You are on page 1of 12

Carlberg, K. A., M. T. Buckman, G. T. Peake' and M. L. Riedesel' 1933. A survey of rnenstrual function in athletes. Eur. J. Appt. Phys:Lq,_l.

51: 2LI-222.

i'hidi616gv
and Occupational physioogy

SpringetrVerlaq 1983

A Survey of Menstrual

Function in Athletes*

K. A. Carlberg, M. T. Buckman, G.T.Peake, and M. L. Riedesel


Departments of Biology and Medicine, University of New Mexico and Veterans Administration Medical Center, Albuquerque, NM 87131, USA

Summary. Questionnaires were given

to

254 female athletes and 426

nonathletic control subjects, and interviews were conducted with 95 athletes. Menstrual characteristics in the two groups were strikingly different, with oligo/amenorrhea reportedby 12.I% of the athletes and 2.60/o ofthe control subjects, and regular menstruation reported by 42.9% of the athletes and 64.3% of the control subjects. About half the athletes interviewed were able to cite specific changes in their menstruation that were associated with specific changes in their athletic training. Low body weight was the factor most commonly associated with oligoiamenorrhea in athletes, but among the control subjects menstrual characteristics did not appear to be influenced by

body weight. Lighter oligo/amenorrheic athletes reported more severe menstrual disturbances than heavier oligo/amenorrheic athletes. Distance runners reported fewer menstrual periods per year than other athletes, and weekly training distance appeared to influence menstrual characteristics among the runners. Other factors which appeared to be associated with athletic oligo/amenorrhea included a vegetarian diet and a high altitude environment. We conclude that menstrual disturbances are often associated with athletic training, and that several factors, particularly low body weight, can increase susceptibility to exercise-related oligo/amenorrhea.
Key words: Exertion
weight

Menstruation

Menstruation disorders

Body

Introduction

With the recent surge in athletic competition for women, there has been an increased awareness that strenuous exercise can affect female reproductive
function. There is now a consensus that athletic women experience amenorrhea
* Supported by NIH grants 2R01-HD05794-08 and 5M01-ER00997-05 Offprint requests /o. Karen A. Carlberg, PhD, Department of Physiology, Box J-274, University of Florida College of Medicine, Gainesville, FL 32610, USA

212

K- A. Carlbers et al.

and oligomenorrhea more frequently than other women. Estimates for the incidence of amenorrhea and other menstrual disturbances among athletes have ranged from2o/o to 57% (Zaharieva 1965; Vaclavinkova and Druckmuller 1969; Feicht et al. 1978; Levenets 1979;Wakat et al.1982).In contrast, the incidence of amenorrhea in the general population of women has been estimated to be between 2Vo and 5Vo (Pettercson et d.. 1973; Singh 1981; Bachmann and Kemmann 1982). No direct comparisons have been made between large numbers of athletes and sedentary women, and it is difficult to make comparisons between different studies because of wide variations in definitions for various menstrual disorders. Thus the first objective of this study was to assess the incidence of amenorrhea in comparable populations of athletic and nonathletic women. There is little information available about athletes who experience menstrual disturbances. Amenorrhea appears to be more common in women with more rigorous training programs (Erdelyi 1976; Feicht et al. 1978; Dale et aL.7979). Low body weight may also contribute to the development of exercise-related menstrual irregularities (Speroff and Redwine 1980; Frisch et al. 1981; Schwartz et al. 1981). The second objective of this study was to describe more completely the characteristics common to amenorrheic athletes. Material and Methods
questionnaire was given to 303 female athletes and 637 nonathletic control subjects. It included questions about menstrual and reproductive history, age, body size, and athletic activity. The questionnaire was approved by the Human Research Review Committee of the University of New Mexico School of Medicine. The athletes were ciassified into three categories: Category 1 - members of collegiate varsity athletic teams (n:180, age 19.5 year + 1.7 SD), Category 2 - members of high school varsity athletic teams (n: 69, age 16.3 year + 1.1), and Category 3 - other athletes, primarily distance runners (n:54, age 30.2 year + 7.0). The control subjects were women enrolled in university classes (n : 637, age 27.7 year + 5.0). Questionnaires from the control subjects and the athletes in Categories 1 and 2 were obtained by going to team workouts. competitions. or university c.lasses and requesting that all women present complete the form. Thus the data represent a cross-section of college athletes, high school athletes, and college students. Athlete categories used for each statistical analysis will be specified in the Results. In general, only Category 1 athletes were used in comparisons with the control subjects, because these two groups were comparable in age, whereas ail three categories were used for comparisons of athletes with different menstrual characteristics. The athletes competed in nine different sports: distance running (n:83), track and freld (n:71), basketball (n - 35), volleyball (n:28), swimming and diving (n:25), tennis (n : 19), gymnastics @: M), softball (zr : 13), and skiing (n : 9).

Menstrual categories were defined as: regular menstruation-menstrual cycles between 23 and 35 days in length during the previous year, irregular menstruation-menstrual cycles longer than 35 days or shorter than 23 days at least once during the previous year, and oligo/amenorrhea-no menstrual

periods during the previous 3 months, or four or fewer periods during the previous year.76Vo ofthe athletes and 33o/o of the controi subjects were eliminated from the study because they had used oral contraceptives within the previous 6 months, been pregnant or breast-feeding within the previous year, had a hysterectomy or other medical treatment interfering with menstruation, or provided inadequate information. All subjects were at least 1 year post-menarche.

Relative weight for height was evaluated by two indices. Percent ideal body weight was
calculated from Metropolitan Life Insurance Tables (1959). Livi Index was computed by the formula

(ke)/height (m) (Olivier 10v-weight

1969).

Menstrual Function in Athletes

Lt)

Interviews were conducted with 26 oligo/amenorrheic athletes and 26 athletes with irregular menstruation. Each woman was asked the following questions: I. What were your menstrual periods like before you became amenorrheic (or irregular)? II. Were changes in your menstruation associated with changes in your athletic training? III. Were changes in your menstruation associated with changes in your weight or diet? IV. Were changes in your menstruation associated with emotional or psychological stress? V. What do you think is the cause for your amenorrhea (or irregular menstruation)? After answering these questions the women were encouraged to talk freely about their observations and experiences. In addition, 43 questionnaires contained sufficient information in response to an essay question to be included with the results ofthe interviews. Thus information from a total of 32 oligo/amenorrheic athletes and 63 irregularly menstruating athletes was included. Statistical analyses included chi-square contingency tables, two-sample t-tests, one-way analyses of variance, and Duncan's multiple range tests (Zar 1974). A significance level of 0.05 was
used.

Results

Menstrual Characteristics

of

College Athletes and Control Subjects

The incidences of regular menstruation, irregular menstruation, and oligo/amenorrhea were compared in the college athletes (Category 1) and control subjects because these two populations of women were considered to be comparable.

Chi-square contingency table analysis indicated that menstrual category was highly dependent on subject category t, < 0.0001, Table 1). Oligo/amenorrhea (12.1%) and irregular menstruation (45.0%) were much more common in the

athletes than

in the control

subjects (2.6% and 33.I%), while regular

menstruation was more common in the control subjects (64.3Eo) than in the athletes (42.9%). Among the high school athletes, percentages of subjects with regular menstruation (32.47o), irregular menstruation (57 .4%), and oligo/amenorrhea (I0.3%) were similar to those of the college athletes.

Menstrual Charscteristics and Bodv Size


Menstrual characteristics appeared to U" i-po.tantly related to body size among the athletes, but not among the control subjects. Several physical characteristics of athletes and control subjects with regular menstruation, irregular menstruation, and oligo/amenorrhea were evaluated by one-way analyses of variance and Duncan:s multiple range tests (Table 2). When comparisons were made among the athletes (Categories 7,2, and 3) in the three menstrual categories, there were no differences in height, but weight, percent ideal body weight, and Livi Index were highest in athletes with regular menstruation and lowest in athletes with oligo/amenorrhea. In contrast, control subjects with regular menstruation, irregular menstruation, and oligo/amenorrhea were similar in all body size parameters excepts height. Among both athletes and control subjects, women with regular menstruation tended to be older than women with irregular menstruation or oligo/amenorrhea, but differences were slight.

274

K. A. Carlberg et al.

Table 1. Menstrual categories in athletes and control subjectso

Regularmenstruation Irregularmenstruation Oligo/Amenorrhea


college

(n (n

: :

athletesb subjects

60
274

(42.9%) (64.3Ea)

63
747

(45.0Eo) (33.1%)

77 (12.1Vo)

140)

Controi

1I

(2.6%)

426)

" p < 0.0001 by chi-square contingency table b Category 1 only

Table 2. Characteristics of women with regular menstruation, irregular menstruation,


oligo/amenorrhea Athletesu

and

Regular (n:1,04)
21.8 (+

Irregular (n:n\

menstruation menstruation
Age (year) Height (cm)

Oligo/
Amenorrhea

p'

@:36)
0.01

weight (kg)
Percent ideal body weight Livi index

6.7)b 19.4 (+ 4.3;a 20.s (t 5.0) (!7.4) 166.7 (+ 7.6) 166.5 (r 6.6) (! 7.7) s6.1 (r 7.3) 53.0 (+ 6.7)" 100.7 (+ 8.2) 98.6 (t 7.0) 94.0 (+ 6.9)"
r66.s s7.7
23.2

n.s.f
0.00s 0.0001 0.0001

(t 0.8)

22.9 (+

0.7)d

22.5 (+

o.qe

Control subjects

Regular Irregular Oligo/ menstruation menstruation Amenorrhea (n : 1.41) (n : 7t) @ : 27\


Age (year) Height (cm)
Weight (kg)
Percent ideal body weight Livi index

22.0 (t 16s.3 (+

102.0 (+ 23.2

5.4) 6.7) s7.3 (+ 8.3)

163.8 702.2

13.0)

4.614 19.8 (+ 2.4)d 0.02 6.1)d 161.4 (+ 6.8)d 0.02 s6.4 (t 7.8) s6.6 (t s.2) n.s.
20.6 (+

(+

(+ 10.4) 108.1 (+ 17.2)


23.8

n.s. n.s.

(! 1.1)

23.4

(t0.9)

(t 1.4)

a d

b Mean +

Categories 1,
SD

2,

and

'

One-Way analysis of variance Significantly different from women with regular menstruation, p
test

< 0.05, Duncan's multiple

range

' Significantly different from women with regular menstruation and irregular p < 0.05, Duncan's multiple range test r n.s. : not significant

mdnstruation,

Classification of subjects into three weight categories, underweight, normal

weight, and overweight, provided further demonstration that body weight influences the incidence of menstrual disturbances among athletes, but not among nonathletic women (Table 3). Underweight was defined as less than
94

.0% ideal body weight, normal weight

as 94.0

105 .9Vo

ideal body weight, and

Menstrual Function in

Athletes

21.5

Table 3. Menstrual categories in underweight, normai weight, and overweight womenu Athletesb (p

<

0.005")

Regular menstruation

lrregularmenstruation Oligo/Amenorrhea
30 (42o/o) 67 (48Eo) 17 (40%)

Underweight

(37Vo)

te

(21%) (11%)

(n -- 7r)
Normal weight @ ra0)

58

(41%) (s6%)

ts

Overweight

2(s%)

@:a3)
Control subjects (n.s.d)
Regular menstruation

Irregularmenstruation Oligo/Amenorrhea
33 (30Vo) 66 (31%) 42 (41%)

Underweight

(n : 110)

75 (68Vo)

(2Vo)

Normal weight

(n : 2Ia)

r44 (67%)
(54Vo)

4 (2%)

Overweight (n: 102)

(s%)

Underweight : less than 94.lVo ideal body weight, normal weight weight, overweight : 106.0% ideal body weight and over
Categories 1, 2, and 3 Chi-square contingency table n.s. : not significant

91.0-105.9% ideal body

overweight as 106.07o ideal body weight and over. Chi-square contingency table analyses indicated that menstrual category was dependent on weight category in athletes (Categories 1.,2, and 3), but not in control subjects. Among the athletes, regular menstruation was reported by increasingly fewer women as percent ideal body weight declined, and oligoiamenorrhea was present in increasingly more women as percent ideal body weight declined. Among the control subjects, percentages of women in the three menstrual categories were similar among women who were underweight, normal weight, and overweight. Using the same

three weight categories, contingency table analyses showed that among underweight and normal weight women menstrual category was highly dependent on subject category (p < 0.0001 for both weight categories). However, percentages of women with regular menstruation, irregular menstruation, and oligo/amenorrhea among overweight athletes were nearly the same as those for overweight control subjects, and did not differ significantly from those for the entire control population. Thus, participation in athletics appeared to influence menstrual characteristics among women of normal or below normal weight, but not among women with weights above normal.
Among the oligo/amenorrheic athletes (Categories 1.,2, and 3) there was an interesting relationship between duration of amenorrhea and body weight (Fig. 1). AII of the oligo/amenorrheic athletes weighing more than 55 kg had been

21,6

K. A. Carlberg et al.

G-

9so
IL
6 o o

836 r!
E c f

.9 r.

att

o
55 75

weishr (ke)
Fig. 1. Relationship between body weight and duration of amenorrhea in 28 oligo/amenorrheic
athletes

amenorrheic for 3-6 months. These women either had a few menstrual periods each year, or they were amenorrheic only during their competitive seasons and menstruated relatively frequently the rest of the year. On the other hand, most of the oligo/amenorrheic athletes weighing less than 55 kg had been amenorrheic for 1 year or more. Average weight for athletes who had been amenorrheic for amenorrheic less than a year (a9 kg + 4 SD, n:76 vs 57 kg -r 7, n:72, p <0.002, two-tailed two-sample /-test). There was no difference between the heavier and lighter athletes in duration of athletic training. The mean duration of amenorrhea was 23 months, with a range of 3-70 months.

more than

year was significantly less than

for

athletes who had been

Menstrual Characteristics and Athletic Training

each of the competitive sports represented by the athlete popultion (Categories 1 and 2) Ihe incidence of oligo/amenorrhea (range 6-78%) appeared to be higher than that in the control population, and the incidence of regular menstruation (range 30-59%) appeared to be lower than that in the control population. Oligo/amenorrhea was most common among distance runners (1.8% of the women competing at 1,500 m and over), and distance runners reported significantly fewer menstrual periods during the previous year (9.2 + 4.7 SD) than other athletes (11.1 + 3.3, p < 0.02, two-tailed two-sample

In

Among distance runners (Categories L, 2, and 3) both weekly training distance and body weight appeared to be important in the development of menstrual irregularities. Of the athletes whose primary sport was distance running, oligo/amenorrheic runners (n : 15) averaged 79 km/week + 32 SD, while runners with regular (n : 13) and irregular menstruation (n : 18)

/-test).

Menstrual Function in Athletes

2r1

o Ollgp/AmercrrtElc Runners I lrregubrly l\llenslrualing Runnrs . Flegularly Merelruallng RunneE

'aa ol

I
oo
o o

bl
OE
a

ro

a o

20

40

Kilomelers Per\ reek

60

80

100

120

Fig. 2. Relationship between weekly training distance, percent ideal body weight, and menstrual characteristics in 71 distance runners

averaged 60 + 27 and 53

21 km/week respectively (p

< 0.05, one-way analysis

of variance). When distance runners were categorized as underweight, normal weight, and overweight, as previously described, oligo/amenorrhea was reported by 52Vo of the underweight runners (n : 21),13% of the normal weight runners (n : 39) , and none of the overweight runners (n : 8), and regular menstruation was reportedby 29% of the underweight runners, 38% of the normal weight runners, and 6370 of the overweight runners 0? < 0.005, contingency table). Figure 2 illustrates the relationships between weekly training distance, percent ideal body weight, and menstrual characteristics in 71 women who compete in distance running. All 19 of the oligo/amenorrheic runners weighed less than I00% ldeal body weight. Of the 11 women who ran more than 81 km/week and weighed less than 1007o ideal body weight, none had regular menstruation, and all seven women running more than 90 km/week and weighing less than 100% ideal body weight were totally amenorrheic.

Menarche Menarche was significantly later in the athletes (Categories7,2, and 3; 13.4 year + 1.5 SD) than in the control subjects (12.9 year + 1.5;p < 0.0001, two-tailed two-sample /-test). Differences between athletes with regular menstruation (13. 1 year + 1.4), irregular menstruation (13.5 year + 1.5), and oligo/amenorrhea

(13.5 year
insignificant.

+ 1.5) were

shown by one-way analysis

of

variance

to

be

218

K. A. Carlberg et al.

Interviews

Exercise was the factor most often cited by the athletes as affecting their
menstruation. 917o of the oligo/amenorrheic athletes and 68Vo of the irregularly menstruating athletes said that exercise was a contributing factor in their menstrual disturbances . 56% of the oligo/amenorrheic athletes and 22Vo of the irregularly menstruating athletes were able to describe specific increments in their training programs which briefly preceded or coincided with cessation of menses or changes in the character of their menstrual periods. Menstrual changes most often reported were prolonged intervals between menses and a reduced volume of menstrual flow. Other observations included more frequent

menstrual periods, shorter duration of menstrual flow, longer duration of menstrual flow, increased volume of menstrual flow, reduced dysmenorrhea, and increased dysmenorrhea. A reduction in exercise was associated with resumption of menses or a more normal frequency of menstrual periods in28% of the oligoiamenorrheic athletes and 1I% of the irregularly menstruating athletes. Five amenorrheic women who generally train year-round reported having a menstrual period within a month of a reduction in training due to vacation or injury, and a resumption of amenorrhea with a return to normal physical activity. Ten athletes said that it was normal for them to menstruate during their off-season but not during heavy training or competition. 28Vo of the oligoiamenorrheic athletes and 22Vo ofthe irregularly menstruating athletes had been continuously involved in athletic competition since before menarche and had never had regular menstruation; about half these women reported more frequent menses when their training was reduced. Only one of the amenorrheic athletes was known to have stopped athletic training during the course of this study. After 4 years of collegiate tennis she had her first menstrual period in 4 years within a month of the end of her last competitive season, and at last report she had continued to menstruate at 28-29 day intervals for 8 months. Loss of weight appeared to be important in the development of menstrual disturbances in 47 7o of the oligo/amenorrheic athletes and 117a of the irregularly menstruating athletes. Fifteen oligo/amenorrheic athletes reported that cessation or prolongation of their menstrual cycles had accompanied weight losses ranging from 2 to 21 kg. The weight loss usuaily resulted from simultaneous dieting and increased exercise. Three athletes had identified a weight threshold for their menstruation which was around 907o ideal body weight in each case. They menstruated sporadically when they weighed more than this threshold, but not when they dropped below it. Six amenorrheic athletes believed that a change to a vegetarian diet was at least partially responsible for the development of their menstrual abnormalities. In all cases other changes occured in their lives concurrently, including increased exercise or weight loss. All of these women were underweight, ranging from 82 to 907o ideal body weight. Only one athlete was known to have become a vegetarian without changes in her menstruation; she was 1767o ideal body
weight.

by 28% of the

Emotional stress was believed to have contributed to menstrual disturbances oligo/amenorrheic athleles and 467o of the irregularly

Menstrual Function in

Athletes

219

menstruating athletes. The stresses most often cited were moving to a new school, new state, or new country. For many athletes moving to a new state or country entailed moving from near sea level to high altitude (i.e., 1,130-1,640 m). Five athletes believed that moving to altitude was one cause for their menstrual irregularities. Discontinuing oral contraceptives appeared to contribute to the menstrual
disturbances of three athletes. All three women were underweight and two were vegetarians. Exercise may also affect menstruation during oral contraceptive use. One distance runner reported that her menstrual flow gradually declined and eventually ceased entirely as she increased her training distance to 65 km/week, despite continuous use of birth control pills. She was 94Vo ideal body weight.

Discussion This is the first study to compare menstrual patterns in a large number of female athletes and a comparable control population. The distribution of women among the three menstrual categories was strikingly different in the two groups, with the athletes having a much higher incidence of oligoiamenorrhea and a much lower incidence of regular menstruation than the nonathletic women. A strong influence of exercise duration or intensity on menstrual

characteristics was most clearly demonstrated by the athletes' interview responses. The majority of the athletes with oligo/amenorrhea or irregular menstruation stated that exercise had affected their menstrual cycles, and over half the women were able to cite specific changes in their menstruation that were associated with changes in their athletic training. These included disruptions in menstrual function associated with increases in exercise, and normalization of menstrual function associated with reductions in exercise. In addition, weekly training distance was higher in oligo/amenorrheic distance runners than in
menstruating runners. We cannot discount the possibility that physical attributes which may predispose a girl or woman to success in athletics may also predispose her to menstrual disturbances. Nevertheless there appears to be a significant association between strenuous exercise and menstrual dysfunction, at least in certain susceptible women. The most important factor in susceptibility to athletic oligoiamenorrhea appears to be low body weight. The largest differences between athletes with oligoiamenorrhea and those with regular menstruation were in weight, percent ideal body weight, and Livi Index. Underweight athletes had a much higher incidence of oligo/amenorrhea than athletes of normal weight. Overweight athletes, on the other hand, had menstrual characteristics similar to those of the

control population. In other words, for women of normal or below normal percent ideal body weight, participation in athletics appeared to have a significant effect on menstrual characteristics, but for women above normal in percent ideal body weight participation in athletics appeared much less likely to affect menstruation. Thus there appears to be an interaction between athletic training and low body weight that disrupts normal menstrual function. It may be

220
disturbances.

K. A. Carlberg er al.

that excess weight somehow protects women from exercise-related menstrual Loss of weight was associated with the development or worsening of oligomenorrhea or amenorrhea in about half the oligoiamenorrheic athletes interviewed. Therefore it appears that loss of weight, as well as chronically low weight, may contribute to the development of exercise-related menstrual
disturbances.

The relationship between duration of amenorrhea. and body weight was surprising and interesting. oligo/amenorrheic athletes weighing more thin 55 kg were oligomenorrheic, whereas most oligo/amenorrheic athletes weighing less than 55 kg were totally amenorrheic. Thus lighter athletes experienced a more
severe form

of

menstrual disturbance than heavier athletes.

All of

these

observations considered together emphasize the importance of low body weight in susceptibility to athletic oligo/amenorrhea. It is well known that extreme low body weight and weight loss are often associated with menstrual disturbances in nonathletic women (Frisch and McArthw 1974; Frisch 1977; Knuth et al.
7977).

An association of vegetarianism with athletic amenorrhea might be related to hormonal changes that have been reported to accompany dietary alterations. changes in pituitary, gonadal, and adrenocortical hormone secretion have been associated with changes from a conventional diet to a vegetarian diet and vice versa (Hill and Wynder 1976; HllI et al. 1977,1980). Schwartz et al. (1981) reported that amenorrheic runners consumed a smaller percentage of their calories as protein than did regularly menstruating runners or nonrunners. While the association between vegetarianism and amenorrhea was rather tenuous in the participants in our study, the findings of these investigators do give some credibility to the athletes' observations. Emotional stress appeared to be a relatively minor factor in the development of menstrual disturbances in the athletes. It might be expected that cbllege
athletes would be exposed to more stresses than the average student as a result of

their higher mobility and their dual roles as athletes and students. It is not known whether questionnaire and interview responses of the athletes accurately reflect the degree of emotional stress they have experienced. However, changes in menstrual function among athletes in this study did not appear to be associated with emotional stresses as often as with changes in exercise programs. The observation by several athletes that moving to high altitude affected their menstruation was intriguing. There are some data to support an effect of altitude on reproductive function. Girls living at high altitude (about 1,600m) were reported to reach menarche later than other girls (valsik 1965;Frisch and Revelle 1971). Men traveling or living at altitude (3,500-4,270m) had sperm abnormalities, reduced fertility rates, and reduced blood gonadotropin levels (Donayre et al. 1968; Guerra Garcia 1971; Sobrevilla and Midgley 1971; Bangham and Hackett 7978; Humpeler et al. 1980). High altitude natives (2,940 m) had reduced gonadotropin responses to a synthetic luteinizing hormone-releasing hormone analog (Paredes Suarez et al. 1982). Thus it is possible that altitude exposure may alter endocrine function sufficiently in some women to contribute to menstrual disturbances.

Menstrual Function in Athletes

227

The delayed menarche reported by our athlete population agrees with the observations of other investigators (Malina et al. I9'73,1978; Sidhu and Grewal 1980).

An

even larger difference

in

age at menarche might be found

if

comparison were made between girls who were and were not involved in athletic competition at the time of puberty. It cannot be assumed that an amenorrheic athlete is infertile. One amenorrheic participant in our study conceived about 4 months after her last menstrual period, and she has not menstruated in the 4 years since delivering a normal child. The consequences of athletic oligo/amenorrhea for fertility after a woman has stopped competing are not known. Several participants in our study resumed menstruation within a month of a reduction or cessation of training, indicating

that athletic oligo/amenorrhea may be a temporary condition. Longitudinal studies are needed to answer this question. We conclude that menstrual disturbances are much more common among athletes than among nonathletic women. Many factors other than strenuous exercise are associated with athletic oligoiamenorrhea and thus may increase a woman's susceptibility to this condition. Low body weight is the factor most commonly associated with athletic oligo/amenorrhea. Other factors, including
participation in long-distance running, a vegetarian diet, emotional stress, a high altitude environment, and discontinuation of oral contraceptives, may be important and deserve further study. In many women it may be the combined effects of two or more stresses, including strenuous exercise, that result in disruption of cyclic menstrual activity.
Acknowledgements. We thank Ms. Allyson E,. Adams for help with data collection and analysis. Dr. Lambert H. Koopmans and Mr. W. Curtis Hunt provided valuable assistance with computer analysis of the data.

References GA, Kemmann E (1982) Prevalence of oligomenorrhea and amenorrhea in a college population. Am J Obstet Gynecol 744l.98-702 Bangham CRM, Hackett PH (1978) Effects of high altitude on endocrine function in the Sherpas of Nepal. J Endocrinol 79:147-1.48 Dale E, Gerlach DH, Wilhite AL (1979) Menstrual dysfunction in distance runners. Obstet Gynecol
Bachmann

54:47

53

Donayre J, Guerra Garcia R, Moncloa F, Sobrevilla LA (1968) Endocrine studies at high altitude. IV. Changes in the semen of men. J Reprod Fertil 16:55-58 Erdelyi GJ (1976) Effects of exercise on the menstrual cycle. Phys Sportsmed 4(3):79-8i Feicht CB, Johnson TS, Martin BJ, Sparkes KE, Wagner WW Jr (1978) Secondary amenorrhea in Frisch RE (1977) Food intake, fatness, and reproductive ability. In: Vigersky RA (ed) Anorexia nervosa. Raven Press, New York, pp 1,49-1,67 Frisch RE, Gotz-Welbergen AV, McArthur JW, Albright T, Witschi J, Bullen B, Birnholz J, Reed RB, Hermann H (1981) Delayed menarche and amenorrhea of college athletes in relation to age

athletes. Lancet 2: 1115-1146 fl-etter]

of onset of training. JAMA 246:1559-1563


Frisch RE, McArthur JW (1974) Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185: 949-951

222

K. A. Carlberg et al
a hypothesis

Frisch RE, Revelle R (1971) Height and weight at menarche and

of menarche. Arch Dis

Child 46: 695-70r


Guerra Garcia R (1971) Testosterone metabolism in men exposed to high aititude. Acta Endocrinol Panam 2'.55-64 Hill P, Chan P, Cohen L, Wynder E, Kuno K (1977) Diet and endocrine-related cancer. Cancer 39: 1820-1826 Hill P, Garbaczewski L, Helman P, Huskisson J, Sporangisa E, Wynder EL (1980) Diet, lifestyle, and menstrual activity. Am J clin Nutr 33: 1792-1,L98 Hill P, Wynder E (1916) Diet and prolactin release. Lancet 2:806-807 Humpeler E, Skrabal F, Bartsch G (1980) Influence of exposure to moderate altitude on the plasma

concentration of cortisol, aldosterone, renin, testosterone, and gonadotropins. Eur J Appl Physiol 45:167-176 Knuth UA, Hull MGR, Jacobs HS (1977) Amenorrhoea and loss of weight. Br J Obstet Gynaecol

84:801-807
Levenets SA (1979) Peculiar features of physical and sexual development of girls regularly going in

for sport. Gig Sanit 7:25-28 Malina RM, Harper AB, Avant HH, Campbell DE (1973) Age at menarche in athletes and non-athletes. Med Sci Sports 5: 11-13 Malina RM, Spirduso WW, Tate C, Baylor AM (1978) Age at menarche and selected menstrual characteristics in athletes at different competitive levels and in different sports. Med Sci Sports 10:278-222 Metropolitan Life Insurance Company (1959) New weight standards for men and women. Statist Bull 40: 1-4
Olivier G (1969) Practical anthropology. CC Thomas, Springfiled, IL, pp 39-42 Paredes Suarez M, VareaTeran JR, Garces G, Avila C, Coy DH, Schally AV (1982) Pituitary
response to luteinizing hormone-releasing hormone analog at sea level and high altitudes. Obstet

Gynecol 59:52-57
Pettersson F, Fries H, Nillius SJ (1973) Epidemiology of secondary amenorrhea. I. Incidence and prevalence rates. Am J Obstet Gynecol 117:80-86 Schwartz B, Cumming DC, Riordan E, Selye M, Yen SSC, Rebar RW (1981) Exercise-associated

amenorrhea: a distinct entity? Am J Obstet Gynecol l4l:662-670 R (1980) Age of menarche in various categories of Indian sportswomen. Br J Sports Med 14:199-203 Singh KB (1981) Menstrual disorders in college students. Am J Obstet Gynecol 740:299-302 Sobrevilla LA, Midgley AR (1971) The plasma gonadotropin response to acute high altitude exposure. Acta Endocrinol Panam 2:47-53 Speroff L, Redwine DB (1980) Exercise and menstrual function. Phys Sportsmed 8(5):41-52 Vaclavinkova V, Druckmuller V (1969) Menstrual cycle and its disorders in artistic and sports gymnasts. Cas Lek Ces 108:769-'/11 Valsik JA (1965) The seasonal rhythm of menarche: a review. Hum Biol 37:75-90 Wakat DK, Sweeney KA, Rogoi AD (1982) Reproductive system function in women cross-country runners. Med Sci Sports Exer 14:263-269 Zaharieva E (1965) Survey of sportswomen at the Tokyo Olympics. J Sports Med Phys Fitness
Sidhu LS, Grewal
5 :275-279 Zar JH (1974) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ

Accepted January26, 1983