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      Energy availability discriminates clinical menstrual status in exercising women

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          Abstract

          Background

          Conditions of low energy availability (EA) (<30 kcal/kgLBM) have been associated with suppressed metabolic hormones and reductions in LH pulsatility in previously sedentary women during short-term manipulations of energy intake (EI) and exercise energy expenditure (EEE) in a controlled laboratory setting. The purpose of this study was to examine if EA, defined as EA = (EI-EEE)/kgLBM, is associated with disruptions in ovarian function in exercising women.

          Methods

          Menstrual status was confirmed with daily measures of urinary reproductive metabolites across 1–3 menstrual cycles or 28-day monitoring periods. EA was calculated for exercise days using EI from 3-day diet logs, EEE from heart-rate monitors and/or exercise logs for a 7-day period, and body composition from DXA. Resting energy expenditure (REE) was measured by indirect calorimetry. Total triiodothyronine (TT 3) was measured from a fasting blood sample.

          Results

          91 exercising women (23.1 ± 0.5 years) were categorized clinically as either exercising amenorrheic (ExAmen, n = 30), exercising oligomenorrheic (ExOligo, n = 20) or exercising eumenorrheic (ExEumen, n = 41). The eumenorrheic group was further divided into more specific subclinical groups as either exercising ovulatory (ExOv, n = 20), exercising inconsistent (ExIncon, n = 13), or exercising anovulatory (ExAnov, n = 8). An EA threshold of 30 kcal/kgLBM did not distinguish subclinical menstrual status ( χ 2 = 0.557, p = 0.46) nor did EA differ across subclinical disturbance groups (p > 0.05). EA was lower in the ExAmen vs. ExEumen (30.9 ± 2.4 vs. 36.9 ± 1.7 kcal/kgLBM, p = 0.04). The ratio of REE/predicted REE was lower in the ExAmen vs. ExEumen (0.85 ± 0.02 vs. 0.92 ± 0.01, p = 0.001) as was TT 3 (79.6 ± 4.1 vs. 95.3 ± 2.9 ng/mL, p = 0.002).

          Conclusions

          EA did not differ among subclinical forms of menstrual disturbances in a large sample of exercising women, but EA did discriminate clinical menstrual status, i.e., amenorrhea from eumenorrhea.

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          Most cited references34

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          Compendium of physical activities: an update of activity codes and MET intensities.

          We provide an updated version of the Compendium of Physical Activities, a coding scheme that classifies specific physical activity (PA) by rate of energy expenditure. It was developed to enhance the comparability of results across studies using self-reports of PA. The Compendium coding scheme links a five-digit code that describes physical activities by major headings (e.g., occupation, transportation, etc.) and specific activities within each major heading with its intensity, defined as the ratio of work metabolic rate to a standard resting metabolic rate (MET). Energy expenditure in MET-minutes, MET-hours, kcal, or kcal per kilogram body weight can be estimated for specific activities by type or MET intensity. Additions to the Compendium were obtained from studies describing daily PA patterns of adults and studies measuring the energy cost of specific physical activities in field settings. The updated version includes two new major headings of volunteer and religious activities, extends the number of specific activities from 477 to 605, and provides updated MET intensity levels for selected activities.
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            Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women.

            To investigate the dependence of LH pulsatility on energy availability (dietary energy intake minus exercise energy expenditure), we measured LH pulsatility after manipulating the energy availability of 29 regularly menstruating, habitually sedentary, young women of normal body composition for 5 d in the early follicular phase. Subjects expended 15 kcal/kg of lean body mass (LBM) per day in supervised exercise at 70% of aerobic capacity while consuming a clinical dietary product to set energy availability at 45 and either 10, 20, or 30 kcal/kg LBM.d in two randomized trials separated by at least 2 months. Blood was sampled daily during treatments and at 10-min intervals for the next 24 h. Samples were assayed for LH, FSH, estradiol (E2), glucose, beta-hydroxybutyrate, insulin, cortisol, GH, IGF-I, IGF-I binding protein (IGFBP)-1, IGFBP-3, leptin, and T3. LH pulsatility was unaffected by an energy availability of 30 kcal/kg LBM.d (P > 0.3), but below this threshold LH pulse frequency decreased, whereas LH pulse amplitude increased (all P < 0.04). This disruption was more extreme in women with short luteal phases (P < 0.01). These incremental effects most closely resembled the effects of energy availability on plasma glucose, beta-hydroxybutyrate, GH, and cortisol and contrasted with the dependencies displayed by the other metabolic hormones (simultaneously P < 0.05). These results demonstrate that LH pulsatility is disrupted only below a threshold of energy availability deep into negative energy balance and suggest priorities for future investigations into the mechanism that mediates the nonlinear dependence of LH pulsatility on energy availability.
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              Dose-response relationships between energy availability and bone turnover in young exercising women.

              To help refine nutritional guidelines for military servicewomen, we assessed bone turnover after manipulating the energy availability of 29 young women. Bone formation was impaired by less severe restrictions than that which increased bone resorption. Military servicewomen and others may need to improve their nutrition to avoid these effects. We determined the dose-response relationship between energy availability (defined as dietary energy intake minus exercise energy expenditure) and selected markers of bone turnover in 29 regularly menstruating, habitually sedentary, young women of normal body composition. For 5 days in the early follicular phase of two menstrual cycles separated by at least 2 months, subjects expended 15 kcal/kgLBM/day in supervised exercise at 70% of aerobic capacity and consumed controlled amounts of a clinical dietary product in balanced (45 kcal/kgLBM/day) and one of three restricted (either 10, 20, or 30 kcal/kgLBM/day) energy availability treatments in random order. Blood was sampled at 10-minute intervals, and urine was collected for 24 h. Samples were assayed for plasma osteocalcin (OC), serum type I procollagen carboxy-terminal propeptide (PICP), and urinary N-telopeptide (NTX). NTX concentrations (p < 0.01) and indices of bone resorption/formation uncoupling (Z(NTX-OC) and Z(NTX-PICP); both p < 10(-4)) were increased by the 10 kcal/kgLBM/day treatment. OC and PICP concentrations were suppressed by all restricted energy availability treatments (all p < 0.05). PICP declined linearly (p < 10(-6)) with energy availability, whereas most of the suppression of OC occurred abruptly between 20 and 30 kcal/kgLBM/day (p < 0.05). These dose-response relationships closely resembled those of particular reproductive and metabolic hormones found in the same experiment and reported previously: similar relationships were observed for NTX and estradiol; for PICP and insulin; and for OC, triiodothyronine (T3), and insulin-like growth factor (IGF)-I. The uncoupling of bone resorption and formation by severely restricted energy availability, if left to continue, may lead to irreversible reductions in BMD, and the suppression of bone formation by less severe restrictions may prevent young women from achieving their genetic potential for peak bone mass. More prolonged experiments are needed to determine the dose-response relationships between chronic restrictions of energy availability and bone turnover.
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                Author and article information

                Contributors
                jreed@ottawaheart.ca
                mjd34@psu.edu
                rjt199@psu.edu
                jlscheid@buffalo.edu
                niw1@psu.edu
                Journal
                J Int Soc Sports Nutr
                J Int Soc Sports Nutr
                Journal of the International Society of Sports Nutrition
                BioMed Central (London )
                1550-2783
                19 February 2015
                19 February 2015
                2015
                : 12
                : 11
                Affiliations
                [ ]Department of Kinesiology, Women’s Health and Exercise Laboratory, 108 Noll Laboratory, The Pennsylvania State University, University Park, PA 16802 USA
                [ ]Current address: Division of Prevention and Rehabilitation, University of Ottawa Heart Institute, 40 Ruskin Street, Ottawa, ON K1Y 4W7 Canada
                [ ]Current address: Department of Pediatrics, School of Medicine and Biomedical Sciences, University at Buffalo, Buffalo, NY USA
                Article
                72
                10.1186/s12970-015-0072-0
                4342163
                25722661
                eeb4bd83-7484-4c62-8229-636ff441f29a
                © Reed et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 16 September 2014
                : 3 February 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Sports medicine
                energy balance,females,exercise training,dietary energy intake,resting metabolic rate,total triiodothyronine

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