The DOI matches its Crossref record; 46 of the 47 references it cites were found in a registry or an index.
High Frequency of Luteal Phase Deficiency and Anovulation in Recreational Women Runners: Blunted Elevation in Follicle-Stimulating Hormone Observed during Luteal-Follicular Transition1
Abstract
The purposes of this investigation were to evaluate the characteristics of three consecutive menstrual cycles and to determine the frequency ofluteal phase deficiency (LPD) and anovulation in a sample of sedentary and moderately exercising, regularly menstruating women. For three consecutive menstrual cycles, subjects collected daily urine samples for analysis of FSH, estrone conjugates (E1C), pregnanediol-3-glucuronide (PdG), and creatinine (Cr). Sedentary (n=11) and exercising (n=24) groups were similar in age (27.0+/-1.3 yr), weight (60.3+/-3.1 kg), gynecological age (13.8+/-1.2 yr), and menstrual cycle length (28.3+/-0.8 days). Menstrual cycles were classified by endocrine data as ovulatory, LPD, or anovulatory. No sedentary women (0%) had inconsistent menstrual cycle classifications from cycle to cycle, but 46% of the exercising women were inconsistent. The sample prevalence of LPD in the exercising women was 48%, and the 3-month sample incidence was 79%. In the sedentary women, 90% of all menstrual cycles were ovulatory (SedOvul; n=28), whereas in the exercising women only 45% were ovulatory (ExOvul; n=30); 43% were LPD (ExLPD; n=28), and 12% were anovulatory (ExAnov; n=8). In ExLPD cycles, the follicular phase was significantly longer (17.9+/-0.7 days), and the luteal phase was significantly shorter (8.2+/-0.5 days) compared to ExOvul (14.8+/-0.9 and 12.9+/-0.3 days) and SedOvul (15.9+/-0.6 and 12.9+/-0.4 days) cycles. Luteal phase PdG excretion was lower (P < 0.001) in ExLPD (2.9+/-0.3 microg/mg Cr) and ExAnov (0.8+/-0.1 microg/mg Cr) cycles compared to SedOvul cycles (5.0+/-0.4 microg/mg Cr). ExOvul cycles also had less (P < 0.01) PdG excretion during the luteal phase (3.7+/-0.3 microg/mg Cr) than the SedOvul cycles. E1C excretion during follicular phase days 2-5 was lower (P=0.05) in ExOvul, ExLPD, and ExAnov cycles compared to SedOvul cycles and remained lower (P < 0.02) in the ExLPD and ExAnov cycles during days 6-12. The elevation in FSH during the luteal-follicular transition was lower (P < 0.007) in ExLPD (0.7+/-0.1 ng/mg Cr) cycles compared to SedOvul and ExOvul cycles (1.0+/-0.1 and 1.1+/-0.1 ng/mg Cr, respectively). Energy balance and energy availability were lower (P < 0.05) in ExAnov cycles than in other menstrual cycle categories. The blunted elevation in FSH during the luteal-follicular transition in exercising women with LPD may explain their lower follicular estradiol levels. These alterations in FSH may act in concert with disrupted LH pulsatility as a primary and proximate factor in the high frequency of luteal phase and ovulatory disturbances in regularly menstruating, exercising women.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In a follow-up study, an acute bout of moderate intensity aerobic exercise did not exert the same effects on ghrelin and insulin for women using a monophasic COC and the participants maintained an energy deficit after exercise”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [139]
Citations
Cites
Generalized equations for predicting body density of women
Jackson, A. S., Pollock, M. L., & Ward, A. (1980) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198023000-00009 · Cited by 1,840
Regulation of ovarian follicular development in primates: facts and hypotheses
GOUGEON, A. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-2-121 · Cited by 1,497
Rivier, C., & Rivest, S. (1991) · Biology of Reproduction · doi:10.1095/biolreprod45.4.523 · Cited by 799
Metabolic fuels and reproduction in female mammals
Wade, G. N., & Schneider, J. E. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80183-6 · Cited by 686
(1986) · CERN Document Server (European Organization for Nuclear Research) · Cited by 583
Low energy availability, not stress of exercise, alters LH pulsatility in exercising women
Loucks, A. B., Verdun, M., Heath, E. M., & (With the Technical Assistance of T. Law, S. A. J. R. T. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.1.37 · Cited by 539 · cited 5×
“In this context, energy availability may be usefully defined as dietary energy intake minus exercise energy expenditure (30, 40).”
BackgroundInfluentialSelf-citationInduction of Menstrual Disorders by Strenuous Exercise in Untrained Women
Bullen, B. A., Skrinar, G. S., Beitins, I. Z., von Mering, G., Turnbull, B. A., & McArthur, J. W. (1985) · New England Journal of Medicine · doi:10.1056/nejm198505233122103 · Cited by 484
Loucks, A. B., Mortola, J. F., GIRTON, L., & Yen, S. S. C. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-68-2-402 · Cited by 478
Self-citationSpinal Bone Loss and Ovulatory Disturbances
Prior, J. C., Vigna, Y. M., Schechter, M. T., & Burgess, A. E. (1990) · New England Journal of Medicine · doi:10.1056/nejm199011013231801 · Cited by 459
Frequency of factors associated with habitual abortion in 197 couples
Daya, S., & Stephenson, M. D. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58382-4 · Cited by 429
Munro, C. J., Stabenfeldt, G. H., Cragun, J. R., Addiego, L. A., Overstreet, J. W., & Lasley, B. L. (1991) · Clinical Chemistry · doi:10.1093/clinchem/37.6.838 · Cited by 421
Self-citationPituitary and Gonadal Hormones in Women during Spontaneous and Induced Ovulatory Cycles
ROSS, G. T., Cargille, C. M., LIPSETT, M. B., Rayford, P. L., Marshall, J. R., Strott, C. A., & Rodbard, D. (1970) · Elsevier eBooks · doi:10.1016/b978-0-12-571126-5.50005-4 · Cited by 373
Menstrual Dysfunction in Distance Runners
Dale, E., Gerlach, D. H., & WILHITE, A. L. (1979) · Obstetrics and Gynecology · doi:10.1097/00006250-197907000-00013 · Cited by 302
SECONDARY AMENORRHŒA IN ATHLETES
Feicht, C. B., Johnson, T., Martin, B. J., Sparkes, K., & Wagner, W. W. (1978) · The Lancet · doi:10.1016/s0140-6736(78)92294-8 · Cited by 279
Nutritional and endocrine-metabolic aberrations in amenorrheic athletes
Laughlin, G. A., & YEN, S. S. C. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.12.8954031 · Cited by 236
Luteal phase defect: the sensitivity and specificity of diagnostic methods in common clinical use
Jordan, J., Craig, K., Clifton, D. K., & Soules, M. R. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56815-0 · Cited by 203
Altered Neuroendocrine Regulation of Gonadotropin Secretion in Women Distance Runners*
Veldhuis, J. D., Evans, W. S., DEMERS, L. M., Thorner, M. O., Wakat, D. K., & Rogol, A. D. (1985) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-61-3-557 · Cited by 186
Moderate recreational running is associated with lowered salivary progesterone profiles in women
Ellison, P. T., & Lager, C. (1986) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(86)90737-4 · Cited by 185
Is athletic amenorrhea specific to runners?
Sanborn, C. F., Martin, B. J., & Wagner, W. W. (1982) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(82)90463-x · Cited by 176
The diagnosis of luteal phase deficiency: a critical review
Wallach, E. E., McNeely, M. J., & Soules, M. R. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59999-3 · Cited by 175
Loucks, A. B. (1994) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.78.4.910 · Cited by 174
Self-citationBREAST CANCER INCIDENCE IN WOMEN WITH A HISTORY OF PROGESTERONE DEFICIENCY
Cowan, L. D., Gordis, L., Tonascia, J., & Jones, G. S. (1981) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a113184 · Cited by 154
Effects of exercise training on the menstrual cycle
Loucks, A. B. (1990) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199006000-00001 · Cited by 151
Self-citationCANCER NEAR POTENTIAL SITES OF NUCLEAR INSTALLATIONS
Cook-Mozaffari, P., Darby, S. C., & Doll, R. (1989) · The Lancet · doi:10.1016/s0140-6736(89)91500-6 · Cited by 148
Hall, J. E., Schoenfeld, D., Martin, K. A., & Crowley, W. F. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.3.1740493 · Cited by 148
Induction and prevention of low-T3 syndrome in exercising women
Loucks, A. B., & Callister, R. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.264.5.r924 · Cited by 145
Self-citationSherman, B. M., & Korenman, S. G. (1974) · Cancer · doi:10.1002/1097-0142(197405)33:5 · Cited by 140
Body weight, exercise and menstrual status among ballet dancers in training
Abraham, S. F., Beumont, P. J. V., Fraser, I. S., & Llewellyn‐Jones, D. (1982) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1982.tb03649.x · Cited by 132
Cyclic ovarian function in recreational athletes
Broocks, A., Pirke, K., Schweiger, U., Tuschl, R. J., Laessle, R. G., Strowitzki, T., Horl, E., Horl, T., Haas, W., & Jeschke, D. (1990) · Journal of Applied Physiology · doi:10.1152/jappl.1990.68.5.2083 · Cited by 126
Calabrese, L. H., Kirkendall, D. T., Floyd, M., Rapoport, S., Williams, G. W., Weiker, G. G., & Bergfeld, J. A. (1983) · The Physician and Sportsmedicine · doi:10.1080/00913847.1983.11708458 · Cited by 125
The effect of marathon training upon menstrual function
Shangold, M. M., & Levine, H. S. (1982) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(82)90464-1 · Cited by 124
Luteal Phase Deficiency: Characterization of Reproductive Hormones over the Menstrual Cycle*
Soules, M. R., McLachlan, R. I., Ek, M., Dahl, K. D., COHEN, N. L., & Bremner, W. J. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-69-4-804 · Cited by 119
Exercise Induces Two Types of Human Luteal Dysfunction: Confirmation by Urinary Free Progesterone*
Beitins, I. Z., McArthur, J. W., Turnbull, B. A., Skrinar, G. S., & Bullen, B. A. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-72-6-1350 · Cited by 97
The reproductive system and exercise in women
Loucks, A. B., Vaitukaitis, J. L., Cameron, J. L., Rogol, A. D., Skrinar, G. S., Warren, M. P., Kendrick, J. S., & Limacher, M. C. (1992) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199206001-00011 · Cited by 79
Self-citationReproductive system function in women cross-country runners
Wakat, D. K., Sweeney, K. A., & Rogol, A. D. (1982) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198204000-00002 · Cited by 67
Souza, M. J. D., Miller, B., Sequenzia, L. C., Luciano, A. A., Ulreich, S., Stier, S. A. G., Prestwood, K. M., & Lasley, B. L. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.9.4201 · Cited by 52
Self-citationExercise, Body Weight, and Amenorrhea in Professional Ballet Dancers
Cohen, J. L., Kim, C. S., May, P., & Ertel, N. H. (1982) · The Physician and Sportsmedicine · doi:10.1080/00913847.1982.11947206 · Cited by 48
Bone density and cyclic ovarian function in trained runners and active controls
Winters, K. M., Adams, W. C., MEREDITH, C. N., Loan, M. D. V., & Lasley, B. L. (1996) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199607000-00002 · Cited by 46
Self-citationChristin‐Maître, S., Taylor, A. E., Khoury, R. H., Hall, J. E., Martin, K. A., Smith, P. C., Albanese, C., Jameson, J. L., Crowley, W. F., & Sluss, P. M. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.6.8964832 · Cited by 41
Qiu, Q., Kuo, A., Todd, H., Dias, J. A., Gould, J. E., Overstreet, J. W., & Lasley, B. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00475-5 · Cited by 35
Self-citationSouza, M. J. D. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.9.2867 · Cited by 33
Qiu, Q., Overstreet, J. W., Todd, H., Nakajima, S. T., Stewart, D. R., & Lasley, B. L. (1997) · Environmental Health Perspectives · doi:10.1289/ehp.97105862 · Cited by 29
Self-citationLuteal phase defect and breast cancer genesis
MAUVAIS-JARVIS, P., Sitruk-Ware, R. L., & Kuttenn, F. (1982) · Breast Cancer Research and Treatment · doi:10.1007/bf01806450 · Cited by 27
Impaired follicular growth and abnormal luteinizing hormone surge in luteal phase defect
Ayabe, T., Tsutsumi, O., Momoeda, M., Yano, T., Mitsuhashi, N., & Taketani, Y. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56641-2 · Cited by 21
Luteal phase defects and ectopic pregnancy
Guillaume, A. J., Benjamin, F., Sicuranza, B. J., Deutsch, S., & Spitzer, M. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57292-6 · Cited by 14
Luteal-Phase Deficiency: The Most Common Abnormality of the Menstrual Cycle?
Soules, M. R. (1989) · Springer eBooks · doi:10.1007/978-3-642-74631-4_11 · Cited by 5
Research works printed but not linked: 2
- De Souza, 1992, Effects of exercise training on sex steroids: endocrine profile and clinical implications., Infertil Reprod Med Clin North Am, 3, 129
- Ross, 1970, Pituitary and gonadal hormones during spontaneous and induced menstrual cycles., Recent Prog Horm Res, 26, 1
Cited by
Sorted by citations
(2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318149f111 · Cited by 1,554
Self-citationLoucks, A. B., & Thuma, J. R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020369 · Cited by 760
Self-citationMountjoy, M., Ackerman, K. E., Bailey, D. M., Burke, L. M., Constantini, N., Hackney, A. C., Heikura, I. A., Melin, A., Pensgaard, A. M., Stellingwerff, T., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-106994 · Cited by 724
De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M., Goolsby, M., Matheson, G., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093218 · Cited by 661
Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline
Gordon, C. M., Ackerman, K. E., Berga, S. L., Kaplan, J. R., Mastorakos, G. P., Misra, M., Murad, M. H., Santoro, N. F., & Warren, M. P. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00131 · Cited by 674
Metadata
- Authors
- De Souza, M. J., Miller, B. E., Loucks, A. B., Luciano, A. A., Pescatello, L. S., Campbell, C. G., & Lasley, B. L.
- Affiliations
- Center for Fertility and Reproductive Endocrinology (M.J.D.S., B.E.M., A.A.L.), New Britain General Hospital, New Britain, Connecticut 06050
- New Britain General Hospital (US)
- Ohio University (US)
- University of Hartford (US)
- University of California, Davis (US)
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1998-12-01
- Volume
- 83
- Issue
- 12
- Pages
- 4220-4232
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2135324780
- Cited by
- 315
- References
- 47
- Citations by year
- 2026: 1 · 2025: 11 · 2024: 8 · 2023: 12 · 2022: 10 · 2021: 13 · 2020: 12 · 2019: 12 · 2018: 6 · 2017: 11 · 2016: 18 · 2015: 9 · 2014: 22 · 2013: 16 · 2012: 16
- FWCI
- 3.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Environmental Health Sciences (ES 06198, P01ES006198)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Keywords
- luteal phase deficiency, anovulation, female runners, follicle-stimulating hormone, luteal phase, follicular phase, pregnanediol-3-glucuronide, estrone conjugates, ovulation, exercise-induced amenorrhea, urinary hormone excretion, sedentary women
- MeSH terms
- Adolescent, Adult, Anovulation, Energy Intake, Energy Metabolism, Estrogens, Female, Follicular Phase, Follicle Stimulating Hormone, Humans, Luteal Phase, Menstrual Cycle, Nutritional Physiological Phenomena, Physical Education and Training, Progesterone, Recreation, Running
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review