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Exercise and the Menstrual Cycle

SSC4 Essay
Exercise in Medical Conditions
0507107

Andrew Haslett

THE HYPOTHALAMIC-PITUITARY-OVARIAN AXIS

The menstrual cycle requires precise coordination between several processes in the
body. [1, 2] The major components of this control system include the hypothalamic
gonadotrophin-releasing hormone (GnRH) pulse generator, the pituitary
gonadotropes (cells in the anterior pituitary that produce gonadotrophins), the
ovaries, and the uterus. Together this system is known as the
hypothalamic-pituitary-ovarian (or gonadal) axis. The GnRH pulse generator is the
primary driver of the menstrual cycle and in the absence of a functional GnRH pulse
generator, the gonadotropes would remain un-stimulated and the ovaries dormant.
The gonadotropes respond to GnRH pulses by releasing the gonadotrophins
follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which stimulate
folliculogenesis and steroid hormone secretion from the ovaries. Hypothalamic and
pituitary activities are strictly controlled by ovarian hormone feedback loops, whereas
the GnRH pulse generator is modulated by a variety of inputs from other neural
centres.

After the age of 8 years [3], hypothalamic GnRH pulses increase in amplitude and
frequency, such that pituitary FSH and then LH release increases. These stimulate
increasing oestrogen release from the ovary, which is responsible for the
development of secondary sexual characteristics during puberty.

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PUBERTY AND MENARCHE

The sexual changes of females during puberty can be divided into three main stages;
thelarche, adrenarche and menarche. Thelarche is the first of the stages to occur and
describes the development of the breast tissue. It involves enlargement of the
breasts, areola and nipples along with a thickening of the duct system and is the
result of increasing oestrogen production.
Adrenarche refers to the development of the adrenal cortex. It involves both
structural and functional changes. Adrenarche is a process related to puberty but
distinct from hypothalamic-pituitary-gonadal maturation and function. As yet, an
initiator of adrenarche has not been identified. In girls, the adrenal androgens of
adrenarche produce most of the early androgenic changes of puberty: pubic hair,
body odour, skin oiliness, and acne. In most girls the early androgen effects coincide
with, or are a few months behind, the earliest estrogenic effects of gonadal puberty,
i.e. thelarche.

Menarche, the onset of menstruation, is the final phase of sexual maturity in

the female. It is the culmination of a series of physiological and anatomic processes
of puberty:

● (Potentially) The attainment of a sufficient body mass (typically 17% body

fat).[4, 5]
● Disinhibition of the GnRH pulse generator in the arcuate nucleus of the
hypothalamus
● Secretion of oestrogen by the ovaries in response to pituitary hormones.
● Over an interval of about 2 to 3 years, oestrogen stimulates growth of the
uterus (as well as height growth, breast growth, widening of the pelvis, and
increased regional adipose tissue).
● Oestrogen stimulates growth and vascularity of the endometrium, the lining of
the uterus.
● Fluctuations of hormone levels can result in changes of adequacy of blood
supply to parts of the endometrium.
● Death of some of the endometrial tissue from these hormone or blood supply
fluctuations leads to a sloughing of part of the lining with some blood flow

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from the vagina.

In most girls, menarche does not signal that ovulation has occurred. In
post-menarchal girls, about 80% of the cycles are anovulatory in the first year after
menarche, 50% in the third and 10% in the sixth year. [6]

Determinants of the Onset of Menarche

It has been observed that the average age of menarche in girls in modern societies
has declined over a number of decades, though the reasons and the degree of
decline remain subjects of debate. Although the true determinants of menarcheal age
remain to be understood, genetic factors, socioeconomic conditions, general health
and well-being, nutrition, certain types of exercise, seasonality, and family size may
all play possible roles.

One of the most popular theories today; the critical weight (fat) hypothesis, (Frisch et
al. 1974) which postulates that menarche is triggered by the attainment of a critical
percentage body fat and that the maintenance of the menstrual cycle requires the
persistence of a minimal level of body fat. If excessive leanness in females occurs
before menarche, menarche may be delayed until as late as age 19 or 20 years and,
at the other extreme, if body fat was above average, menarche may be premature. [4]
As obesity is on the increase in the developed world this would be a plausible
explanation for the trend of earlier menarche that has been observed.

In accordance with this study, there is a considerable body of evidence suggesting

that larger body size (whether that be higher weight, taller height, or higher BMI) in
childhood has been consistently associated with earlier age at menarche. However,
more recent research disagrees, to some extent, with Frisch’s hypothesis and it is
now known that height, of both the maturing child and their mother, is the greatest
determinant of age at menarche [7]. Findings also support the hypothesis that in well
nourished populations the relationship between menarche and body size is largely
regulated by genetic factors and that nutrition is less important. [8]

The critical weight (fat) hypothesis has generated a lot of interest among researchers
over the last number of decades. However, a closer examination of the evidence
reveals the hypothesis to have a number of serious methodological flaws; the study

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used estimates of body fat from height and weight, which has been shown to be
extremely inaccurate, rather than an accepted measure of body fat. There were also
numerous exceptions to the theory within the data involving fat levels above and
below the suggested threshold and, finally, where specific conditions involving
reduced fatness and menstrual delay or dysfunction were used to support the
hypothesis, it may be shown that other confounding factors were equally plausible. [9]

Subsequently, based on available evidence, the critical weight (fat) hypothesis is

becoming increasingly difficult to accept. Hypotheses based on normal maturational
processes, especially of the central nervous system, and genetic influences, currently
provide better explanations. [9]

The Normal Menstrual Cycle

Follicular Phase

Through the influence of a rise in FSH during the first days of the menstrual cycle, a
number of ovarian follicles are stimulated. [10] These follicles, which have been
present since birth[10] and have been developing for approximately a year in a
(folliculogenesis), compete with each other for dominance.

As they mature, the follicles secrete increasing amounts of oestradiol (owing to FSH
activation of aromatase production in granulosa cells), which contributes to
proliferation of the endometrium.

The rising estradiol, through a negative feedback loop, suppresses FSH levels to
concentrations that are too low to sustain maturation of the other follicles in the
cohort with the consequence that these undergo final atresia [11]. As a consequence
of this, one dominant follicle in the ovary will continue to maturity (the Graafian
follicle, which forms the ovum) while the rest cease development.

In the late follicular phase, the diameter of the graafian follicle increases
exponentially, and as a result, secretion of oestradiol increases exponentially. As the
oestradiol secretion reaches its peak it acts as the crucial signal that triggers an
ovulatory gonadotropin surge. The process by which oestradiol stimulates the
release of LH and FSH is referred to as the positive oestradiol feedback loop and
represents the crucial process that synchronizes follicle maturity and ovulation.

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Ovulatory Phase

The LH surge initiates a chain of events that results in follicular rupture and ovulation.
The large increase in LH inhibits estradiol production, and as a result estradiol
concentrations decrease dramatically from the concentrations prior to ovulation.
Granulosa cells become 'luteinized', and consequently a small pre-ovulatory rise in
progesterone occurs within one hour of the LH surge. [12]

Luteal Phase

Shortly after the ovulatory gonadotropin surge, capillaries from the theca interna
invade the granulosa layer to form an extensive capillary network that has ‘effects’ on
the steroidogenic cells of the granulosa layer forming the corpus luteum. This results
in the activation of new steroidogenic enzymes that allow the corpus luteum to
secrete both progesterone and estradiol

Progesterone dominates this phase of the menstrual cycle and causes changes in
the genital tract that prepare it for possible implantation of a fertilized ovum; there is
increased secretion by the endometrial glands and changes in the characteristics of
the cervical mucus, which becomes thick and viscous. Progesterone also inhibits the
estradiol positive feedback loop [13] and gametogenic follicle growth

The life span of the corpus luteum is around 14 days. The corpus luteum reaches
maturity 8–9 days after ovulation, after which time its ability to secrete hormones
declines. Midway through the luteal phase, levels of estradiol and progesterone begin
to decrease and menstruation follows ovulation by 13-15 days due to falling
progesterone. There is a resultant increase in the FSH:LH ratio at the end of the
cycle. The increase in the FSH:LH ratio heralds the new cycle and the recruitment of
a new cohort of follicles.

Exercise and Delayed Menarche

The effect of exercise on the onset of menarche is a highly debated area in the field
of Sports Medicine. A number of studies have demonstrated that overall
mean-menarcheal age of female athletes is higher than that of their non-athlete
controls [14] and menarche is delayed in those athletes who start physical training

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before the onset of menstruation.

However, it has also been shown that the familial resemblance in age at menarche in
athletes, their mothers and sisters, is identical with that in the general population. [15]
This would suggest that the later onset of menarche commonly observed among
female athletes is to a large extent familial.

Another suggested explanation for the trend of delayed age of menarche in athletes
is the result of pre-menarcheal girls becoming thinner due to exercise [16] and thus
that body composition is the causal factor associated with delayed menarche, this
being in keeping with Frisch’s critical weight (fat) hypothesis discussed previously .
However, the associations between body composition and intense exercise with
delayed menarche do not necessarily imply a causative relation.

A study carried out by Baxter-Jones et al. (1994) investigated the effects of intensive
training in a population of elite young British athletes who practised swimming, tennis
and gymnastics. It was discovered that menarche took place at a significantly later
age (14.3 years) in only one of the sports studied (gymnastics), suggesting that
training might have been a cause in this case. However, the amount of training
carried out by individuals did not have any effect in this or the other sports studied,
implying that elite gymnasts were selected for this attribute and that their menarche
was naturally late rather than delayed. These results seem to add further evidence to
the hypothesis that menarche is affected by biological selective factors and social
factors,[15] and that late maturation contributes to a young girl’s decision to continue
participation in gymnastics [17] rather than her participation causing the late
maturation.

It would seem there is an increasing body of evidence suggesting that athletes tend
to be late maturers rather than the intensive training delaying maturation [14, 15,16], but
perhaps it would more desirable and beneficial for exercise to delay menarche in light
of the potential health risks posed by the reducing age at menarche in the general
population. The age at menopause has remained relatively constant at approximately
50 years. As the age of menarche has fallen, the length of time during which women
are exposed to endogenous oestrogen has therefore been increasing. Longer
exposure to oestrogen is known to be associated with an increased risk of a number

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of pathologies and therefore delayed menarche may actually be desirable for several
medical and societal reasons other than its possible relation to leaner physiques.
Later menarche is not only associated with a decreased frequency of breast cancer
[18]
and of coronary heart disease [19] but also with later initiation of sexual activity, [20]
later first pregnancy, [21] and taller eventual adult height. These associations raise the
possibility of future improvements in rates of sexually transmitted disease, and
teenage pregnancy with its risk of single motherhood, disrupted education, and
financial insecurity.

Late menarche, however, may be associated with the risk of developing Alzheimer's
disease and is also known to be associated with low BMD [22] and increased fracture
risk; a number of studies have demonstrated that increasing menarcheal age
correlates with an increasing risk of postmenopausal fracture. [23, 24]

The Female Athletic Triad

The female athletic triad is a combination of three inter-related conditions that are
associated with more intense athletic training:
1. Disordered eating
2. Amenorrh0ea
3. Osteoporosis

Athletes may engage in a wide range of harmful behaviours, from food restriction to
bingeing or ‘purging’, in order to lose weight (e.g. to make weight classes) or to
maintain a thin physique which may have benefits for their performance.
Accumulating evidence suggests that a critical "energy" balance is crucial in
regulation of GnRH pulsatility, and adaptation to reduced energy intake is a
contributor to the development of amenorrhoea in some female athletes;
menstruation is not a vital process and the energy saved here can be used for more
essential processes in the body. Studies attempting to reproduce these abnormalities
in normal women found that exercise with energy deprivation affected LH pulsatility
while exercise without energy deprivation did not [25]

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Menstrual change in athletes represents a continuum along which an athlete can shift
depending on their 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. [26]

Amenorrhoea occurs in 34-66% of female athletes, compared with only 2-5% of

women in the general population.[27, 28]

Frequent causes of menstrual dysfunction are related to lifestyle variables, such as

stress, and exercise-related or diet-related causes that have effects on hypothalamic
function. The resultant condition is commonly referred to as ‘functional hypothalamic
amenorrhoea’. [29] This syndrome is characterized by a significant reduction in the
activity of the GnRH pulse generator that results in a decrease in the frequency of LH
and FSH release. As I have highlighted previously, adherence to a specific regimen
of GnRH and LH pulse frequency is crucial for normal menstrual activity, oestrogen
secretion and reproductive function, therefore abnormal LH secretion can lead to
anovulation and amenorrhoea. [30]

The degree of inhibition of the GnRH pulse generator determines whether the
menstrual cycle is disturbed only slightly or whether the patient becomes anovulatory.
Ovarian function becomes depressed with lower oestradiol secretion and an
inadequate (shorter in length with lower progesterone levels) luteal phase. Ultimately
the LH surge may become ineffective in stimulating ovulation altogether.
Menstruation may occur episodically as shedding of the inadequately
progesterone-primed (secretory) endometrium or as a response to infrequent
ovulation. [31] Eventually menses may cease altogether.

This is highlighted in a study by Bullen et al. (1985) that investigated whether

strenuous exercise spanning two menstrual cycles would induce menstrual disorders
in untrained college women. The participants were subjected to an intense training
programme (4 miles per day, progressing to 10 miles per day by week 5, and 3½
hours of moderate-intensity sports daily) and the normality of the menstrual cycles
was measured by gonadotrophin and sex-steroid excretion. As training progressed,
of the 28 participants, only 4 had a normal menstrual cycle during training and of the
others; the most frequent cause of menstrual dysfunction was the loss of the
pre-ovulatory LH surge. Within six months of termination of the study, all subjects
were again experiencing normal menstrual cycles. To ascertain the influence, if any,

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that weight loss might exert, they assigned the participants to weight-loss and
weight-maintenance groups. Results indicated significantly more women lost the ‘LH
surge’ in the weight loss group suggesting that vigorous exercise, particularly if
compounded by weight loss, can reversibly disturb reproductive function in women.

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, and hence decreased progesterone levels are also prone to
boneloss. Amenorrhoeic athletes also commonly manifest one or more further risk
factors for osteopenia itself; they often have low total energy intake, low calcium
intake, low body weight and are nulliparous. Cann et al. first described decreased
spinal but normal wrist BMD in amenorrhoeic athletes. While some research
indicates that bone mass increases once menstruation and normal hormonal profiles
return,[32] it appears that the loss of spinal bone mass may never be fully recovered
after long term amenorrhoea. [33] It is not accurate however, to define these athletes
as 'osteoporotic'. 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.

Having said all that, I feel it is important to emphasize that athletes with normal
menstruation are likely to have normal, if not increased, bone density and exercise
induced amenorrhoea does not necessarily equate with osteopaenia as some
athletes maintain normal spinal BMD despite prolonged amenorrhoea. [34]

Exercise and Peak Done Mineral Density

Females achieve maximal bone mass in the spine and femur by age 15, while bone
mass in males continues to increase between ages 15 and 18. Research carried out
in children and adolescents has confirmed a direct relationship between physical
activity and increased bone mass [35]. For example, studies in children have
consistently found higher BMD values in dominant limbs when compared to
non-dominant limbs and jumping and other weight-bearing activities have been found
to provide a significant increase in bone density at the spine and hip in prepubescent

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children. [36]

Current evidence seems to suggest that exercise provides the best long-term
benefits in BMD when it is initiated before puberty. Exercise in the post-pubertal
period seems to have only minor benefits with regards to BMD, however
weight-bearing exercise has been shown to reduce BMD loss in post menopausal
women [37] which has serious clinical implications for fracture risk and the
development of osteoporosis, a significant contributor to morbidity and mortality in
the elderly population.

Conclusion

The relationship between exercise and the menstrual cycle is, to say the least,
complex. There is a lot of conflicting evidence with regards to the potential risks of
intense exercise but a number of conclusions can be drawn from the evidence
presented above; exercise seems unlikely to delay menarche, if such a delay
occurred it would have serious implications for achievement of peak BMD and
osteoporosis risk, but instead it seems weight-bearing exercise is more likely to be
beneficial in terms of bone mineral deposition. Intense exercise through its effects on
the hypothalamus (and more specifically the GnRH pulse generator) is a known
reversible cause of amenorrhoea, the consequences of this include osteopaenia,
however, as yet osteoporotic fractures have not been shown in athletes.

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References

1. Ferin M, Jewelewicz R, Warren M: The menstrual cycle: Physiology, reproductive

disorders and infertility. New York. Oxford Press, 1993
2. Ferin M: The menstrual cycle: an integrative view. In: Reproductive
Endocrinology, Surgery, and Technology. Adashi EY, Rock JA, Rosenwaks Z
(eds). Raven Press NY, chapter 6: 103, 1996
3. Impey L, Child T, Obstetrics and Gynaecology, 3rd Edition, Wiley-Blackwell, 2009,
pp.9-11
4. Frisch RE, et al. Menstrual Cycles – Fatness as a Determinant of Minimum
Weight for Height Necessary for their Maintenance or Onset, Science 1974;185:
949
5. Frisch RE. Body fat, menarche, fitness and fertility. Human Reproduction
1987;2(6);521–33
6. Apter D. "Serum steroids and pituitary hormones in female puberty: a partly
longitudinal study". Clinical Endocrinology 1980;12 (2);107–20.
7. St George IM, Williams S, Silva PA. Body size and the menarche: the Dunedin
Study. J Adolesc Health 1994;15(7);573–576.
8. Stark O, Peckham CS, Moynihan C. Weight and age at menarche. Arch Dis Child
1989;64(3):383–387.
9. Scott EC, Johnston FE. Critical fat, menarche, and the maintenance of menstrual
cycles: A critical review Journal of Adolescent Health Care 1982;2(4);249-260
10. Losos JB, Raven PH, Johnson GB, Singer SR (2002), Biology, 2002 New York:
McGraw-Hill. pp. 1207–09
11. Zeleznik AJ, Hutchison JS, Schuler HM: Interference with the
gonadotropin-suppressing actions of estradiol in macaques overrides the
selection of a single preovulatory follicle. Endocrinology. 1985;117(3):991-9
12. Batista MC, Cartledge TP, Zellmer AW et al: Evidence for a critical role of
progesterone in the regulation of the midcycle gonadotropin surge and ovulation.
J Clin Endocrinol Metab. 1992;74(3):565-70.
13. Harris TG, Dye S, Robinson JE et al: Progesterone can block transmission of the
estradiol-induced signal for luteinizing hormone surge generation during a
specific period of time immediately activation of the GnRH surge-generating
system. Endocrinology. 1999;140(2):827-34
14. Mathur DN, Toriola AL, Age at menarche in Nigerian athletes, Br J Sports Med

Andrew Haslett Matriculation Number: 0507107

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1982;16:250-252
15. Malina RM, Ryan RC and Bonci CM, ‌Age at menarche in athletes and their
mothers and sisters, Annals of Human Biology. 1994;21(5): 417-422
16. Rees M, The Age of Menarche, ORGYN 1995;4:2-4
17. Baxter-Jones ADG, Helms P, Preece M, et al.. Menarche in intensively trained
gymnasts, swimmers and tennis players. Ann Hum Biol 1994;21(5);407-415
18. Petridou E, Syrigou E, Toupadaki N, et al. Determinants of age at menarche as
early life predictors of breast cancer risk. Int J Cancer 1996;68(2):193–198.
19. Colditz GA, Willett WC, Stampfer MJ, et al. A prospective study of age at
menarche, parity, age at first birth, and coronary heart disease. Am J Epidemiol
1987;126:861-70.
20. Soefer EF, Scholl TO, Sobel E, et al. Menarche: target age for reinforcing sex
education for adolescents. J Adolesc Health Care 1985;6:383-86.
21. Sandler DP, Wilcox AJ, Horney LF, Age at menarche and subsequent
reproductive events. Am J Epidemiol 1984;119:765-74.
22. Rosenthal DI, Mayo-Smith W, Hayes CW, Khurana JS, Biller BM, Neer RM &
Klibanski A. Age and bone mass in premenopausal women. Journal of Bone and
Mineral Research 1989;4:533–538
23. Fujiwara S, Kasagi F, Yamada M & Kodama K. Risk factors for hip fracture in a
Japanese cohort. Journal of Bone and Mineral Research 1997;12:998–1004
24. Roy DK, O’Neill TW, Finn JD, et al. 2003 Determinants of incident vertebral
fracture in men and women: results from the European Prospective Osteoporosis
Study (EPOS). Osteoporosis International 2003;14:19–26
25. Loucks AB, Brown R, King K, Thuma JR, Verdum M. A combined regimen of
moderate dietary restriction and exercise training alters luteinizing hormone
pulsatility in regularly menstruating young women. The 77th Annual Meeting of
The Endocrine Society, Washington, DC, 1995 (Abstract 558)
26. Prior JC, Cameron K, Ho Yuen B, Thomas J. Menstrual cycle changes with
marathon training: anovulation and short luteal phase. Can J Appl Sport Sci
1982;7:173-177
27. Otis CL. Exercise-associated amenorrhea. Clin Sports Med 1992;11:351-62
28. Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The
inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports
Med 1994;13:405-18
29. Berga SL, Mortola JF, Girton L et al: Neuroendocrine aberrations in women with

Andrew Haslett Matriculation Number: 0507107

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functional hypothalamic amenorrhea. J Clin Endocrinol Metab. 1989;68(2):301-8.

30. Filicori M, Tabarelli C, Casadio P et al: Interaction between menstrual cyclicity
and gonadotropin pulsatility. Horm Res. 1998;49(3-4):169-72.
31. Carbon RJ, Exercise, amenorrhoea and the skeleton, British Medical Bulletin
1992;48(3):546-560
32. Drinkwater BL, Nelson K, On S, Chesnut CH. Bone mineral density after
resumption of menses in amenorrhoeic athletes. J Am Med Assoc 1986;
256:380-382
33. Cann CE, Martin MC, Genant HK, Jaffe RB. Decreased spinal bone mineral
content in amenorrheic women. J Am Med Assoc 1984;251:626-629
34. Lindberg JS, Fears WB, Hunt MM, Powell MR, Boll D, Wade DE.
Exercise-Induced Amenorrhea and Bone Density. Ann Int Med 1984;101(5):
647-648
35. Vuori I. Peak bone mass and physical activity: a short review. Nutr Rev
1996;54:S11-4
36. Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes.
JAMA 1996;276:238-40.
37. Matkovic V, Jelic T, Wardlaw GM, Ilich JZ, Goel PK, Wright JK, et al. Timing of
peak bone mass in Caucasian females and its implication for the prevention of
osteoporosis. Inference from a cross-sectional model. J Clin Invest
1994;93:799-808

Further Reading

1. Blell M, Pollard TM, Pearce MS. Predictors of age at menarche in the Newcastle
thousand families study. J Biosoc Sci. 2008;40(4);563–575.
2. Baxter-Jones A, Helms P, Preece M, et al., Age at Menarche. The Lancet
1994;343(8894);423-424
3. Malina RM, Spirduso WW, Tate C, Baylor AM. Age at menarche and selected
menstrual characteristics in athletes at different competitive levels and in different
sports. Med Sci Sports 1978; 10: 218-222
4. Jones IE, Taylor RW, Williams SM, Manning PJ, Goulding A. 2002a Four-year
gain in bone mineral in girls with and without past forearm fractures: a DXA study.
Dual energy X-ray absorptiometry. Journal of Bone and Mineral Research
2002;17:1065–1072

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5. Parfitt AM. Misconceptions (1): epiphyseal fusion causes cessation of growth.

Bone 2002;30:337–339
6. Bullen BA, Skrinar GS, Beitins IZ, von Mering G, Turnbull BA, McArthur JW,
Induction of menstrual disorders by strenuous exercise in untrained women
NEJM 1985;312:1349-1353
7. Xiao E, Xia-Zhang L, Ferin M: Stress and the menstrual cycle: short- and
long-term response to a five-day endotoxin challenge during the luteal phase in
the rhesus monkey. J Clin Endocrinol Metab. 1999;84(2):623-6.
8. Koprowski C, Ross RK, Mack WJ, et al. Diet, body size and menarche in a
multiethnic cohort. Br J Cancer 1999;79(11–12);1907–1911.
9. Frisch RE, Delayed Menarche and Amenorrhoea in Ballet Dancers, New England
Journal of Medicine 1980;303:17
10. Loucks AB, Mortola JF, Girton L et al: Alterations in the
hypothalamic-pituitary-ovarian and the hypothalamic-pituitary-adrenal axes in
athletic women. J Clin Endocrinol Metab. 1989;68(2):402-11.
11. Pirke KM, Schweiger U, Broocks A et al: Luteinizing hormone and follicle
stimulating hormone secretion patterns in female athletes with and without
menstrual disturbances. Clin Endocrinol (Oxf). 1990;33(3):345-53.
12. Bonen A: Exercise-induced menstrual cycle changes. A functional, temporary
adaptation to metabolic stress. Sports Med. 1994;17(6):373-92.
13. Drinkwater, B. L. (1994). McCoy research lecture. Does physical activity plan a
role in preventing osteoporosis? Research Quarterly for Exercise and Sport.
65:197-206
14. Myburgh KH, Hutchins J, Fataar AB, Hough SF, Noakes TD. Low bone density is

an etiologic factor for stress fractures in athletes. Ann Intern Med 1990;113:754-9.

Andrew Haslett Matriculation Number: 0507107