Luteal Phase Deficiency in Recreational Runners: Evidence for a Hypometabolic State
Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreatio...
Saved in:
Published in | The journal of clinical endocrinology and metabolism Vol. 88; no. 1; pp. 337 - 346 |
---|---|
Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
Bethesda, MD
Endocrine Society
01.01.2003
Copyright by The Endocrine Society |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreational runners. Menstrual cycle status was determined for three consecutive cycles in sedentary and moderately active women. Menstrual status was defined as ovulatory or LPD. Subjects were either sedentary (n = 10) or moderately active (n = 20) and were matched for age (27.7 ± 1.2 yr), body mass (60.2 ± 3.3 kg), menstrual cycle length (28.4 ± 0.9 d), and reproductive age (14.4 ± 1.2 yr). Daily urine samples for the determination of estrone conjugates, pregnanediol 3-glucuronide, and urinary levels of LH were collected. Blood was collected on a single day during the follicular phase (d 2–6) of each menstrual cycle for analysis of TSH, insulin, total T3, total T4, free T4, leptin, hGH, IGF-I, and IGF binding protein (IGFBP)-1 and IGFBP-3. Among the 10 sedentary subjects, 28 of 31 menstrual cycles were categorized as ovulatory (SedOvul). Among the 20 exercising subjects, 24 menstrual cycles were included in the ovulatory category (ExOvul), and 21 menstrual cycles were included in the LPD category (ExLPD). TSH, total T4, and free T4 levels were not significantly different among the three categories of cycles. Total T3 was suppressed (P = 0.035) in the ExLPD (1.63 ± 0.07 nmol/liter) and the ExOvul categories of cycles (1.75 ± 0.8 nmol/liter) compared with the SedOvul category of cycles (2.15 ± 0.1 nmol/liter). Leptin levels were lower (P < 0.001) in both the ExOvul (5.2 ± 0.4 μg/liter) and the ExLPD categories of cycles (5.1 ± 0.4 μg/liter) when compared with the SedOvul category of cycles (13.7 ± 1.7 μg/liter). Insulin was lower (P = 0.009) only in the ExLPD category of cycles (31.9 ± 2.8 pmol/liter) compared with the SedOvul (60.4 ± 8.3 pmol/liter) and ExOvul (61.8 ± 10.4 pmol/liter) categories of cycles. IGF-I, IGFBP-1, IGFBP-3, IGF-I/IGFBP-1, IGF-I/IGFBP-3, and hGH were comparable among the different categories of cycles. These data suggest that exercising women with LPD menstrual cycles exhibit hormonal alterations consistent with a hypometabolic state that is similar to that observed in amenorrheic athletes and other energy-deprived states, although not as comprehensive. These alterations may represent a metabolic adaptation to an intermittent short-term negative energy balance. |
---|---|
AbstractList | Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreational runners. Menstrual cycle status was determined for three consecutive cycles in sedentary and moderately active women. Menstrual status was defined as ovulatory or LPD. Subjects were either sedentary (n = 10) or moderately active (n = 20) and were matched for age (27.7 +/- 1.2 yr), body mass (60.2 +/- 3.3 kg), menstrual cycle length (28.4 +/- 0.9 d), and reproductive age (14.4 +/- 1.2 yr). Daily urine samples for the determination of estrone conjugates, pregnanediol 3-glucuronide, and urinary levels of LH were collected. Blood was collected on a single day during the follicular phase (d 2-6) of each menstrual cycle for analysis of TSH, insulin, total T3, total T4, free T4, leptin, hGH, IGF-I, and IGF binding protein (IGFBP)-1 and IGFBP-3. Among the 10 sedentary subjects, 28 of 31 menstrual cycles were categorized as ovulatory (SedOvul). Among the 20 exercising subjects, 24 menstrual cycles were included in the ovulatory category (ExOvul), and 21 menstrual cycles were included in the LPD category (ExLPD). TSH, total T4, and free T4 levels were not significantly different among the three categories of cycles. Total T3 was suppressed (P = 0.035) in the ExLPD (1.63 +/- 0.07 nmol/liter) and the ExOvul categories of cycles (1.75 +/- 0.8 nmol/liter) compared with the SedOvul category of cycles (2.15 +/- 0.1 nmol/liter). Leptin levels were lower (P < 0.001) in both the ExOvul (5.2 +/- 0.4 microg/liter) and the ExLPD categories of cycles (5.1 +/- 0.4 microg/liter) when compared with the SedOvul category of cycles (13.7 +/- 1.7 microg/liter). Insulin was lower (P = 0.009) only in the ExLPD category of cycles (31.9 +/- 2.8 pmol/liter) compared with the SedOvul (60.4 +/- 8.3 pmol/liter) and ExOvul (61.8 +/- 10.4 pmol/liter) categories of cycles. IGF-I, IGFBP-1, IGFBP-3, IGF-I/IGFBP-1, IGF-I/IGFBP-3, and hGH were comparable among the different categories of cycles. These data suggest that exercising women with LPD menstrual cycles exhibit hormonal alterations consistent with a hypometabolic state that is similar to that observed in amenorrheic athletes and other energy-deprived states, although not as comprehensive. These alterations may represent a metabolic adaptation to an intermittent short-term negative energy balance. Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreational runners. Menstrual cycle status was determined for three consecutive cycles in sedentary and moderately active women. Menstrual status was defined as ovulatory or LPD. Subjects were either sedentary (n = 10) or moderately active (n = 20) and were matched for age (27.7 +/- 1.2 yr), body mass (60.2 +/- 3.3 kg), menstrual cycle length (28.4 +/- 0.9 d), and reproductive age (14.4 +/- 1.2 yr). Daily urine samples for the determination of estrone conjugates, pregnanediol 3-glucuronide, and urinary levels of LH were collected. Blood was collected on a single day during the follicular phase (d 2-6) of each menstrual cycle for analysis of TSH, insulin, total T3, total T4, free T4, leptin, hGH, IGF-I, and IGF binding protein (IGFBP)-1 and IGFBP-3. Among the 10 sedentary subjects, 28 of 31 menstrual cycles were categorized as ovulatory (SedOvul). Among the 20 exercising subjects, 24 menstrual cycles were included in the ovulatory category (ExOvul), and 21 menstrual cycles were included in the LPD category (ExLPD). TSH, total T4, and free T4 levels were not significantly different among the three categories of cycles. Total T3 was suppressed (P = 0.035) in the ExLPD (1.63 +/- 0.07 nmol/liter) and the ExOvul categories of cycles (1.75 +/- 0.8 nmol/liter) compared with the SedOvul category of cycles (2.15 +/- 0.1 nmol/liter). Leptin levels were lower (P < 0.001) in both the ExOvul (5.2 +/- 0.4 microg/liter) and the ExLPD categories of cycles (5.1 +/- 0.4 microg/liter) when compared with the SedOvul category of cycles (13.7 +/- 1.7 microg/liter). Insulin was lower (P = 0.009) only in the ExLPD category of cycles (31.9 +/- 2.8 pmol/liter) compared with the SedOvul (60.4 +/- 8.3 pmol/liter) and ExOvul (61.8 +/- 10.4 pmol/liter) categories of cycles. IGF-I, IGFBP-1, IGFBP-3, IGF-I/IGFBP-1, IGF-I/IGFBP-3, and hGH were comparable among the different categories of cycles. These data suggest that exercising women with LPD menstrual cycles exhibit hormonal alterations consistent with a hypometabolic state that is similar to that observed in amenorrheic athletes and other energy-deprived states, although not as comprehensive. These alterations may represent a metabolic adaptation to an intermittent short-term negative energy balance. Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreational runners. Menstrual cycle status was determined for three consecutive cycles in sedentary and moderately active women. Menstrual status was defined as ovulatory or LPD. Subjects were either sedentary (n = 10) or moderately active (n = 20) and were matched for age (27.7 ± 1.2 yr), body mass (60.2 ± 3.3 kg), menstrual cycle length (28.4 ± 0.9 d), and reproductive age (14.4 ± 1.2 yr). Daily urine samples for the determination of estrone conjugates, pregnanediol 3-glucuronide, and urinary levels of LH were collected. Blood was collected on a single day during the follicular phase (d 2–6) of each menstrual cycle for analysis of TSH, insulin, total T3, total T4, free T4, leptin, hGH, IGF-I, and IGF binding protein (IGFBP)-1 and IGFBP-3. Among the 10 sedentary subjects, 28 of 31 menstrual cycles were categorized as ovulatory (SedOvul). Among the 20 exercising subjects, 24 menstrual cycles were included in the ovulatory category (ExOvul), and 21 menstrual cycles were included in the LPD category (ExLPD). TSH, total T4, and free T4 levels were not significantly different among the three categories of cycles. Total T3 was suppressed (P = 0.035) in the ExLPD (1.63 ± 0.07 nmol/liter) and the ExOvul categories of cycles (1.75 ± 0.8 nmol/liter) compared with the SedOvul category of cycles (2.15 ± 0.1 nmol/liter). Leptin levels were lower (P < 0.001) in both the ExOvul (5.2 ± 0.4 μg/liter) and the ExLPD categories of cycles (5.1 ± 0.4 μg/liter) when compared with the SedOvul category of cycles (13.7 ± 1.7 μg/liter). Insulin was lower (P = 0.009) only in the ExLPD category of cycles (31.9 ± 2.8 pmol/liter) compared with the SedOvul (60.4 ± 8.3 pmol/liter) and ExOvul (61.8 ± 10.4 pmol/liter) categories of cycles. IGF-I, IGFBP-1, IGFBP-3, IGF-I/IGFBP-1, IGF-I/IGFBP-3, and hGH were comparable among the different categories of cycles. These data suggest that exercising women with LPD menstrual cycles exhibit hormonal alterations consistent with a hypometabolic state that is similar to that observed in amenorrheic athletes and other energy-deprived states, although not as comprehensive. These alterations may represent a metabolic adaptation to an intermittent short-term negative energy balance. |
Author | de Souza, Mary Jane Demers, Laurence M Lasley, Bill L Van Heest, Jaci |
AuthorAffiliation | Women’s Exercise and Bone Health Laboratory (M.J.D.S., J.V.H.), Faculty of Physical Education and Health, University of Toronto, Toronto, Ontario, Canada M5S 2W6; Department of Kinesiology (J.V.H.), University of Connecticut, Storrs, Connecticut 06269; Penn State University (L.M.D.), Milton S. Hershey Medical Center, Hershey, Pennsylvania 17033; and Institute of Toxicology and Environmental Health (B.L.L.), University of California, Davis, California 95616 |
AuthorAffiliation_xml | – name: Women’s Exercise and Bone Health Laboratory (M.J.D.S., J.V.H.), Faculty of Physical Education and Health, University of Toronto, Toronto, Ontario, Canada M5S 2W6; Department of Kinesiology (J.V.H.), University of Connecticut, Storrs, Connecticut 06269; Penn State University (L.M.D.), Milton S. Hershey Medical Center, Hershey, Pennsylvania 17033; and Institute of Toxicology and Environmental Health (B.L.L.), University of California, Davis, California 95616 |
Author_xml | – sequence: 1 givenname: Mary Jane surname: de Souza fullname: de Souza, Mary Jane – sequence: 2 givenname: Jaci surname: Van Heest fullname: Van Heest, Jaci – sequence: 3 givenname: Laurence M surname: Demers fullname: Demers, Laurence M – sequence: 4 givenname: Bill L surname: Lasley fullname: Lasley, Bill L |
BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14467709$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/12519874$$D View this record in MEDLINE/PubMed |
BookMark | eNp1kc9rHCEUxyWkJJs01xyLl_Q2W3V0HHMLaX4UFlqSFnoTx3mybmd1ozMN-9_XMAs5VRCR9_k-Hx_P0HGIARC6pGRJGSVfNnbJCGEVYUSJ9ggtqOKiklTJY7QoBVopyX6forOcN4RQzkV9gk4pE1S1ki_Q82oawQz4x9pkwF_Beesh2D32AT-BTWBGH0MBnqYQIOVrfPfX94UA7GLCBj_ud3ELo-ni4C1-Hs0IH9EHZ4YMF4fzHP26v_t5-1itvj98u71ZVVbQVlayt4zUUEvmqHOub7iwnTOqZW3XNXXjasO7RnQtUDBMgAFrRcM7IpRl3Lj6HH2e--5SfJkgj3rrs4VhMAHilLVkijec8wIuZ9CmmHMCp3fJb03aa0r0m0a9sfpNo541lsCnQ-ep20L_jh-8FeDqAJhszeCSCdbnd47zRkqiCsdn7jUOY9H3Z5heIel1UT6uNSmrgG1V3q4JLbeqbCFLTMwxCH20yQfYJchZb-KUymfk_839D4_bnck |
CODEN | JCEMAZ |
CitedBy_id | crossref_primary_10_1249_01_MSS_0000084530_31478_DF crossref_primary_10_3390_cells11060957 crossref_primary_10_1002_ajhb_20057 crossref_primary_10_2165_00024677_200504030_00003 crossref_primary_10_1016_j_cdp_2007_04_003 crossref_primary_10_3390_ijms24043685 crossref_primary_10_1123_ijsnem_2019_0199 crossref_primary_10_3148_cjdpr_2014_024 crossref_primary_10_1007_s11154_008_9077_1 crossref_primary_10_1016_j_fertnstert_2014_04_035 crossref_primary_10_1080_13625187_2017_1410881 crossref_primary_10_1016_j_fertnstert_2006_11_171 crossref_primary_10_1177_1559827616641379 crossref_primary_10_1186_s12905_019_0779_1 crossref_primary_10_1249_01_MSS_0000084528_13358_67 crossref_primary_10_1016_j_appet_2008_09_016 crossref_primary_10_1002_ijc_29834 crossref_primary_10_1016_j_jpag_2016_09_013 crossref_primary_10_1080_0264041031000140518 crossref_primary_10_1016_j_fertnstert_2012_06_050 crossref_primary_10_1016_j_xfre_2023_04_005 crossref_primary_10_15857_ksep_2014_23_1_23 crossref_primary_10_1016_j_nurpra_2012_11_001 crossref_primary_10_1007_s00198_016_3590_y crossref_primary_10_1016_j_cpm_2006_12_004 crossref_primary_10_1158_1055_9965_EPI_04_0880 crossref_primary_10_3390_endocrines3040063 crossref_primary_10_1097_00005237_200404000_00003 crossref_primary_10_1016_j_tem_2004_10_005 crossref_primary_10_1007_s11932_007_0059_y crossref_primary_10_2105_AJPH_2007_120444 crossref_primary_10_1249_MSS_0b013e3182a32b72 crossref_primary_10_1093_humrep_dep337 crossref_primary_10_2165_11317910_000000000_00000 crossref_primary_10_1089_jwh_2006_0046 crossref_primary_10_1093_ilar_45_2_89 crossref_primary_10_1080_03014460903103921 crossref_primary_10_1097_01_AOG_0000254982_68119_16 crossref_primary_10_1016_j_mayocp_2013_07_001 crossref_primary_10_1016_j_fertnstert_2014_12_128 crossref_primary_10_1080_17461391_2021_1915391 crossref_primary_10_1093_ajcn_86_5_1791 crossref_primary_10_1123_ijsnem_2018_0127 crossref_primary_10_1097_01_CSMR_0000305620_72745_81 crossref_primary_10_3177_jnsv_57_1 crossref_primary_10_1080_02640410500456986 crossref_primary_10_1097_01_AOG_0000235704_45652_0b crossref_primary_10_29089_paom_148215 crossref_primary_10_1016_j_fertnstert_2021_02_010 crossref_primary_10_1080_02640410701607320 crossref_primary_10_1093_humrep_deq288 crossref_primary_10_1097_01_CSMR_0000306070_67390_cb crossref_primary_10_1093_humrep_dep350 crossref_primary_10_1136_bjsm_2006_031070 crossref_primary_10_1016_S1773_035X_22_00369_0 crossref_primary_10_1139_h04_005 crossref_primary_10_3389_fphys_2020_00629 crossref_primary_10_1126_sciadv_abm7201 |
Cites_doi | 10.1016/S0149-7634(05)80183-6 10.1249/00005768-199101000-00004 10.2165/00007256-199825060-00003 10.1210/jcem-68-2-301 10.1249/00005768-199510000-00007 10.1016/S0015-0282(16)60488-0 10.1016/S0015-0282(16)59523-5 10.1249/00005768-199109000-00002 10.1093/oxfordjournals.humrep.a138015 10.1146/annurev.nu.15.070195.001543 10.1249/00005768-198023000-00009 10.1152/jappl.1991.70.6.2378 10.1210/endo.140.4.6622 10.1210/jcem.84.3.5551 10.1016/0002-9378(86)90737-4 10.1210/endo-128-3-1337 10.1249/00005768-199006000-00001 10.1056/NEJM197711242972103 10.1038/372425a0 10.1016/S0015-0282(01)03010-2 10.1016/S0039-128X(97)00117-7 10.1210/jcem-60-6-1174 10.1210/jcem.82.1.3840 10.1210/jcem.86.11.8024 10.1210/endo.142.6.8113 10.1016/0022-3999(85)90010-8 10.1016/S0015-0282(16)56815-0 10.1093/clinchem/37.6.838 10.1210/jcem-68-1-135 10.1152/jappl.1998.84.1.37 10.1002/bio.1170040174 10.1056/NEJM198505233122103 10.1016/S0167-0115(00)00149-X 10.1152/ajpendo.2000.278.1.E43 10.1210/jcem-72-6-1350 10.1097/00005768-199607000-00002 10.1046/j.1365-2265.1999.00784.x 10.1097/00005768-199909000-00004 10.1016/S0889-8529(18)30233-0 |
ContentType | Journal Article |
Copyright | Copyright © 2003 by The Endocrine Society 2003 INIST-CNRS |
Copyright_xml | – notice: Copyright © 2003 by The Endocrine Society – notice: 2003 INIST-CNRS |
DBID | IQODW CGR CUY CVF ECM EIF NPM AAYXX CITATION 7X8 |
DOI | 10.1210/jc.2002-020958 |
DatabaseName | Pascal-Francis Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef MEDLINE - Academic |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef MEDLINE - Academic |
DatabaseTitleList | MEDLINE - Academic MEDLINE |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Medicine |
EISSN | 1945-7197 |
EndPage | 346 |
ExternalDocumentID | 10_1210_jc_2002_020958 12519874 14467709 00004678-200301000-00057 |
Genre | Journal Article |
GroupedDBID | - 02 08R 0R 1TH 29K 2WC 34G 39C 3O- 3V. 4.4 48X 53G 55 5GY 5RS 5YH 7X7 88E 8F7 8FI 8FJ AABJS AABMN AAIMJ AAJQQ AAPQZ AAQQT AAUQX AAWTL AAYJJ ABFLS ABOCM ABPMR ABPPZ ABSAR ABUWG ACGFS ACIMA ACPRK ACUTJ ADBBV ADBIT ADEIU ADGZP ADHKW ADRTK AELNO AELWJ AEMDU AENEX AENZO AETBJ AEWNT AFCHL AFFNX AFKRA AFRAH AFXEN AGINJ AGKRT AGVJH AHMBA AIKOY AIMBJ ALMA_UNASSIGNED_HOLDINGS APIBT AQKUS ARIXL ASMCH ASPBG AVWKF AYOIW AZFZN AZQFJ BAWUL BAYMD BBAFP BCRHZ BENPR BEYMZ BGYMP BHONS BPHCQ BSWAC BTRTY BVXVI C45 CDBKE CS3 D-I DAKXR DIK DPPUQ E3Z EBS EIHJH EJD ENERS F5P FEDTE FH7 FHSFR FOTVD FQBLK FYUFA G8K GAUVT GJ GJXCC GX1 H1 H13 HVGLF HZ H~9 IAO IHR INH J5H KBUDW KOP KQ8 KSN L7B M1P M5 MBLQV MHKGH N9A NLBLG NOYVH NVLIB O0- O9- OBH OCB ODMLO OGEVE OK1 OVD P2P PQEST PQQKQ PQUKI PRINS PROAC PSQYO REU ROX ROZ TCN TJX TLC TMA TWZ VH1 WOQ X X52 X7M XZ ZA5 ZGI ZXP ZY1 .XZ 3RD AJYGW M2M M5~ ROL ~H1 --- -~X .55 .GJ 08P 0R~ 18M 354 AABZA AACZT AAKAS AAPGJ AAPXW AAUGY AAVAP AAWDT ABBLC ABLJU ABPQP ABPTD ABWST ABXZS ACFRR ACGFO ACYHN ADGKP ADVEK ADZCM AERZD AFFZL AFGWE AFOFC AFXAL AFYAG AGQXC AGUTN AI. AJEEA ALXQX APJGH AQDSO BYORX CASEJ EMOBN FECEO FLUFQ FOEOM HZ~ IQODW KSI MJL N4W NOMLY OAUYM OBFPC OFXIZ OHH OPAEJ OVIDX P6G TEORI TR2 VVN W8F WHG YBU YFH YHG YOC YSK ~02 AARHZ ABJNI ABMNT ABNHQ ABQNK ABXVV ADQBN AGMDO AVNTJ CGR CUY CVF ECM EIF NPM OJZSN AAUAY AAYXX ATGXG CITATION 7X8 |
ID | FETCH-LOGICAL-c5187-7dc203e372f1fffd645cbfa9828bb636f3a4b65b8e1ea25eaecc564b059c24af3 |
ISSN | 0021-972X |
IngestDate | Fri Aug 16 12:16:43 EDT 2024 Thu Sep 12 19:35:08 EDT 2024 Thu May 23 23:08:34 EDT 2024 Sun Oct 22 16:05:27 EDT 2023 Thu Aug 13 19:45:24 EDT 2020 Tue Jan 05 21:44:35 EST 2021 |
IsDoiOpenAccess | false |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 1 |
Keywords | Endocrinopathy Human Physical exercise Menstruation disorders Pancreatic hormone Anovulation Energy metabolism Pathophysiology Somatotropin hormone Insulin like growth factor 1 Insulin Running locomotion Female genital diseases Blood plasma Insulin like growth factor binding protein Ovarian diseases Luteal phase Adenohypophyseal hormone Ovarian failure Leptin Young adult Female Thyroid hormone Hormonal investigation |
Language | English |
License | CC BY 4.0 |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c5187-7dc203e372f1fffd645cbfa9828bb636f3a4b65b8e1ea25eaecc564b059c24af3 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
OpenAccessLink | https://academic.oup.com/jcem/article-pdf/88/1/337/10743608/jcem0337.pdf |
PMID | 12519874 |
PQID | 72946444 |
PQPubID | 23479 |
PageCount | 10 |
ParticipantIDs | proquest_miscellaneous_72946444 crossref_primary_10_1210_jc_2002_020958 pubmed_primary_12519874 pascalfrancis_primary_14467709 wolterskluwer_health_00004678-200301000-00057 endocrinepress_journals_10_1210_jc_2002_020958 |
ProviderPackageCode | .XZ OBH C45 5RS AFCHL OGEVE ~H1 ABPMR M5~ OVD OCB |
PublicationCentury | 2000 |
PublicationDate | 2003-01 2003-January 2003 2003-Jan 2003-01-01 20030101 |
PublicationDateYYYYMMDD | 2003-01-01 |
PublicationDate_xml | – month: 01 year: 2003 text: 2003-01 |
PublicationDecade | 2000 |
PublicationPlace | Bethesda, MD |
PublicationPlace_xml | – name: Bethesda, MD – name: United States |
PublicationTitle | The journal of clinical endocrinology and metabolism |
PublicationTitleAlternate | J Clin Endocrinol Metab |
PublicationYear | 2003 |
Publisher | Endocrine Society Copyright by The Endocrine Society |
Publisher_xml | – name: Endocrine Society – name: Copyright by The Endocrine Society |
References | Beitins (2019041117010809500_R21) 1991; 72 Loucks (2019041117010809500_R9) 1998; 84 Schweiger (2019041117010809500_R30) 1987; 48 Williams (2019041117010809500_R42) 1995; 27 Karlsson (2019041117010809500_R50) 1997; 82 Pirke (2019041117010809500_R29) 1989; 51 Ellison (2019041117010809500_R36) 1993; 8 Myerson (2019041117010809500_R18) 1991; 23 Berga (2019041117010809500_R17); 68 Mentoer (2019041117010809500_R44) 1991; 128 Olson (2019041117010809500_R39) 1995; 80 Magni (2019041117010809500_R49) 1999; 140 Munro (2019041117010809500_R24) 1991; 37 De Souza (2019041117010809500_R34) 1991; 23 Moschos (2019041117010809500_R45) 2002; 77 Waters (2019041117010809500_R14) 2001; 86 Blackwell (2019041117010809500_R25) 1998; 63 Suikkari (2019041117010809500_R51) 1989; 68 Warren (2019041117010809500_R32) 1999; 84 Jenkins (2019041117010809500_R53) 1999; 50 Pirke (2019041117010809500_R31) 1985; 60 Winters (2019041117010809500_R23) 1996; 28 Loucks (2019041117010809500_R2) 1990; 22 DeCree (2019041117010809500_R52) 1998; 25 Jordan (2019041117010809500_R22) 1994; 62 Magini (2019041117010809500_R26) 1989; 4 Ellison (2019041117010809500_R38) 1986; 154 De Souza (2019041117010809500_R13) 1991; 70 Laughlin (2019041117010809500_R11) 1997; 82 Hilton (2019041117010809500_R15) 2000; 273 Laughlin (2019041117010809500_R10) 1996; 81 Loucks (2019041117010809500_R12) 1992; 75 Lebenstedt (2019041117010809500_R19) 1999; 31 De Souza (2019041117010809500_R3) 1998; 83 Wade (2019041117010809500_R20) 1992; 16 Williams (2019041117010809500_R5) 2001; 86 Stunkard (2019041117010809500_R40) 1985; 29 Wade (2019041117010809500_R46) 1996; 270 Williams (2019041117010809500_R6) 2001; 142 Loucks (2019041117010809500_R8) 1994 Leslie (2019041117010809500_R27) 1996; 68 Zhang (2019041117010809500_R48) 1994; 372 Ginsburg (2019041117010809500_R4) 1992 Williams (2019041117010809500_R43) 1996 Laughlin (2019041117010809500_R16) 1998; 83 Jackson (2019041117010809500_R28) 1980; 12 Bullen (2019041117010809500_R37) 1985; 312 Vigersky (2019041117010809500_R33) 1977; 297 Magni (2019041117010809500_R47) 2000; 92 2019041117010809500_R35 Larsen (2019041117010809500_R41) 1995; 15 Loucks (2019041117010809500_R7) 1993; 264 De Souza (2019041117010809500_R1) 1992; 3 |
References_xml | – volume: 3 start-page: 129 year: 1992 ident: 2019041117010809500_R1 article-title: Effects of exercise training on sex steroids: endocrine profile and clinical implications. publication-title: Infertil Reprod Med Clin North Am contributor: fullname: De Souza – volume: 16 start-page: 235 year: 1992 ident: 2019041117010809500_R20 article-title: Metabolic fuels and reproduction in female mammals. publication-title: Neurosci Biobehav Rev doi: 10.1016/S0149-7634(05)80183-6 contributor: fullname: Wade – volume: 83 start-page: 4220 year: 1998 ident: 2019041117010809500_R3 article-title: High frequency of LPD and anovulation in recreational women runners: blunted elevation in FSH observed during luteal-follicular transition. publication-title: J Clin Endocrinol Metab contributor: fullname: De Souza – volume: 23 start-page: 15 year: 1991 ident: 2019041117010809500_R18 article-title: Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. publication-title: Med Sci Sports Exerc doi: 10.1249/00005768-199101000-00004 contributor: fullname: Myerson – volume: 25 start-page: 369 year: 1998 ident: 2019041117010809500_R52 article-title: Sex steroid metabolism and menstrual irregularities in the exercising female. publication-title: Sports Med doi: 10.2165/00007256-199825060-00003 contributor: fullname: DeCree – volume: 68 start-page: 301 ident: 2019041117010809500_R17 publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem-68-2-301 contributor: fullname: Berga – volume: 27 start-page: 1390 year: 1995 ident: 2019041117010809500_R42 article-title: Strenuous exercise with caloric restriction: effect on luteinizing hormone secretion. publication-title: Med Sci Sports Exerc doi: 10.1249/00005768-199510000-00007 contributor: fullname: Williams – volume: 51 start-page: 263 year: 1989 ident: 2019041117010809500_R29 article-title: Dieting causes menstrual irregularities in normal weight young women through impairment of episodic luteinizing hormone secretion. publication-title: Fertil Steril doi: 10.1016/S0015-0282(16)60488-0 contributor: fullname: Pirke – volume: 48 start-page: 746 year: 1987 ident: 2019041117010809500_R30 article-title: Diet-induced menstrual irregularities: effects of age and weight loss. publication-title: Fertil Steril doi: 10.1016/S0015-0282(16)59523-5 contributor: fullname: Schweiger – volume: 23 start-page: 995 year: 1991 ident: 2019041117010809500_R34 article-title: Reproductive dysfunction in amenorrheic athletes and anorexic patients: a review. publication-title: Med Sci Sports Exerc doi: 10.1249/00005768-199109000-00002 contributor: fullname: De Souza – volume: 75 start-page: 514 year: 1992 ident: 2019041117010809500_R12 article-title: Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. publication-title: J Clin Endocrinol Metab contributor: fullname: Loucks – volume: 80 start-page: 1187 year: 1995 ident: 2019041117010809500_R39 article-title: Short-term fasting affects luteinizing hormone secretory dynamics but not reproductive function in normal-weight sedentary women. publication-title: J Clin Endocrinol Metab contributor: fullname: Olson – volume: 8 start-page: 2248 year: 1993 ident: 2019041117010809500_R36 article-title: The ecological context of human ovarian function. publication-title: Hum Reprod doi: 10.1093/oxfordjournals.humrep.a138015 contributor: fullname: Ellison – volume: 270 start-page: E1 year: 1996 ident: 2019041117010809500_R46 article-title: Control of fertility by metabolic cues publication-title: Am J Physiol contributor: fullname: Wade – volume: 83 start-page: 25 year: 1998 ident: 2019041117010809500_R16 article-title: Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. publication-title: J Clin Endocrinol Metab contributor: fullname: Laughlin – volume: 15 start-page: 323 year: 1995 ident: 2019041117010809500_R41 article-title: Nutritional and hormonal regulation of thyroid hormone deiodinases. publication-title: Annu Rev Nutr doi: 10.1146/annurev.nu.15.070195.001543 contributor: fullname: Larsen – ident: 2019041117010809500_R35 – volume: 12 start-page: 175 year: 1980 ident: 2019041117010809500_R28 article-title: Generalized equations for predicting body density in women. publication-title: Med Sci Sports Exerc doi: 10.1249/00005768-198023000-00009 contributor: fullname: Jackson – volume: 70 start-page: 2378 year: 1991 ident: 2019041117010809500_R13 article-title: Adrenal activation and the prolactin response to exercise in eumenorrheic and amenorrheic runners. publication-title: J Appl Physiol doi: 10.1152/jappl.1991.70.6.2378 contributor: fullname: De Souza – volume: 140 start-page: 1581 year: 1999 ident: 2019041117010809500_R49 article-title: Expression of a leptin receptor in immortalized gonadotropin-releasing hormone-secreting neurons. publication-title: Endocrinology doi: 10.1210/endo.140.4.6622 contributor: fullname: Magni – volume: 84 start-page: 873 year: 1999 ident: 2019041117010809500_R32 article-title: Functional hypothalamic amenorrhea: hypoleptinemia and disordered eating. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem.84.3.5551 contributor: fullname: Warren – volume: 154 start-page: 1000 year: 1986 ident: 2019041117010809500_R38 article-title: Moderate recreational running is associated with lowered salivary progesterone profiles in women. publication-title: Am J Obstet Gynecol doi: 10.1016/0002-9378(86)90737-4 contributor: fullname: Ellison – volume: 81 start-page: 4301 year: 1996 ident: 2019041117010809500_R10 article-title: Nutritional and endocrine metabolic aberrations in amenorrheic athletes. publication-title: J Clin Endocrinol Metab contributor: fullname: Laughlin – volume: 128 start-page: 1337 year: 1991 ident: 2019041117010809500_R44 article-title: Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. publication-title: Endocrinology doi: 10.1210/endo-128-3-1337 contributor: fullname: Mentoer – volume: 22 start-page: 275 year: 1990 ident: 2019041117010809500_R2 article-title: Effects of exercise training on the menstrual cycle: existence and mechanisms. publication-title: Med Sci Sports Exerc doi: 10.1249/00005768-199006000-00001 contributor: fullname: Loucks – volume: 297 start-page: 1141 year: 1977 ident: 2019041117010809500_R33 article-title: Hypothalamic dysfunction in secondary amenorrhea associated with simple weight loss. publication-title: N Engl J Med doi: 10.1056/NEJM197711242972103 contributor: fullname: Vigersky – volume: 372 start-page: 425 year: 1994 ident: 2019041117010809500_R48 article-title: Positional cloning of the mouse obese gene and its human homologue. publication-title: Nature doi: 10.1038/372425a0 contributor: fullname: Zhang – volume: 77 start-page: 433 year: 2002 ident: 2019041117010809500_R45 article-title: Leptin and reproduction: a review. publication-title: Fertil Steril doi: 10.1016/S0015-0282(01)03010-2 contributor: fullname: Moschos – volume: 63 start-page: 5 year: 1998 ident: 2019041117010809500_R25 article-title: Definition of the potentially fertile period from urinary steroid excretion rates. Part II. A threshold value for pregnanediol glucuronide as a marker for the end of the potentially fertile period in the human menstrual cycle. publication-title: Steroids doi: 10.1016/S0039-128X(97)00117-7 contributor: fullname: Blackwell – volume: 82 start-page: 4144 year: 1997 ident: 2019041117010809500_R50 article-title: Expression of functional leptin receptors in the human ovary. publication-title: J Clin Endocrinol Metab contributor: fullname: Karlsson – start-page: 531 volume-title: Proc of the 10th International Congress of Endocrinology year: 1996 ident: 2019041117010809500_R43 article-title: Stimulation of luteinizing hormone (LH) secretion in male rhesus monkeys by food intake: role of circulating triiodothyronine (T3) contributor: fullname: Williams – volume: 68 start-page: 95 year: 1996 ident: 2019041117010809500_R27 article-title: Evaluation of reproductive function in Turkana women with enzyme immunoassays of urinary hormones in the field. publication-title: Hum Biol contributor: fullname: Leslie – volume: 60 start-page: 1174 year: 1985 ident: 2019041117010809500_R31 article-title: The influence of dieting on the menstrual cycle of healthy young women. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem-60-6-1174 contributor: fullname: Pirke – volume: 82 start-page: 318 year: 1997 ident: 2019041117010809500_R11 article-title: Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem.82.1.3840 contributor: fullname: Laughlin – volume: 86 start-page: 5184 year: 2001 ident: 2019041117010809500_R5 article-title: Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem.86.11.8024 contributor: fullname: Williams – volume: 142 start-page: 2381 year: 2001 ident: 2019041117010809500_R6 article-title: Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea. publication-title: Endocrinology doi: 10.1210/endo.142.6.8113 contributor: fullname: Williams – volume: 29 start-page: 71 year: 1985 ident: 2019041117010809500_R40 article-title: The three-factor eating questionnaire to measure dietary restraint disinhibition and hunger. publication-title: J Psychosom Res doi: 10.1016/0022-3999(85)90010-8 contributor: fullname: Stunkard – volume: 62 start-page: 54 year: 1994 ident: 2019041117010809500_R22 article-title: Luteal phase defect: the sensitivity and specificity of diagnostic methods in common clinical use. publication-title: Fertil Steril doi: 10.1016/S0015-0282(16)56815-0 contributor: fullname: Jordan – volume: 37 start-page: 838 year: 1991 ident: 2019041117010809500_R24 article-title: Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured enzyme immunoassay and radioimmunoassay. publication-title: Clin Chem doi: 10.1093/clinchem/37.6.838 contributor: fullname: Munro – volume: 68 start-page: 135 year: 1989 ident: 2019041117010809500_R51 article-title: Dose-response characteristics for suppression of low molecular weight plasma insulin-like growth factor-binding protein by insulin. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem-68-1-135 contributor: fullname: Suikkari – volume: 264 start-page: R924 year: 1993 ident: 2019041117010809500_R7 article-title: Induction and prevention of low-T3 syndrome in exercising women publication-title: Am J Physiol contributor: fullname: Loucks – volume: 84 start-page: 37 year: 1998 ident: 2019041117010809500_R9 article-title: Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. publication-title: J Appl Physiol doi: 10.1152/jappl.1998.84.1.37 contributor: fullname: Loucks – volume: 4 start-page: 567 year: 1989 ident: 2019041117010809500_R26 article-title: Measurement of estrone-3-glucuronide and pregnanediol-3 α-glucuronide in early morning urine samples to monitor ovarian function. publication-title: J Biolumin Chemilumin doi: 10.1002/bio.1170040174 contributor: fullname: Magini – volume: 312 start-page: 1349 year: 1985 ident: 2019041117010809500_R37 article-title: Induction of menstrual disorders by strenuous exercise in untrained women. publication-title: N Engl J Med doi: 10.1056/NEJM198505233122103 contributor: fullname: Bullen – volume: 92 start-page: 51 year: 2000 ident: 2019041117010809500_R47 article-title: Leptin: a possible link between food intake, energy expenditure and reproductive function. publication-title: Regul Pept doi: 10.1016/S0167-0115(00)00149-X contributor: fullname: Magni – volume: 273 start-page: E43 year: 2000 ident: 2019041117010809500_R15 article-title: Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women publication-title: Am J Physiol Endocrinol Metab doi: 10.1152/ajpendo.2000.278.1.E43 contributor: fullname: Hilton – volume: 72 start-page: 1350 year: 1991 ident: 2019041117010809500_R21 article-title: Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone. publication-title: J Clin Endocrinol Metab doi: 10.1210/jcem-72-6-1350 contributor: fullname: Beitins – volume: 28 start-page: 776 year: 1996 ident: 2019041117010809500_R23 article-title: Bone density and cyclic ovarian function in trained runners and active controls. publication-title: Med Sci Sport Exerc doi: 10.1097/00005768-199607000-00002 contributor: fullname: Winters – volume: 50 start-page: 683 year: 1999 ident: 2019041117010809500_R53 article-title: Growth hormone and exercise publication-title: Clin Endocrinol (Oxf) doi: 10.1046/j.1365-2265.1999.00784.x contributor: fullname: Jenkins – volume: 31 start-page: 1250 year: 1999 ident: 2019041117010809500_R19 article-title: Reduced resting metabolic rate in athletes with menstrual disturbances. publication-title: Med Sci Sports Exerc doi: 10.1097/00005768-199909000-00004 contributor: fullname: Lebenstedt – volume: 86 start-page: 1013 year: 2001 ident: 2019041117010809500_R14 article-title: Increased pulsatility, process regularity and nocturnal through concentrations of growth hormone in amenorrheic compared to eumenorrheic athletes. publication-title: J Clin Endocrinol Metab contributor: fullname: Waters – start-page: 85 year: 1992 ident: 2019041117010809500_R4 article-title: Luteal phase defect: etiology diagnosis and management publication-title: In: Moghissi KS, ed. Endocrinology and metabolism clinics of North America. Philadelphia: WB Saunders Co; doi: 10.1016/S0889-8529(18)30233-0 contributor: fullname: Ginsburg – start-page: R817 year: 1994 ident: 2019041117010809500_R8 article-title: Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability publication-title: Am J Physiol contributor: fullname: Loucks |
SSID | ssj0014453 |
Score | 2.0540378 |
Snippet | Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD)... |
SourceID | proquest crossref pubmed pascalfrancis wolterskluwer endocrinepress |
SourceType | Aggregation Database Index Database Publisher |
StartPage | 337 |
SubjectTerms | Adult Biological and medical sciences Biomarkers Energy Metabolism - physiology Estrogens - biosynthesis Female Female genital diseases Fundamental and applied biological sciences. Psychology Gynecology. Andrology. Obstetrics Humans Insulin - blood Leptin - blood Luteal Phase - physiology Medical sciences Menstrual Cycle - physiology Metabolic Diseases - physiopathology Non tumoral diseases Physical Education and Training Progesterone - urine Recreation Running - physiology Thyroid Hormones - blood Vertebrates: body movement. Posture. Locomotion. Flight. Swimming. Physical exercise. Rest. Sports |
Title | Luteal Phase Deficiency in Recreational Runners: Evidence for a Hypometabolic State |
URI | http://dx.doi.org/10.1210/jc.2002-020958 http://ovidsp.ovid.com/ovidweb.cgi?T=JS&NEWS=n&CSC=Y&PAGE=fulltext&D=ovft&AN=00004678-200301000-00057 https://www.ncbi.nlm.nih.gov/pubmed/12519874 https://search.proquest.com/docview/72946444 |
Volume | 88 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Jb9NAFB5FRUIcQOwNS5kDEofIlT2LF24RCgqlKRJJUMXF8tgzaqA4EUmEyo_iN_Jmi21axHKxIjt2nHmf3zJ-3zcIPa9oyioieFAIqgKWZmlQkIgGcSFlmJGo4qnmDk9O4vGcHZ3y017vR6trabsRh-X3K3kl_2NV2Ad21SzZf7Ds7qKwAz6DfWELFobtX9n4eLvRusCrMwhFg0pqMQjDpDQcFZ8OauX-rV5gyzS_-VVEbffk4OxitfwiN4AELXZt2EXtdFWDqKUtsaNRyrpagrupGwEnfxEnSKhT49Fg-m7-cegYQReDo6J5hf9heDIYj0bTme3ULRfNWZPR-6lnbFu3448dD6eQThtELs7PHV_Cz1jQZgLN3Zz0Laltz6xbRRKztDrEJeuMM8aDJLL9u95bp-klVFrXS614jIvi1E5sXgoQUOHqAGHEK0kAuXJmleO7Sty_RMhd36IunpNE80WvkQQqS52Ev3m7e2vFmFM9df_FiYRqllT3FztJ0E1vM9v6rLtzizXYUtmVVa4qfeA735a6m2L92ZApWinR7Da65WoZPLTAvIN6sr6Lrk9ct8Y9NLX4xAafuMEnXtS4jU_s8PkSe3RiQCcucAed2KDzPpq_Hs1ejQO3iEdQ8ggCWFKVJKSSJkRFSqkqZrwUqsig0hciprGiBRMxF6mMZEG4LMCn8JgJSPtLwgpFH6C9elnLfYR5SEQoikwkcclSRVOZlVSmsQpVRTgJ--iFH9V8ZbVacl3jwvjnn0q94CrJ7fj30WF30HP3LK1_e8JBxyjN9R0i-uiZt1IODlq_dYOHarld51C9Mig6WB89tMZrztWs8TSBI0HHmrmlQOemfodkUvs8iMNOA4Inj_50M4_RDdNzamYKn6C9zdetfAq580YcGMD-BNNHxAY |
link.rule.ids | 315,786,790,4043,27956,27957,27958 |
linkProvider | Flying Publisher |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Luteal+phase+deficiency+in+recreational+runners%3A+Evidence+for+a+hypometabolic+state&rft.jtitle=The+journal+of+clinical+endocrinology+and+metabolism&rft.au=DE+SOUZA%2C+Mary+Jane&rft.au=VAN+HEEST%2C+Jaci&rft.au=DEMERS%2C+Laurence+M&rft.au=LASLEY%2C+Bill+L&rft.date=2003&rft.pub=Endocrine+Society&rft.issn=0021-972X&rft.eissn=1945-7197&rft.volume=88&rft.issue=1&rft.spage=337&rft.epage=346&rft_id=info:doi/10.1210%2Fjc.2002-020958&rft.externalDBID=n%2Fa&rft.externalDocID=14467709 |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0021-972X&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0021-972X&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0021-972X&client=summon |