Osteoporosis and/or osteopenia in athletes is associated with: the age of onset of training; duration; intensity; volume of training; the sport concerned (e.g. light weight rowers, synchronised swimmers, ballet dancers, gymnastics, marathon runners); diet; stress (psychological as well as physical stress); not excluding additional risk factors such as genetics; medications; other diseases which cause bone loss. The loss is mainly of trabecular bone which is found in the vertebrae (bones in your back) and the neck of the femur in your hip.
Exercise plays a very important role both in the formation of bone and the maintenance of bone throughout the life cycle. Bones require normal levels of sex hormones, adequate calories particularly protein. Bones also require the daily recommended amounts of calcium, Vitamin D and regular weight bearing exercise.
Exercise affects the skeleton in different ways. The direct effect of stress loading can be to increase bone mineral density. However, Intensive aerobic exercise can adversely affect bone density indirectly by its effect on the hypothalamic-pituitary-gonadal axis, which results in low oestrogen levels in females (Wolman 1994;O Brien 2007). Over trained male athletes may also show low levels of testosterone and may develop stress fractures and osteoporosis (Gillooly 2002, Rigby 2003).
Wolff’s Law states that changes in bone function lead to changes in bone. Bone is laid down where it is needed. Bone is resorbed where it is not needed (Wolff 1892). Osteogenesis is induced by dynamic not static strains. The optimal type of osteogenic activity should provide relatively high levels of strain. (Rubin and Lanyon1984). Tensile Forces result in osteoclastic activity on the convex side of an angulated bone. Compressive force results in osteoblastic activity on the concave side.
Muscle action is the main stimulus for bone formation, the mechanical force and weight bearing. (O Brien 2001). Greater loads and fewer repetition of a load will result in greater gains in bone mass. Lower loads repeated a greater number of times result in lower gains (Kerr et al., 1994) Weight bearing activity accounted for up to 17% of the variance in B.M.D. between individuals in their late twenties (Welten et al. 1994).
Peak Height Velocity for girls occurs usually between 10.5 – 13 Years and is earlier than 12.5 – 15 years for boys. Around this period, bone is most responsive to exercise and during the time of Peak Weight Velocity and Menarche, which occur approximately 6 months and 1 year after height peak (Sanborn et al 1994). Average age in Ireland is 12-13 years – A late menarche is after 16 years.
Bone mass is affected by peak bone mass and the degree of subsequent bone loss. 60-80% of Peak bone mass is due to genetics (Khan et al 2001). Other factors include: hormones; nutrition; environmental factors; mechanical strain. Growing bone has a greater capacity to add new bone to skeleton than mature bone, 7-8% gain of bone mass per year is gained during childhood and early adolescence. (Matkovic et al 2000).
Many factors including hormones, diet, exercise, medication, and their chronological age, which can be affected by their skeletal or bone age and the stage of sexual maturation, can affect Low peak bone mass. (McKay et al. 1998). Woods (1999) in a study of apprentice jockeys found that the majority had a bone age 18-24 months below their chronological age. Apprentice jockeys had significantly lower BMD than flat and jump jockeys. The jockeys had lower BMD in their spine and neck of femur, than rugby players and sedentary controls (Woods 1999).
Daily weight bearing exercise has a positive effect on BMD, while immobilisation and space flight have a negative effect (Kanis 1994). The effects of exercise are not homogenous; they reflect the strains imposed at individual sites. Osteogenic response to mechanical loading is site specific. Professional tennis players have 30% greater bone density in their dominant forearm (Krahl et al. 1994). Weight bearing exercises such as running on the spot, jumping, skipping, dancing and walking, are gravity stimulated and are more effective than non-weight bearing exercise such as swimming and equestrian.
Weight bearing activity during adolescence and early adulthood was a far more important predictor of peak bone mass than calcium intake. (Welten et al. 1994). Young women participating regularly in sports at school demonstrated higher bone mass than those who did not (Heinonen 2001).
Highest bone mineral content and bone mineral density are found in strength and power- trained athletes. (Suominen 1993). World class and recreational weight lifters had 10-35% greater lumbar spine B.M.D. Athletes with habitually high levels of physical activity show increased B.M.D. value when compared with controls that undertake moderate physical activity. Road cyclists have lower bone mineral density in their lumbar spine compared to mountain bikers. (Gillooly 2002, Rigby 2003).
Premenopausal women who participate regularly in high impact exercise tend to have higher B.M.D. than sedentary controls. But intensive endurance training and amenorrhea may be associated with decreased trabecular bone density in young females (Suominen 1993). Menstrual irregularities occurred in elite university athletes, swimmers who had lower B.M.D. in their spine and hip than gymnasts. Untreated amenorrhea is associated with long -term morbidity especially in young women (Drinkwater et al 1990).
“Overtraining” due to excessive physical or psychological stress, particularly if it is associated with inadequate caloric intake, results in low levels of sex hormones, in both male and female athletes and an increased risk of osteopenia and/or osteoporosis. There is a higher incidence of gonadal insufficiency particularly in sports where there are weight categories, such as light weight rowing, judo, diving, gymnasts, synchronised swimming, skating and ballet dancers and long-distance running, but it can occur in any sport. Non-weight bearing sports particularly swimmers and road cyclist’s bones in their lumbar spine (Low back) are more prone to having low bone mineral density, either osteopenia or osteoporosis. (Taafe et al. 1995).
Osteoporosis is a systemic skeletal disorder characterized by low bone mass and micro-architectural deterioration of bone tissue, with a consequence increase in bone fragility. Osteoporosis is associated with a reduction in bone mineral density and an increased risk of fractures.
Bone is a dynamic tissue in which the process of resorption, (mediated by the osteoclasts), is coupled with the processes of formation, (mediated by the osteoblasts) when they are in a state of balance. Osteoporosis results when uncoupling occurs and there is an imbalance between resorption and formation. The bone most frequently affected is the trabecular bone in the distal end of the radius, vertebral bodies and the neck of the femur. The commonest cause of osteoporosis in women and men is hypogonadism, which are due to low levels of oestrogen in females and testosterone in males.
Hormones secreted by the hypothalamus, anterior pituitary, and ovary and to a lesser extent the adrenal gland, regulate the menstrual cycle. Acting on the uterus and ovaries, they are dependent on a feedback mechanism. This is necessary for the normal development of the follicle. The Gonadotrophin Releasing Hormone (GnRH) causes the synthesis, storage, activation and release of Follicle Stimulating Hormone (FSH) and Lutenizing Hormone (LH). The timing and intensity of the GnRH determines the amount of FSH and LH released, and their ratio relative to each other. (Prior 86). Physical exercise produces marked changes in the post exercise pulsatile nature of LH, FSH and Oestrodial. (Keizer 1983).
During strenuous exercise there is an increased concentration of dopamine, beta-endorphins and Catechol-oestrogens. Dopamine has an inhibitory effect on the release of GnRH. Beta-endorphins act in two ways; they appear to stimulate dopamine, and this is their main action on GnRH (Yen, 1982), but they also combine with the nor-adrenaline receptors in the hypothalamus and prevent the stimulatory effects of nor-epinephrine on GnRH. The normal pulsatile release of gonadatrophin releasing hormone is altered, resulting in changes in the secretion of FSH and LH and the ovarian hormones.
Corticotrophin – releasing hormone may also act indirectly by endorphins. The level of Cortisol is increased by intense exercise and in athletes who are over trained. Cortisol levels are increased in amenorrheic athletes, compared to sedentary women and cyclic athletes. Long term elevated levels of Cortisol affect calcium and bone metabolism resulting in osteopenia and osteoporosis. Cortisol increases bone resorption and decreases bone formation. Cortisol also decreases intestinal absorption of calcium. Hypothyroidism may also be a complication of over trained athletes who may also be amenorrheic. Amenorrhoeic athletes who are hypo-oestrogenic have reduced bone mass. This may be due to late menarche, irregular menstruation, or may be part of the Athletic Triad, which consists of amenorrhea, an eating disorder and osteoporosis and/or osteopenia. (Khan et al 2001).
Menstrual irregularities result in alterations in the normal levels of sex hormones and predispose to osteopenia and in some cases osteoporosis. Menstrual irregularities tend to occur in the athletes with the most intense training schedules, who had trained for the longest period of time. Vegetarians and people with a low caloric intake had the highest incidence of oligomenorrhea and amenorrhea. Menstrual irregularities are not consistent across sports; 7% recreational runners, 12% swimmers and 25% distance runners. Many so-called normal cycles are abnormal, when serum hormone levels are done after the 21st day of cycle.
There are multifactorial causes; Stress, both psychological and physical stress. This may be due to an increase in the amount and intensity of training and in the number of competitions, with inadequate rest periods.
Other factors which predispose to menstrual irregularities include a late menarche (>16 years), irregular cycles prior to sports participation, intense training prior to menarche, immature pituitary axis. Tall thin girls and those with a poor maternal menstrual history, have a later menarche than small overweight girls. Average age for menarche in USA for Caucasians is 12.8 years, for European’s it is 12-13.4 years.
Progression of menstrual changes to abnormal is from,
- Normal follicular phase and a normal luteal phase.
- A prolonged follicular phase and a shortened luteal phase, this can only be diagnosed by taking bloods to measure progesterone levels after the 21st day of the cycle. Luteal phase defects are associated with low progesterone levels, premenstrual tension and infertility.
- Further progression results in euoestrogenic anovulatory oligomenorhea, if this phase persists there is a risk of endometrial hyperplasia.
- Hypo oestrogenic amenorrhea results in osteoporosis and genital atrophy due to low levels of oestrogen. (O’Brien 2007, Shangold 1988).
Diet also plays an important role. Decreased caloric intake and a high fibre diet are associated with a raised level of Serum Sex Hormone Binding Globulin and lowered levels of biological active oestrogens.
There is a higher incidence of amenorrhea in athletes who have a low caloric intake or who are vegetarians. The increased fibre is thought to bind with calcium and reduce calcium absorption. Excess fibre may also lead to decreased bone density by the binding of steroids to fibre or indirectly by decreasing enterohepatic circulation of oestrogens, either of which would have a negative effect on bone remodelling.
Increases in dietary fat consumption are associated with increased levels of circulating oestrogens. Amenorrheic athletes have an increased risk of musculosketal injuries and may have a low calcium and vitamin D intake. The recommended daily calcium for an adolescent is 1500mg and 800 international units of vitamin D.
Drinkwater et al (1990) reported vertebral BMD to be significantly lower in athletes with a long history of menstrual irregularity. There is a higher incidence of stress fractures in amenorrheic athletes particularly those with a late menarche. (Warren et al. 1991). The mean bone mineral density is comparable in some cases to a 60-year-old woman. If untreated they have a high risk of developing stress fractures now and osteoporotic fractures now and also at the menopause. Moderate exercise protects but excessive exercise may cause osteoporosis.
“The Athletic Triad” (Yeager et al 1993) is the name of the syndrome, which occurs, in female athletes, when amenorrhoea, an eating disorder and osteoporosis occur together. Bennell 2004: Khan et al. 2004 have found that they may have osteopenia rather than osteoporosis. They may each occur on their own, or in combination.
The female athlete is most at risk to develop the athletic triad during adolescence and young adulthood. This may be due to psychological, biological and social pressures at this time. During the prepubertal spurt 60% of the final bone mass is laid down. Anorexia and bulimia are now more frequently recognised, both in the general population and among athletes (Grinspoon et al., 1999; Sundgot-Borgen, 1993; Sundgot-Borgen, 2000; Miller et al., 2005).
Individuals with eating disorders strive for perfection; have a marked preoccupation with food, a distorted body image and fear of gaining weight or becoming fat, despite being at least 15% below their ideal body mass. Amenorrhea is one of the cardinal features of anorexia and is associated with hypothalamic dysfunction with low levels of oestrogen (Lindsay 1995; Compston et al., 2006); in addition, anorexics may also have high levels of the stress hormone Cortisol (Katz, 1988). BMD is also significantly lower in females who have developed anorexia during their growth period than in those who have developed anorexia at an older age (Biller et al., 1989).
Athletes, parents and coaches, who have unrealistic goals and poorly designed training programmes with inadequate recovery periods are placing the athlete at a much higher risk of developing an eating disorder. Talented athletes participating in more than one sport and who are training and playing for school club and county, “Win at all costs, ambitious coaches, and pushy parents with unrealistic goals, wrong training plan, emphasis on weight,” are detrimental to talented athletes.
Osteoporosis in young female athletes is sports specific; there is a much greater incidence in appearance sports, such as diving, figure skating, gymnastics, synchronised swimming and ballet. Endurance sports, which involve distance running, particularly in marathon runners. Weight category sports: jockeys, judo and light weight rowers. It is associated with age of onset of training, duration of participation in training, intensity and volume of training, the sport concerned, diet and stress (Riggs, 1981).
Stress, both psychological and physical, play a role in menstrual irregularity, which may progress to oligomenorrhea or amenorrhea. Physical stress may be due to a sudden increase in the intensity and duration of training or too many competitions. A sudden marked increase in the intensity and the amount of aerobic exercise may cause problems particularly in the younger nulliparous female with an immature hypothalamic – pituitary axis.
Nattiv et al. (1994) state that eating disorders such as anorexia and bulimia affect as many as one third of athletic females. Disordered eating has become a major concern in female and in some male athletes. Some researchers have estimated the prevalence to be as high as 50% in certain sports. Female athletes who had a late menarche (after 16 years) or who have irregular cycles, particularly if they have had long periods of oligomenorrhea or amenorrhea, e.g. athletes with eating disorders and hypogonadism due to any cause, are more at risk to develop osteopenia or osteoporosis, particularly if they are ” over trained”. Long-term Corticosteroid users, patients with malabsorption, hypothyroidism, and hyperparathyroidism, high levels of prolactin, Cortisol, Parathyroid hormone, hyperthyroidism or low levels of vitamin D are also at risk.
If a female athlete has been amenorrhoea for four months and is not pregnant, hormonal studies should be carried out and her bone mineral density should be assessed using a Dual Energy X-ray Absorptiometer (DXA). DXA is non-invasive and is currently the most precise and widely used method of assessing Bone Mineral Density. Measurement of the spine and hips should be carried out and bone markers, if they are available. If osteoporosis is diagnosed in either a male or female she/he should be treated. Medical causes must be excluded.
The treatment for amenorrhoeic athletes:
- Reduce the amount and intensity of the exercise and competition.
- Reduce psychological stress if possible.
- Prescribe combination low dose pill or HRT.
- Increase the calcium, Vitamin D, protein is usually necessary.
- Increase the total calorific content, if it is below the required level for the activity performed.
They should be advised to decrease their exercise intensity and a 2-3% increase in weight should be encouraged. Recreational athletes will reduce the intensity of their exercise; elite athletes are unlikely to take this advice. If the female athlete will not reduce the amount of training and competition, she should be advised to go on hormone replacement therapy or the low dose contraceptive pill. Some athletes do not want to go on any medication, as they think it will affect their weight, but they must consider that if they get a stress fracture they will be unable to compete or train.
All athletes should keep a training diary, which should include details of their diet, exercise regime and menstrual cycle. Excessive carbohydrate loading may result in some athletes developing diarrhoea, due to intolerance to gluten. This will affect absorption of Calcium, vitamin D iron and protein.
“Over trained athletes” should have the following measured: Sex hormones, oestrogen, progesterone, serum sex hormone binding globulin (SHBG), and free testosterone, androstenedione in males, cortisol, gonadotrophins (LH,FSH ) and prolactin, thyroid, hepatic, and renal and intestinal function.
Female athletes who had a late menarche, or irregular cycles, particularly if they have had long periods of oligomenorrhea or amenorrhea are more vulnerable and should have a DXA and hormone levels done, in the second half of the cycle if they are having periods.
Maximum bone loss probably occurs in the early phase of amenorrhoea, so they should start treatment early. A large number of amenorrhea athletes develop breast tenderness and bloating, when they start hormone therapy and they should be warned about this and reassured that the symptoms are usually transitory. Adolescent athletes are at high risk of developing eating disorders.
All athletes should be given nutritional advice from a nutritionist interested in sport and eating disorders and if appropriate consult a psychiatrist with a special interest in eating disorders. Ensure they have an adequate caloric intake and increase the calcium and vitamin D intake.
Medical Team Approach: Physician, Physiotherapist, Nutritionist, Physiologist, Psychologist, (Psychiatrist), working with athlete and coach. The successful treatment and prevention of Osteoporosis is to identify those at risk at an early stage and assess their hormone levels and bone mineral density.
- Biller B, Saxe V, Herzog D, et al. Mechanisms of osteoporosis in adults and adolescent women with anorexia nervosa. J Clin Endocrinol Metab 1989; 68: 548-554.
- Bennell K, The female Athlete in Clinical Sports Medicine, Editors Brukner P., Khan K. 2nd Edition McGraw- Hill2004; 674-699.
- Compston J, McConachie C, Stott C, Hannon R, Kaptoge S, Debiram I, Love S, Jaffa, A. Changes in bone mineral density, body composition and biochemical markers of bone turnover during weight gain in adolescent with severe anorexia nervosa: A 1 Year prospective study. Osteoporosis International; 2006. 17: 77-78.
- Drinkwater BL., Bruemmer B., and Chestnut III CH: Menstrual history as a determinant of current bone mineral density in young athletes. JAMA; 1990; 263:545
- Gillooly JJ The relationship between cycle training, hormone levels, mood state, bone mineral density and fracture incidence in male road cyclists MSC Thesis in Sports Medicine, Trinity College Dublin, 2002; 66-67.
- Grinspoon S, Miller K, Coyle C, et al. Severity of osteopenia in oestrogen deficient women with anorexia nervosa and hypothalamic amenorrhea. J Clin Endocrinol Metab 1999; 84: 2049-2055.
- Heinonen A Physical activity, targeted bone loading and bone mineral density in premenopausal women in. In: Physical activity and bone health. Human Kinetics.2001; 129-142
- Kanis J.A in: Osteoporosis. Blackwell Science, London. 1994:22-55.
- Katz, J.L. Eating disorders in: Women in exercise, edited by Shangold, M. and Mirkin G. Philadelphia, Davis; 1988; 248-263.
- Keizer H.A. Hormonal responses in women as a function of physical exercise and training. Uitgeverij de Vrieseborch, Harlem. 1983
- Kerr D.A., Prince R.L., Morton A., Dick I., Does high resistance weight training have a greater effect on bone mass than low resistance weight training? (Abstract 128) Journal Bone Mineral Research (Supplement 1) 1994;S152
- Khan K, McKay H, Kannus P, Bailey D, Wark J, Bennell K. In: Physical Activity and bone health. Human Kinetics. 2001; 111-114.
- Klibanski A, Biller BMK, Rosenthal DI, Schoenfeld D A, Saxe V. Effects of prolactin and oestrogen deficiency in amenorrhoeic bone loss. . Journal of Clinical Endocrinology and Metabolism; 1998. ; 67: 124-130.
- Kral H, Michaelis U., Peiper H.G., Quack G., Montag M., Stimulation of bone growth through sports; American Journal Sports medicine 1994; 22:751-7
- Lindsay R. Oestrogen deficiency. In: Osteoporosis: Etiology, Diagnosis and Management, 2nd edition, edited by Riggs, B.L. and Melton L.J.Lippincott Raven, Philadelphia, 1995.133-160.
- Lutter J.M., Prevalence of menstrual Change in Athletes and Active Women. In: The menstrual Cycle and Physical Activity, edited by Puhl, J.L., and Brown, C.H. Human Kinetics, 1986; 29-44.
- Matkovic V. Badenhop N.E., Landoll J.E., Mobley S.L., Calcium, hormones and bone health. Osteoporosis Int. Suppl. 2000; 4,1-11
- McKay HA, Bailey DA Mirwald RL et al peak bone mineral accrual and age of menarche in adolescent girls: A6year longitudinal study J Pediatrics 1998; 133; 682-687).
- Miller K, Grinspoon, S, Ciampa J, Hier J, Herzog D, Klibanski A. Medical findings in outpatients with anorexia nervosa. Archives of Internal Medicine; 2005. ; 165: 561 -566.
- Nattiv A., Agostini R., Drinkwater B., Yeager K K., The Female triad; The Athletic Woman. Clinics In Sports Medicine, 1994 Vol 13; 2 April. 405-418
- O’Brien M ” Exercise and Osteoporosis” 7th Samuel Haughton lecture, Irish Journal of Medical Science 2001 (Volume 170, Number 1): 58-62; 27.
- O’Brien M Women, Oxford Handbook of Sports and Exercise Medicine Ed Domhnall Macauley; Oxford University press 2007: 749-772.
- Prior JC. Hormonal mechanisms of reproductive function and Hypothalamic adaptation to endurance training; The Menstrual Cycle And Physical Activity. Human Kinetics. 1984 63-80:
- Rigby O. M., fractures, hormones and bone mineral density in competitive male mountain bikers and road cyclists, MSc Thesis Sports Medicine, Trinity College Dublin, 2002; 60,69.
- Riggs, B.L., Wahner H.W., Dunn W.L., et al. Differential changes in bone mineral density of the appendicular and axial skeleton with ageing .J. Clin. Investigations 1981:67:328-335.
- Rubin C.T. and Lanyon L.E. Regulation of bone formation by applied dynamic loads Journal Bone Joint Surgery 1984; 66:397-402
- Sanborn C.F., Martin B.J., Wagner W.W Is athletic amenorrhea specific to runners? IS J Obstet Gynaecology 1982; 142: 589
- Shangold M. Menstrual disorders in: Women in exercise, edited by Shangold, M. and Mirkin G.) Philadelphia, Davis; 1988: 248-263.
- Suominen H., Bone mineral density and long term exercise. An overview of cross-sectional athlete studies Sports Medicine 1993; 16:316-30
- Sundgot-Borgen, J. Prevalence of eating disorders in elite female athletes.
- International Journal of Sports Nutrition; 1993. ; 3: 29-40. Sundgot-Borgen, J. Eating Disorders. In: Women in Sport (Ed. Drinkwater, B.L.) Oxford, Blackwell Science. 2000; 364-377.
- Taafe D.R., Snow-Harter C., Connolly D.A., Robinson T.L., Marcus R., Differential effects of swimming versus weight bearing activity on bone mineral density: Status of eumenorrhoeic athletes.
- Journal Bone Mineral Research .1995;10:586-93.
- Warren MP. Brooks- Gunn J., Fox RP. et al. Lack of bone accretion and amenorrhea: Evidence for a relative Osteopenia in weight bearing bones. Clin. Endocrinol Metab. 72: 847-853, 1991
- Welten D.C., Kemper H.C., Post G.B. Weight bearing activities during youth is a more important factor for peak bone mass than calcium, Journal Bone Mineral Research 1994; 9:1089-96
- Wolff J., Das Gesetz der transformation der Knocher: Berlin Hirschwold 1892
- Wolman R. L. Osteoporosis and exercise BMJ 1994; 309:400-3
- Woods C. MSc in Sports Medicine Thesis Bone mineral of male jockeys, rugby players and sedentary controls, 1999. Trinity College Dublin
- Yeager K.K., Agostini R., Nattiv A., Drinkwater B., The female athlete triad; Disordered eating, amenorrhea osteoporosis Med.Sci Sports Exerc, 1993: 25:775,
- Yen S.S. Neuroendocrine regulation of gonadatrophin and prolactin secretion in women. Clin. Reproductive Neuroendrocrinology N.Y.1982; 137-174.
- Zanker C, Swaine I. The relationship between bone turnover, oestradiol and energy balance in women distance runners. British Journal of Sports Medicine; 1998. 32: 167-171.
Professor Moira O’Brien FFSEM