help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS

Journal of Clinical Endocrinology & Metabolism Vol. 68, No. 2 402-411
doi:10.1210/jcem-68-2-402
Copyright © 1989 by the Endocrine Society.
This Article
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by LOUCKS, A. B.
Right arrow Articles by YEN, S. S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by LOUCKS, A. B.
Right arrow Articles by YEN, S. S. C.

Alterations in the Hypothalamic-Pituitary-Ovarian and the Hypothalamic-Pituitary-Adrenal Axes in Athletic Women*

A. B. LOUCKS, J. F. MORTOLA, L. GIRTON and S. S. C. YEN{dagger}

Department of Reproductive Medicine, School of Medicine (T-002) and the General Clinical Research Center, University of California-San Diego La Jolla, California 92093

Address all correspondence and requests for reprints to: Dr. A. B. Loucks, Department of Zoological and Biomedical Sciences, Ohio University, Athens, Ohio 45701.

The functional integrity of the hypothalamicpituitary-ovarian and hypothalamic-pituitary-adrenal axes was assessed by determining pulsatile LH, ACTH, and cortisol secretion during the early follicular phase in athletic women with regular menstrual cycles (CA; n = 9), athletic women with amenorrhea (AA; n = 9), and regularly cyclic sedentary women (CS; n = 8). The CA and AA women were not significantly different in body composition, exercise training, psychometric tests, or dietary consumption. The CA women had shorter luteal phases (P < 0.05) and lower urinary excretion of pregnanediol glucuronide than the CS women. In the AA women, urinary estrone glucuronide, pregnanediol glucuronide, and LH excretion were low throughout a 30-day period.

The CA women had a 24-h pattern of pulsatile LH secretion characterized by reduced frequency (P < 0.05) and increased amplitude (P < 0.05), yielding an overall increased 24-h mean level (P < 0.05), but interpulse intervals similar to those in the CS women. During sleep, LH pulse frequency slowed in the CS and CA women, while pulse amplitude increased and the mean serum LH level decreased in both groups. The AA women had even fewer pulses (P < 0.05) of normal amplitude occurring at much more variable (P < 0.01) interpulse intervals. Sleepassociated changes in LH pulsatility were absent. Responses to a 10-µg bolus GnRH dose revealed blunted (P < 0.05) FSH release in CA and augmented (P < 0.05) LH release in AA women.

The groups did not differ in any 24-h ACTH pulse pattern parameter or in cortisol pulse frequencies. Yet, early morning (0200–0800 h) serum cortisol levels were higher (P < 0.05) in both groups of athletes, and this elevation was extended through the day (0800–2000 h; P < 0.001) and evening (2000–0200 h; P < 0.05) in the AA women. The plasma ACTH and serum cortisol responses to bolus human CRH administration were blunted in the CA and AA women [change from baseline ({Delta}) in ACTH, P < 0.05 and P < 0.01; {Delta} cortisol, P < 0.01 and P < 0.01, respectively], but adrenal sensitivity ({Delta} cortisol/{Delta} ACTH ratio) was increased (P < 0.05). The plasma ACTH and serum cortisol responses to meals also were blunted in the athletic groups (P < 0.05).

These results indicate that the degree to which the hypothalamic-pituitary-adrenal axis is disturbed in cyclic and amenorrheic athletes is associated, perhaps causally, with their hypothalamic-pituitary-ovarian axis abnormalities.

* This work was supported by NICHHD Grant HD-21198-02, NICHHD Research Center Grant HD-12303, and in part Grant USPHS RR-00827 from the General Clinical Research Branch, Division of Research Resources, NIH. This work was conducted in part by the Clayton Foundation for Research, California Division.

{dagger} Clayton Foundation Investigator.

Received May 23, 1988.




This article has been cited by other articles:


Home page
ReproductionHome page
C. Garcia, P. C Lee, and L. Rosetta
Impact of social environment on variation in menstrual cycle length in captive female olive baboons (Papio anubis)
Reproduction, January 1, 2008; 135(1): 89 - 97.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Endocrinol. Metab.Home page
N. I. Williams, S. L. Berga, and J. L. Cameron
Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys
Am J Physiol Endocrinol Metab, July 1, 2007; 293(1): E270 - E276.
[Abstract] [Full Text] [PDF]


Home page
Cancer Epidemiol. Biomarkers Prev.Home page
M.-F. Chan, M. Dowsett, E. Folkerd, S. Bingham, N. Wareham, R. Luben, A. Welch, and K.-T. Khaw
Usual Physical Activity and Endogenous Sex Hormones in Postmenopausal Women: The European Prospective Investigation into Cancer-Norfolk Population Study
Cancer Epidemiol. Biomarkers Prev., May 1, 2007; 16(5): 900 - 905.
[Abstract] [Full Text] [PDF]


Home page
Br. J. Sports. Med.Home page
A B Loucks
Refutation of "the myth of the female athlete triad"
Br. J. Sports Med., January 1, 2007; 41(1): 55 - 57.
[Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
M. M. Wenner, A. V. Prettyman, R. E. Maser, and W. B. Farquhar
Preserved autonomic function in amenorrheic athletes
J Appl Physiol, August 1, 2006; 101(2): 590 - 597.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. B. Loucks
The Response of Luteinizing Hormone Pulsatility to 5 Days of Low Energy Availability Disappears by 14 Years of Gynecological Age
J. Clin. Endocrinol. Metab., August 1, 2006; 91(8): 3158 - 3164.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
B. Brundu, T. L. Loucks, L. J. Adler, J. L. Cameron, and S. L. Berga
Increased Cortisol in the Cerebrospinal Fluid of Women with Functional Hypothalamic Amenorrhea
J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1561 - 1565.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
J. B. Becker, A. P. Arnold, K. J. Berkley, J. D. Blaustein, L. A. Eckel, E. Hampson, J. P. Herman, S. Marts, W. Sadee, M. Steiner, et al.
Strategies and Methods for Research on Sex Differences in Brain and Behavior
Endocrinology, April 1, 2005; 146(4): 1650 - 1673.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
K. M. Breen, H. J. Billings, E. R. Wagenmaker, E. W. Wessinger, and F. J. Karsch
Endocrine Basis for Disruptive Effects of Cortisol on Preovulatory Events
Endocrinology, April 1, 2005; 146(4): 2107 - 2115.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
G. N. Wade and J. E. Jones
Neuroendocrinology of nutritional infertility
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2004; 287(6): R1277 - R1296.
[Abstract] [Full Text] [PDF]


Home page
Hum Reprod UpdateHome page
M. J. De Souza and N. I. Williams
Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women
Hum. Reprod. Update, September 1, 2004; 10(5): 433 - 448.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
M. J. De Souza, H. J. Leidy, E. O'Donnell, B. Lasley, and N. I. Williams
Fasting Ghrelin Levels in Physically Active Women: Relationship with Menstrual Disturbances and Metabolic Hormones
J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3536 - 3542.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
M. F. Dallman, S. E. la Fleur, N. C. Pecoraro, F. Gomez, H. Houshyar, and S. F. Akana
Minireview: Glucocorticoids--Food Intake, Abdominal Obesity, and Wealthy Nations in 2004
Endocrinology, June 1, 2004; 145(6): 2633 - 2638.
[Abstract] [Full Text] [PDF]


Home page
Arch Pediatr Adolesc MedHome page
J. Z. Kasa-Vubu, M. Sowers, W. Ye, N. E. Carlson, and T. Meckmongkol
Differences in Endocrine Function With Varying Fitness Capacity in Postpubertal Females Across the Weight Spectrum
Arch Pediatr Adolesc Med, April 1, 2004; 158(4): 333 - 340.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. Rickenlund, M. Thoren, K. Carlstrom, B. von Schoultz, and A. L. Hirschberg
Diurnal Profiles of Testosterone and Pituitary Hormones Suggest Different Mechanisms for Menstrual Disturbances in Endurance Athletes
J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 702 - 707.
[Abstract] [Full Text] [PDF]


Home page
Br. J. Sports. Med.Home page
P Klentrou and M Plyley
Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls
Br. J. Sports Med., December 1, 2003; 37(6): 490 - 494.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
P. K. Dhillon and V. L. Holt
Recreational Physical Activity and Endometrioma Risk
Am. J. Epidemiol., July 15, 2003; 158(2): 156 - 164.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. B. Loucks and J. R. Thuma
Luteinizing Hormone Pulsatility Is Disrupted at a Threshold of Energy Availability in Regularly Menstruating Women
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 297 - 311.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
B. Sternfeld, M. K. Jacobs, C. P. Quesenberry Jr., E. B. Gold, and M. Sowers
Physical Activity and Menstrual Cycle Characteristics in Two Prospective Cohorts
Am. J. Epidemiol., September 1, 2002; 156(5): 402 - 409.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
M. P. Warren, J. Brooks-Gunn, R. P. Fox, C. C. Holderness, E. P. Hyle, and W. G. Hamilton
Osteopenia in Exercise-Associated Amenorrhea Using Ballet Dancers as a Model: A Longitudinal Study
J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3162 - 3168.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
B. A. Kaufman, M. P. Warren, J. E. Dominguez, J. Wang, S. B. Heymsfield, and R. N. Pierson
Bone Density and Amenorrhea in Ballet Dancers Are Related to a Decreased Resting Metabolic Rate and Lower Leptin Levels
J. Clin. Endocrinol. Metab., June 1, 2002; 87(6): 2777 - 2783.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
E. Xiao, L. Xia-Zhang, and M. Ferin
Inadequate Luteal Function Is the Initial Clinical Cyclic Defect in a 12-Day Stress Model that Includes a Psychogenic Component in the Rhesus Monkey
J. Clin. Endocrinol. Metab., May 1, 2002; 87(5): 2232 - 2237.
[Abstract] [Full Text] [PDF]


Home page
Br. J. Sports. Med.Home page
K M Khan, T Liu-Ambrose, M M Sran, M C Ashe, M G Donaldson, J D Wark, and A Nattiv
New criteria for female athlete triad syndrome?
Br. J. Sports Med., February 1, 2002; 36(1): 10 - 13.
[Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
N. I. Williams, D. L. Helmreich, D. B. Parfitt, A. Caston-Balderrama, and J. L. Cameron
Evidence for a Causal Role of Low Energy Availability in the Induction of Menstrual Cycle Disturbances during Strenuous Exercise Training
J. Clin. Endocrinol. Metab., November 1, 2001; 86(11): 5184 - 5193.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
R. Valentino, S. Savastano, A. P. Tommaselli, G. D'Amore, M. Dorato, and G. Lombardi
The Influence of Intense Ballet Training on Trabecular Bone Mass, Hormone Status, and Gonadotropin Structure in Young Women
J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4674 - 4678.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
N. I. Williams, A. L. Caston-Balderrama, D. L. Helmreich, D. B. Parfitt, C. Nosbisch, and J. L. Cameron
Longitudinal Changes in Reproductive Hormones and Menstrual Cyclicity in Cynomolgus Monkeys during Strenuous Exercise Training: Abrupt Transition to Exercise-Induced Amenorrhea
Endocrinology, June 1, 2001; 142(6): 2381 - 2389.
[Abstract] [Full Text] [PDF]


Home page
Biol. Reprod.Home page
T.-J. Huang and P. Shirley Li
Dexamethasone Inhibits Luteinizing Hormone-Induced Synthesis of Steroidogenic Acute Regulatory Protein in Cultured Rat Preovulatory Follicles
Biol Reprod, January 1, 2001; 64(1): 163 - 170.
[Abstract] [Full Text]


Home page
Arch Gen PsychiatryHome page
E. A. Young, A. R. Midgley, N. E. Carlson, and M. B. Brown
Alteration in the Hypothalamic-Pituitary-Ovarian Axis in Depressed Women
Arch Gen Psychiatry, December 1, 2000; 57(12): 1157 - 1162.
[Abstract] [Full Text] [PDF]


Home page
PediatricsHome page
Committee on Sports Medicine and Fitness
Medical Concerns in the Female Athlete
Pediatrics, September 1, 2000; 106(3): 610 - 613.
[Abstract] [Full Text]


Home page
J. Appl. Physiol.Home page
F. S. L. Thong, C. McLean, and T. E. Graham
Plasma leptin in female athletes: relationship with body fat, reproductive, nutritional, and endocrine factors
J Appl Physiol, June 1, 2000; 88(6): 2037 - 2044.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
J. J. Puder, P. U. Freda, R. S. Goland, M. Ferin, and S. L. Wardlaw
Stimulatory Effects of Stress on Gonadotropin Secretion in Estrogen-Treated Women
J. Clin. Endocrinol. Metab., June 1, 2000; 85(6): 2184 - 2188.
[Abstract] [Full Text]


Home page
Am. J. Physiol. Endocrinol. Metab.Home page
L. K. Hilton and A. B. Loucks
Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women
Am J Physiol Endocrinol Metab, January 1, 2000; 278(1): E43 - E49.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
Growth and Pubertal Development in Elite Female Rhythmic Gymnasts
J. Clin. Endocrinol. Metab., December 1, 1999; 84(12): 4525 - 4530.
[Abstract] [Full Text]


Home page
Endocr. Rev.Home page
L. Poretsky, N. A. Cataldo, Z. Rosenwaks, and L. C. Giudice
The Insulin-Related Ovarian Regulatory System in Health and Disease
Endocr. Rev., August 1, 1999; 20(4): 535 - 582.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
M. P. Warren
Health Issues for Women Athletes: Exercise- Induced Amenorrhea
J. Clin. Endocrinol. Metab., June 1, 1999; 84(6): 1892 - 1896.
[Full Text]


Home page
J. Clin. Endocrinol. Metab.Home page
M. P. Warren, F. Voussoughian, E. B. Geer, E. P. Hyle, C. L. Adberg, and R. H. Ramos
Functional Hypothalamic Amenorrhea: Hypoleptinemia and Disordered Eating
J. Clin. Endocrinol. Metab., March 1, 1999; 84(3): 873 - 877.
[Abstract] [Full Text]


Home page
J. Clin. Endocrinol. Metab.Home page
M. J. De Souza, B. E. Miller, A. B. Loucks, A. A. Luciano, L. S. Pescatello, C. G. Campbell, and B. L. Lasley
High Frequency of Luteal Phase Deficiency and Anovulation in Recreational Women Runners: Blunted Elevation in Follicle-Stimulating Hormone Observed during Luteal-Follicular Transition
J. Clin. Endocrinol. Metab., December 1, 1998; 83(12): 4220 - 4232.
[Abstract] [Full Text]


Home page
Endocr. Rev.Home page
S. B. Seminara, F. J. Hayes, and W. F. Crowley Jr.
Gonadotropin-Releasing Hormone Deficiency in the Human (Idiopathic Hypogonadotropic Hypogonadism and Kallmann's Syndrome): Pathophysiological and Genetic Considerations
Endocr. Rev., October 1, 1998; 19(5): 521 - 539.
[Abstract] [Full Text]


Home page
Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
A. B. Loucks and M. Verdun
Slow restoration of LH pulsatility by refeeding in energetically disrupted women
Am J Physiol Regulatory Integrative Comp Physiol, October 1, 1998; 275(4): R1218 - R1226.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
E. Stacey, P. Korkia, M. V. J. Hukkanen, J. M. Polak, and O. M. Rutherford
Decreased Nitric Oxide Levels and Bone Turnover in Amenorrheic Athletes with Spinal Osteopenia
J. Clin. Endocrinol. Metab., September 1, 1998; 83(9): 3056 - 3061.
[Abstract] [Full Text]


Home page
J. Clin. Endocrinol. Metab.Home page
J. Hangaard, M. Andersen, E. Grodum, O. Koldkjær, and C. Hagen
Pulsatile Luteinizing Hormone Secretion in Patients with Addison's Disease. Impact of Glucocorticoid Substitution
J. Clin. Endocrinol. Metab., March 1, 1998; 83(3): 736 - 743.
[Abstract] [Full Text]


Home page
NEJMHome page
B. S. McEwen
Protective and Damaging Effects of Stress Mediators
N. Engl. J. Med., January 15, 1998; 338(3): 171 - 179.
[Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
A. B. Loucks, M. Verdun, and E. M. Heath
Low energy availability, not stress of exercise, alters LH pulsatility in exercising women
J Appl Physiol, January 1, 1998; 84(1): 37 - 46.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
G. A. Laughlin, C. E. Dominguez, and S. S. C. Yen
Nutritional and Endocrine-Metabolic Aberrations in Women with Functional Hypothalamic Amenorrhea
J. Clin. Endocrinol. Metab., January 1, 1998; 83(1): 25 - 32.
[Abstract] [Full Text]


Home page
NEJMHome page
I. Thune, T. Brenn, E. Lund, and M. Gaard
Physical Activity and the Risk of Breast Cancer
N. Engl. J. Med., May 1, 1997; 336(18): 1269 - 1275.
[Abstract] [Full Text] [PDF]


Home page
Am J Sports MedHome page
P. Pigeon, I. Oliver, J.P. Charlet, and P. Rochiccioli
Intensive Dance Practice: Repercussions on Growth and Puberty
Am. J. Sports Med., March 1, 1997; 25(2): 243 - 247.
[Abstract] [PDF]


Home page
J. Appl. Physiol.Home page
A. Lucia, J. L. Chicharro, M. Perez, L. Serratosa, F. Bandres, and J. C. Legido.
Reproductive function in male endurance athletes: sperm analysis and hormonal profile
J Appl Physiol, December 1, 1996; 81(6): 2627 - 2636.
[Abstract] [Full Text] [PDF]




HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals
Copyright © 1989 by The Endocrine Society