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

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 Laughlin, G. A.
Right arrow Articles by Yen, S. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Laughlin, G. A.
Right arrow Articles by Yen, S. S.

Journal of Clinical Endocrinology & Metabolism, Vol 81, 4301-4309, Copyright © 1996 by Endocrine Society


ARTICLES

Nutritional and endocrine-metabolic aberrations in amenorrheic athletes

GA Laughlin and SS Yen
Department of Reproductive Medicine, University of California-San Diego School of Medicine, La Jolla 92093-0633, USA.

Growing evidence suggests that menstrual disturbances in female athletes are related to the metabolic cost of high levels of energy expenditure without compensatory increases in dietary intake. However, the linkage(s) between nutritional deficits and reproductive impairments as a result of slowing of LH pulsatility has not been defined. This study was directed to simultaneously characterize nutritional intake, insulin sensitivity (by rapid iv glucose tolerance test), and 24-h dynamics of insulin/glucose, cortisol, somatotropic [GH/GH-binding protein (GHBP)/insulin-like growth factor I (IGF-I)/IGF- binding proteins (IGFBPs)], and LH axes in highly trained athletes with (cycling athletes; CA) and without (amenorrheic athletes; AA) menstrual cyclicity and in age- and body mass index-matched cycling sedentary controls (CS; n = 8/group). Although daily caloric intake did not differ among the three groups, athletes (CA and AA) consumed less fat and protein than CS. However, the restriction of fat was 50% greater (P < 0.01) in AA than CA and was accompanied by increased carbohydrate (P < 0.05) and fiber (P < 0.01) intake. Athletes, independent of menstrual status, had increased (P < 0.05) insulin sensitivity and reduced insulin levels during the feeding phase of the day. Hypoinsulinemia was more pronounced in AA (P < 0.05) than CA, extending throughout the day, and was accompanied by reduced glucose increments in response to meals (P < 0.05), not seen in CA. Levels of the insulin-dependent IGFBP-1 were markedly elevated (P < 0.001) throughout the diurnal pattern in AA, whereas in CA, a modest elevation (P < 0.001) of IGFBP-1 levels occurred only during the feeding portion of the day. IGFBP-1 levels for the three groups related inversely to 24-h insulin (r = -0.63) and directly to 24-h cortisol (r = 0.69) levels. A 70-80% augmentation (P < 0.001) of 24-h mean GH levels was seen in both groups of athletes, but with distinct pulsatile features. Although pulse amplitude was increased 60% in CA with no change in pulse number, AA displayed more frequent (P < 0.001) pulses, with an elevated (P < 0.01) baseline between pulses. The distorted pattern of GH pulses seen in AA was associated with a 35% decrease in GHBP levels, not seen in CA. Although levels of IGF-I and IGFBP-3 did not differ in either CA or AA, the 2- to 4-fold higher levels of IGFBP-1 in AA than in CA and CS resulted in a 3-fold reduced ratio of IGF-I/IGFBP-1 in AA, which may decrease the bioactivity and hypoglycemic effect of IGF-I. LH pulse frequency was progressively attenuated in the athletes, with a greater (P < 0.001) slowing in AA than CA, unaccompanied by alterations in pulse amplitude or 24-h levels. LH pulse frequency was related positively with insulin (r = 0.65) levels and the ratio of IGF-I/IGFBP-1 (r = 0.69), and negatively with cortisol (r = -0.70) and IGFBP-1 (r = -0.75) concentrations. Stepwise regression analysis suggested that negative influences associated with hypercortisolemia and elevated IGFBP-1 levels predominate in determining GnRH/LH pulsatile activity in these athletes. In sum, although neuroendocrine-metabolic adaptations to the energy cost of exercise training were evident in both groups of athletes, AA displayed alterations distinct from their cycling counterparts, with evidence of a hypometabolic state, including decreased basal body temperature and reduced levels of plasma glucose and serum GHBP, a decrease in the ratio of IGF-I/IGFBP-1, accelerated GH pulse frequency, and elevated interpulse GH levels. Thus, in AA, increased insulin sensitivity, decreased circulating insulin, and a reduced hypoglycemic effect of IGF-I together with elevated GH and cortisol concentrations may comprise a cascade of glucoregulatory adaptations to repartition metabolic fuels for conservation of protein. (ABSTRACT TRUNCATED)


This article has been cited by other articles:


Home page
Hum ReprodHome page
A. Rickenlund, M. Thoren, A. Nybacka, J. Frystyk, and A. Linden Hirschberg
Effects of oral contraceptives on diurnal profiles of insulin, insulin-like growth factor binding protein-1, growth hormone and cortisol in endurance athletes with menstrual disturbance
Hum. Reprod., October 19, 2009; (2009) dep350v1.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Endocrinol. Metab.Home page
W. Huang, M. Acosta-Martinez, T. H. Horton, and J. E. Levine
Fasting-induced suppression of LH secretion does not require activation of ATP-sensitive potassium channels
Am J Physiol Endocrinol Metab, December 1, 2008; 295(6): E1439 - E1446.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
J. L. Chan, C. J. Williams, P. Raciti, J. Blakeman, T. Kelesidis, I. Kelesidis, M. L. Johnson, M. O. Thorner, and C. S. Mantzoros
Leptin Does Not Mediate Short-Term Fasting-Induced Changes in Growth Hormone Pulsatility but Increases IGF-I in Leptin Deficiency States
J. Clin. Endocrinol. Metab., July 1, 2008; 93(7): 2819 - 2827.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
J. Z. Kasa-Vubu, A. Rosenthal, E. G. Murdock, and K. B. Welch
Impact of Fatness, Fitness, and Ethnicity on the Relationship of Nocturnal Ghrelin to 24-Hour Luteinizing Hormone Concentrations in Adolescent Girls
J. Clin. Endocrinol. Metab., August 1, 2007; 92(8): 3246 - 3252.
[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
Br. J. Sports. Med.Home page
C L Zanker and M P Warren
Regulation of reproductive function in athletic women: an investigation of the roles of energy availability and body composition * Commentary
Br. J. Sports Med., June 1, 2006; 40(6): 489 - 490.
[Full Text] [PDF]


Home page
EndocrinologyHome page
M. E. Lujan, A. A. Krzemien, R. L. Reid, and D. A. Van Vugt
Developing a Model of Nutritional Amenorrhea in Rhesus Monkeys
Endocrinology, January 1, 2006; 147(1): 483 - 492.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. Rickenlund, M. J. Eriksson, K. Schenck-Gustafsson, and A. L. Hirschberg
Oral Contraceptives Improve Endothelial Function in Amenorrheic Athletes
J. Clin. Endocrinol. Metab., June 1, 2005; 90(6): 3162 - 3167.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. Rickenlund, M. J. Eriksson, K. Schenck-Gustafsson, and A. L. Hirschberg
Amenorrhea in Female Athletes Is Associated with Endothelial Dysfunction and Unfavorable Lipid Profile
J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1354 - 1359.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
N. R. Vulliemoz, E. Xiao, L. Xia-Zhang, M. Germond, J. Rivier, and M. Ferin
Decrease in Luteinizing Hormone Pulse Frequency during a Five-Hour Peripheral Ghrelin Infusion in the Ovariectomized Rhesus Monkey
J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5718 - 5723.
[Abstract] [Full Text] [PDF]


Home page
NEJMHome page
C. K. Welt, J. L. Chan, J. Bullen, R. Murphy, P. Smith, A. M. DePaoli, A. Karalis, and C. S. Mantzoros
Recombinant Human Leptin in Women with Hypothalamic Amenorrhea
N. Engl. J. Med., September 2, 2004; 351(10): 987 - 997.
[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
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
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
J. Clin. Endocrinol. Metab.Home page
M. J. de Souza, J. Van Heest, L. M. Demers, and B. L. Lasley
Luteal Phase Deficiency in Recreational Runners: Evidence for a Hypometabolic State
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 337 - 346.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
S. Andrico, A. Gambera, C. Specchia, C. Pellegrini, L. Falsetti, and E. Sartori
Leptin in functional hypothalamic amenorrhoea
Hum. Reprod., August 1, 2002; 17(8): 2043 - 2048.
[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
Am. J. Physiol. Endocrinol. Metab.Home page
D. E. Larson-Meyer, B. R. Newcomer, and G. R. Hunter
Influence of endurance running and recovery diet on intramyocellular lipid content in women: a 1H NMR study
Am J Physiol Endocrinol Metab, January 1, 2002; 282(1): E95 - E106.
[Abstract] [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
J. Clin. Endocrinol. Metab.Home page
D. L. Waters, C. R. Qualls, R. Dorin, J. D. Veldhuis, and R. N. Baumgartner
Increased Pulsatility, Process Irregularity, and Nocturnal Trough Concentrations of Growth Hormone in Amenorrheic Compared to Eumenorrheic Athletes
J. Clin. Endocrinol. Metab., March 1, 2001; 86(3): 1013 - 1019.
[Abstract] [Full Text]


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
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
J. Clin. Endocrinol. Metab.Home page
Author's Response
J. Clin. Endocrinol. Metab., December 1, 1999; 84(12): 4751 - 4751.
[Full Text]


Home page
J. Clin. Endocrinol. Metab.Home page
A. E. Taylor, J. Hubbard, and E. J. Anderson
Impact of Binge Eating on Metabolic and Leptin Dynamics in Normal Young Women
J. Clin. Endocrinol. Metab., February 1, 1999; 84(2): 428 - 434.
[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
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. 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 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 © 1996 by The Endocrine Society