at times of emotional stress such as bereavement or home shift. Chronic physical or emotional stress may produce a state of either amenorrhoea or anovulation but amenorrhoeic runners as a group are similar to menstrually regular runners in levels of depression, hypochondriasis, anxiety and obsessive/compulsive tendencies.30 Menstrual change in athletes constitutes a continuum along which an athlete can shift depending on her level of activity, bodyweight, life stresses and diet. The range changes from normal ovulatory cycles, to delayed menarche, luteal phase deficiency, oligomenorrhoea and established amenorrhoea. This 'dynamic dimension' of AA as described by Prior & colleagues,36 makes exact definitions and estimates of incidence difficult to determine. Furthermore the literature is complicated by inaccurate descriptions of athletic populations and factors such as body fat estimation.37 Menstrual blood flow is an inaccurate measure of menstrual status and estimates of menstrual irregularity by survey are likely to be conservative.38 AAANDBMD It is now established that amenorrhoeic athletes are likely to develop osteopenia—decreased BMD—in response to their hypooestrogenaemia. It is likely that women with anovulatory cycles,

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and hence decreased progesterone levels are also prone to bone loss.19 Amenorrhoeic athletes also commonly manifest one or more further risk factors for osteopenia itself; they are often white and have low total energy intake, low calcium intake, low body weight and are nulliparous or have not used the oral contraceptive. Cann and co-workers39 first described decreased spinal but normal wrist BMD in amenorrhoeic athletes. This work has been confirmed by many other researchers.4041 It is noteworthy that skeletal sites predominated by trabecular bone rather than cortical bone have consistently been shown to suffer the effects of hormonal insufficiency. While some research indicates that bone mass increases once menstruation and normal hormonal profiles return,42 it appears that the short-fall of spinal bone mass may never be fully recovered after long term amenorrhoea.43 It is not accurate however, to define these athletes as 'osteoporotic' in terms of the disease entity. Osteoporotic fractures have not been reported in athletes, even those with decreased BMD, and this may reflect improved quality of trabecular bone in young compared with older women with similar BMD. However, vertebral crush fractures have been reported in anorexics who don't exercise and suffer greater extremes of bone loss.44 Studies from the armed forces indicate that female recruits suffer significantly more stress fractures than males45 but statistics from athletic populations are inconclusive. Reports of an increased incidence of stress fractures in AA athletes 41 ' 4647 led to the assumption that this is as a direct result of decreased BMD in these athletes. It is also possible that athletes who run further or train harder (and subsequently become amenorrhoeic) are therefore prone to injury. Stress fractures also occur in both male athletes and eumenorrhoeic women, and are usually ascribed to training errors and biomechanical faults.48 Moreover stress fractures occur predominantly in weightbearing cortical bone and not at sites commonly affected by postmenopausal osteoporosis. Recent research has demonstrated that femoral neck and tdbial bone density is in fact preserved in amenorrhoeic athletes, which is consistent with the known site-specific effect of physical activity. When adjusted for differences in body weight, femoral shaft but not vertebral BMD were equivalent for menstruating and nonmenstruating athletes.49 Lower limb bone density (measured by whole body DEXA scanning) of amenorrhoeic dancers has been shown to be greater than that of weight-matched anorexics but

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similar to a heavier sedentary control group. However spinal bone density was diminished in both the dancers and anorexics compared with the control group.50 Furthermore, amenorrhoeic lightweight rowers, who had significantly stronger spinal muscles (iliopsoas) had normal spinal trabecular BMD in contrast to amenorrhoeic dancers and runners.51 The authors, own research has specifically looked at the bone density in spine, wrist and hip of athletes with stress fractures. No differences were demonstrated between the BMD of stress fractured athletes compared with non-injured control athletes, despite the injured group having lower skin-fold measurements and a later age of menarche." Similar findings have been confirmed in two further reports. 5354 Recent work on military recruits identified a positive correlation between stress fracture incidence and both narrower tdbial bone width and increased external rotation of the hip but no correlation with tibia] BMD. 55 However another study of older athletes which included men and oral contraceptive users showed lower bone density in the spine and hip of stress fractured athletes.56 Further research into the BMD of those sites most commonly stress fractured may well indicate whether an aetiological relationship exists. It is possible that measurements of BMD are too crude to indicate whether an individual is prone to stress fractures and accurate measurement of bone turnover, as yet not fully identified, may be more likely to yield a meaningful answer. It is important to emphasize that athletes with normal menses are likely to have normal if not increased bone density. Only one study has reported decreased bone density in eumenorrhoeic athletes but comparisons were made with a sedentary control group who weighed on average 20 kg more.57 Nor does AA per se necessarily equate with osteopenia as some athletes maintain normal spinal BMD despite prolongued AA.41 Osteoporosis in the elderly is already at epidemic proportions in the Western world. The obvious concern exists in amenorrhoeic athletes for the premature onset of osteoporosis, as the age related decline from a lower peak BMD would pre-empt an early drop below the fracture threshold. However it is not yet established what pattern an amenorrhoeic athlete's BMD follows throughout life. It may be possible that peak BMD is achieved later in some of these athletes, or that the rapid decline of BMD at menopause may not be evident in a woman already chronically endocrine suppressed. Current evidence however indicates that those who

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develop menstrual disturbance, whether it be due to weight loss, high exercise levels or other contributing factors need to be counselled on the prognosis of low bone mass and must seek the return of normal menses. REFERENCES 1 Martin AD, McCulloch RG. Bone dynamics: Stress, strain and fracture. J Sports Sci 1987; 5: 155-163 2 Nilsson BEC, Westlin NE. Bone density in athletes. Clin Orthop 1971; 77: 179-182 3 Block JE, Genant HK, Black D. Greater vertebral bone mineral mass in exercising young men. West J Med 1986; 145: 39-42 4 Margulics JY, Simkin A, Leichter I et al. Effect of intense physical activity on the bone mineral content in the lower limbs of young adults. J Bone Joint Surg [Am] 1986; 68A: 1090-1093 5 Pocock NA, Eisman JA, Ycates MG, Sambrook PN, Eberl S. Physical fitness is a major determinant of femoral neck and lumbar spine bone mineral density. J Clin Invest 1986; 78: 618-621 6 Dalsky GP, Stocke KS, Ehsani AA, Slatopolsky E, Lee WC, Birge SJ. Weightbearing exercise training and lumbar bone in postmenopausal women. Ann Intern Med 1988; 108: 824-828 7 Bailey DA, McCulloch RG. Bone tissue and physical activity. Can J Sports Sci 1990; 15: 4 229-239 8 Jones HH, Priest JD, Hayes WC, Tichenor CC, Nagel DA. Humeral hypertrophy in response to exercise. J Bone Joint Surg [Am] 1977; 59A: 204-208 9 Williams JA, Wagner J, Wasnich R, Heilbrum L. The effect of long-distance running upon appendicular bone mineral content. Med Sci Sports Exerc 1984; 16: 223-7 10 Mazess RB, Whedon GD. Immobilization and bone. Calcif Tiss Int 1983; 35: 605-612 11 Leblanc A, Schneider V, Krebs J, Evans H, Jhingran S, Johnson P. Spinal bone mineral after 5 weeks of bed rest. Calcif Tiss Int 1987; 41: 259-261 12 Uhthoff HK, Jaworski ZFG. Bone loss in response to long-term immobilisation. J Bone Joint Sur 1978; 60B: 420-429 13 Tilton FE, Degianni JJC, Schneider VD. Longterm follow-up of Skylab bone demineralisation. Aviat Space Environ Med 1980; 51: 1209-1213 14 Wolff JD. Das Geretz der Transformation der Knochen. Berlin: Hirchwald, 1892 15 Roub LW, Gumerman LW, Hanley EN, Williams Clark M, Goodman M, Herbert DL. Bone stress: a radionuclide imaging perspective. Radiology 1979; 132: 431-438 16 Grimston SK, Sanborn CF, Huffer WE, Miller PD (1989) Bone biopsy analysis detects metabolic bone disease in female runners. Med Sci Sports Exerc 1989; 21 (Supp2): S114Abs 17 Evans RA. Calcium and osteoporosis. Med J Aust 1990; 152: 431-433 18 National Institutes of Health Consensus Development Conference on Osteoporosis. J Am Med Assoc 1984; 252: 799-802 19 Prior JC. Progesterone as a bone-trophic hormone. Endocr Rev 1990; 11: 386-398 20 Snow GR, Anderson C. The effects of continuous progestagen treatment on cortical bone remodelling activity in beagles. Calcif Tissue Int 1985; 37: 282-286

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Exercise, amenorrhoea and the skeleton.

One of the accepted benefits of regular exercise is the development of increased bone mineral density (BMD) and hence a skeleton more capable of withs...
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