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Cited by 42Sports Performance and TrainingRegulation of Appetite and ObesityHypothalamic control of reproductive hormones

Decreased energy availability during training overload is associated with non-functional overreaching and suppressed ovarian function in female runners

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Schaal, Karine, VanLoan, Marta D., Hausswirth, Christophe, Casazza, Gretchen A.·2021·Applied Physiology, Nutrition, and Metabolism
DOI 10.1139/apnm-2020-0880
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Abstract

Low energy availability (EA) suppresses many physiological processes, including ovarian function in female athletes. Low EA could also predispose athletes to develop a state of overreaching. This study compared the changes in ad libitum energy intake (EI), exercise energy expenditure (ExEE), and EA among runners completing a training overload (TO) phase. We tested the hypothesis that runners becoming overreached would show decreased EA, suppressed ovarian function and plasma leptin, compared with well-adapted (WA) runners. After 1 menstrual cycle (baseline), 16 eumenorrheic runners performed 4 weeks of TO followed by a 2-week recovery (131 ± 3% and 63 ± 6% of baseline running volume, respectively). Seven-day ExEE, EI, running performance (RUN perf) and plasma leptin concentration were assessed for each phase. Salivary estradiol concentration was measured daily. Urinary luteinizing hormone concentration tests confirmed ovulation. Nine runners adapted positively to TO (WA, ΔRUN perf: +4 ± 2%); 7 were non-functionally overreached (NFOR; ΔRUN perf: −9 ± 2%) as RUN perf remained suppressed after the recovery period. WA increased EI during TO, maintaining their baseline EA despite a large increase in ExEE (ΔEA = +1.9 ± 1.3 kcal·kg fat free mass (FFM)−1·d−1, P = 0.17). By contrast, NFOR showed no change in EI, leading to decreased EA (ΔEA = −5.6 ± 2.1 kcal·kg FFM−1·d−1, P = 0.04). Plasma leptin concentration mid-cycle and luteal salivary estradiol concentration decreased in NFOR only. Contrasting with WA, NFOR failed to maintain baseline EA during TO, resulting in poor performance outcomes and suppressed ovarian function. ClinicalTrials.gov no. NCT02224976. Novelty: Runners adapting positively to training overload (TO) increased ad libitum energy intake, maintaining baseline EA and ovarian function through TO. By contrast, NFOR runners failed to increase energy intake, showing suppressed EA and ovarian function during TO.

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  • Regression analysis showed that change in run performance was directly correlated to change in energy intake (R = 0.61, p = 0.017).

    “Regression analysis showed that change in run performance was directly correlated to change in energy intake (Correlation coefficient (R) = 0.61, p = 0.017), suggesting that runners who increased their energy intake sufficiently saw performance improvements, whereas those who did not fuel properly saw declining run performance [78].”

    From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [78]

    The Energy Variables section reports a direct correlation between change in running performance and change in energy intake, but gives it as R = 0.59, P = 0.021. The cited R = 0.61, P = 0.017 instead belongs to the correlation with energy availability. No page number is provided in our copy. (LLM, conf=0.94)

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  • Schaal et al. found female runners who did not adequately increase energy intake commensurate with an increase in training load (up to 130% of baseline) over 4 weeks had decreased run performance of ≥1.8% below baseline at the end of 4 weeks and after a 2-week recovery period.

    “Schaal et al. found that female runners who did not adequately increase their energy intake commensurate with an increase in training load (up to 130% of baseline training volume) over a 4-week period had decreased run performance of ≥ 1.8% below baseline both at the end of the 4 weeks and following a subsequent 2-week recovery period (down to 50% of baseline training volume).”

    From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [78]

  • Psychological indicators associated with problematic LEA and REDs are mood disturbances/fluctuations, cognitive dietary restraint, drive for thinness, reduced sleep quality and perfectionistic tendencies.

    “Psychological indicators associated with problematic LEA and REDs are mood disturbances/fluctuations, 8 71 72 cognitive dietary restraint, 73 drive for thinness, 74 75 reduced sleep quality 50 76 and perfectionistic tendencies.77”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [71]

    The Results report increased perceived fatigue in non-functionally overreached runners, and the Discussion reports no baseline difference in restrictive eating attitudes. Our copy does not report reduced sleep quality or establish the listed psychological indicators as markers of problematic low energy availability or REDs; searches for sleep quality and mood found no supporting passage. (LLM, conf=0.75)

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Research works printed but not linked: 34

  1. Achten, J., Halson, S.L., Moseley, L., Rayson, M.P., Casey, A., and Jeukendrup, A.E. 2004. Higher dietary carbohydrate content during intensified running training results in better maintenance of performance and mood state. J. Appl. Physiol. Bethesda Md 1985 96(4): 1331-1340. doi:10.1152/japplphysiol.00973.2003. · DOI · Paper page
  2. Ackerman, K.E., Nazem, T., Chapko, D., Russell, M., Mendes, N., Taylor, A.P., Bouxsein, M.L., and Misra, M. 2011. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J. Clin. Endocrinol. Metab. 96(10): 3123-3133. doi:10.1210/jc.2011-1614. · DOI
  3. Aubry, A., Hausswirth, C., Louis, J., Coutts, A.J., and Le Meur, Y. 2014. Functional Overreaching: The Key to Peak Performance during the Taper? Med. Sci. Sports Exerc. 46(9): 1769-77.
  4. Bellem, A., Meiyappan, S., Romans, S., and Einstein, G. 2011. Measuring Estrogens and Progestagens in Humans: An Overview of Methods. Gend. Med. doi:10.1016/j.genm.2011.07.001. · DOI
  5. Bellinger, P., Desbrow, B., Derave, W., Lievens, E., Irwin, C., Sabapathy, S., Kennedy, B., Craven, J., Pennell, E., Rice, H., and Minahan, C. 2020. Muscle fiber typology is associated with the incidence of overreaching in response to overload training. J. Appl. Physiol. Bethesda Md 1985 129(4): 823-836. doi:10.1152/japplphysiol.00314.2020. · DOI
  6. Blundell, J.E., Gibbons, C., Caudwell, P., Finlayson, G., and Hopkins, M. 2015. Appetite control and energy balance: impact of exercise. Obes. Rev. Off. J. Int. Assoc. Study Obes. 16 Suppl 1: 67-76. doi:10.1111/obr.12257. · DOI · Paper page
  7. Borg, G. 1970. Perceived exertion as an indicator of somatic stress. Scand. J. Rehabil. Med. 2(2): 92-98.
  8. Bosquet, L., Montpetit, J., Arvisais, D., and Mujika, I. 2007. Effects of tapering on performance: a meta-analysis. Med. Sci. Sports Exerc. 39(8): 1358-1365. doi:10.1249/mss.0b013e31806010e0. · DOI
  9. Brage, S., Ekelund, U., Brage, N., Hennings, M.A., Froberg, K., Franks, P.W., and Wareham, N.J. 2007. Hierarchy of individual calibration levels for heart rate and accelerometry to measure physical activity. J. Appl. Physiol. 103(2): 682-692. doi:10.1152/japplphysiol.00092.2006. · DOI · Paper page
  10. Burke, L.M., Hawley, J.A., Wong, S.H.S., and Jeukendrup, A.E. 2011. Carbohydrates for training and competition. J. Sports Sci. 29 Suppl 1: S17-27. doi:10.1080/02640414.2011.585473. · DOI · Paper page
  11. Capling, L., Beck, K.L., Gifford, J.A., Slater, G., Flood, V.M., and O'Connor, H. 2017. Validity of Dietary Assessment in Athletes: A Systematic Review. Nutrients 9(12). doi:10.3390/nu9121313. · DOI
  12. Crouter, S.E., Churilla, J.R., and Bassett, D.R., Jr. 2008. Accuracy of the Actiheart for the assessment of energy expenditure in adults. Eur. J. Clin. Nutr. 62(6): 704-711. doi:10.1038/sj.ejcn.1602766. · DOI · Paper page
  13. Darcy, A.M., Hardy, K.K., Lock, J., Hill, K.B., and Peebles, R. 2013. The Eating Disorder Examination Questionnaire (EDE-Q) among university men and women at different levels of athleticism. Eat. Behav. 14(3): 378-381. doi:10.1016/j.eatbeh.2013.04.002. · DOI
  14. De Souza, M.J., Luciano, A.A., Arce, J.C., Demers, L.M., and Loucks, A.B. 1994. Clinical tests explain blunted cortisol responsiveness but not mild hypercortisolism in amenorrheic runners. J. Appl. Physiol. Bethesda Md 1985 76(3): 1302-9.
  15. Deem, J.D., Muta, K., Ogimoto, K., Nelson, J.T., Velasco, K.R., Kaiyala, K.J., and Morton, G.J. 2018. Leptin regulation of core body temperature involves mechanisms independent of the thyroid axis. Am. J. Physiol.-Endocrinol. Metab. 315(4): E552-E564. American Physiological Society. doi:10.1152/ajpendo.00462.2017. · DOI
  16. Drenowatz, C., Eisenmann, J.C., Carlson, J.J., Pfeiffer, K.A., and Pivarnik, J.M. 2012. Energy expenditure and dietary intake during high-volume and low-volume training periods among male endurance athletes. Appl. Physiol. Nutr. Metab. Physiol. Appliquée Nutr. Métabolisme 37(2): 199-205. doi:10.1139/h11-155. · DOI · Paper page
  17. Fairburn, C.G., and Beglin, S.J. 1994. Assessment of eating disorders: interview or self-report questionnaire? Int. J. Eat. Disord. 16(4): 363-70.
  18. Flint, A., Raben, A., Blundell, J.E., and Astrup, A. 2000. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int. J. Obes. Relat. Metab. Disord. J. Int. Assoc. Study Obes. 24(1): 38-48.
  19. Foster, C., Florhaug, J.A., Franklin, J., Gottschall, L., Hrovatin, L.A., Parker, S., Doleshal, P., and Dodge, C. 2001. A new approach to monitoring exercise training. J. Strength Cond. Res. Natl. Strength Cond. Assoc. 15(1): 109-115.
  20. Hilton, L.K., and Loucks, A.B. 2000. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am. J. Physiol. -Endocrinol. Metab. 278(1): E43-E49.
  21. Jürimäe, J., Mäestu, J., Jürimäe, T., Mangus, B., and von Duvillard, S.P. 2011. Peripheral signals of energy homeostasis as possible markers of training stress in athletes: a review. Metabolism 60(3): 335-350. doi:10.1016/j.metabol.2010.02.009. · DOI
  22. Karklin, A., Driver, H.S., and Buffenstein, R. 1994. Restricted energy intake affects nocturnal body temperature and sleep patterns. Am. J. Clin. Nutr. 59(2): 346-349.
  23. Laughlin, G.A., and Yen, S.S. 1996. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J. Clin. Endocrinol. Metab. 81(12): 4301-9.
  24. LeMeur, Y., Hausswirth, C., Natta, F., Couturier, A., Bignet, F., and Vidal, P.-P. 2013. A multidisciplinary approach to overreaching deterction in endurance-trained athletes. J. Appl. Physiol. 114(3): 411-20.
  25. Livingstone, M.B.E., and Black, A.E. 2003. Markers of the Validity of Reported Energy Intake. J. Nutr. 133(3): 895S-920S.
  26. Loucks, A.B., Laughlin, G.A., Mortola, J.F., Girton, L., Nelson, J.C., and Yen, S.S. 1992. Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. J. Clin. Endocrinol. Metab. 75(2): 514-8.
  27. Loucks, A.B., and Thuma, J.R. 2003. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J. Clin. Endocrinol. Metab. 88(1): 297-311.
  28. Molé, P.A. 1990. Impact of energy intake and exercise on resting metabolic rate. Sports Med. Auckl. NZ 10(2): 72-87.
  29. Mueller, W.M., Gregoire, F.M., Stanhope, K.L., Mobbs, C.V., Mizuno, T.M., Warden, C.H., Stern, J.S., and Havel, P.J. 1998. Evidence that glucose metabolism regulates leptin secretion from cultured rat adipocytes. Endocrinology 139(2): 551-558. doi:10.1210/endo.139.2.5716. · DOI
  30. Nana, A., Slater, G.J., Hopkins, W.G., Halson, S.L., Martin, D.T., West, N.P., and Burke, L.M. 2014. Importance of Standardized DXA Protocol for Assessing Physique Changes in Athletes. Int. J. Sport Nutr. Exerc. Metab. doi:10.1123/ijsnem.2013-0111. · DOI
  31. Roffey, D.M., Byrne, N.M., and Hills, A.P. 2006. Day-to-Day Variance in Measurement of Resting Metabolic Rate Using Ventilated-Hood and Mouthpiece & Nose-Clip Indirect Calorimetry Systems. J. Parenter. Enter. Nutr. 30(5): 426-432. doi:https://doi.org/10.1177/0148607106030005426. · DOI
  32. Schaal, K., Tiollier, E., Le Meur, Y., Casazza, G., and Hausswirth, C. 2016. Elite synchronized swimmers display decreased energy availability during intensified training. Scand. J. Med. Sci. Sports: n/a-n/a. doi:10.1111/sms.12716. · DOI
  33. Schwartz, M.W., Woods, S.C., Porte, D., Seeley, R.J., and Baskin, D.G. 2000. Central nervous system control of food intake. Nature 404(6778): 661-671. doi:10.1038/35007534. · DOI · Paper page
  34. Uusitalo, A.L., Huttunen, P., Hanin, Y., Uusitalo, A.J., and Rusko, H.K. 1998. Hormonal responses to endurance training and overtraining in female athletes. Clin. J. Sport Med. Off. J. Can. Acad. Sport Med. 8(3): 178-186.

Cited by

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Authors
Schaal, K., VanLoan, M. D., Hausswirth, C., & Casazza, G. A.
Affiliations
  • University of California, Davis (US)
  • Nutrition Department, University of California, Davis, CA, USA.
  • Université Côte d'Azur (FR)
  • California State University, Sacramento (US)
ORCID
Venue
Applied Physiology, Nutrition, and Metabolism
Publisher
Canadian Science Publishing
Published
2021-10
Volume
46
Issue
10
Pages
1179-1188
ISSN
  • 1715-5312 (ISSN-L)
  • 1715-5320
DOI
10.1139/apnm-2020-0880
OpenAlex
W3134320127
Cited by
42
References
6
Citations by year
2026: 8 · 2025: 9 · 2024: 9 · 2023: 9 · 2022: 4 · 2021: 3
FWCI
6.14
Type
journal article
Language
en
Open access
Licence
www.nrcresearchpress.com/page/about/CorporateTextAndDataMining (tdm)
Locations
  • Applied Physiology, Nutrition, and Metabolism (publishedVersion)
  • PubMed (publishedVersion)
  • TSpace (University of Toronto) (submittedVersion)
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
energy availability, training overload, female runners, non-functional overreaching, ovarian function, energy intake, exercise energy expenditure, leptin, estradiol, luteinizing hormone, menstrual cycle, running performance, female athletes
MeSH terms
Adult, Energy Intake, Dysmenorrhea, Energy Metabolism, Estradiol, Fatigue, Female, Humans, Menstrual Cycle, Ovary, Physical Endurance, Running, Exercise, Workload, Leptin, Young Adult

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