Fuel for the work required: A practical approach to amalgamating train-low paradigms for endurance athletes
Open accessAbstract
Using an amalgamation of previously studied "train-low" paradigms, we tested the effects of reduced carbohydrate (CHO) but high leucine availability on cell-signaling responses associated with exercise-induced regulation of mitochondrial biogenesis and muscle protein synthesis (MPS). In a repeated-measures crossover design, 11 males completed an exhaustive cycling protocol with high CHO availability before, during, and after exercise (HIGH) or alternatively, low CHO but high protein (leucine enriched) availability (LOW + LEU). Muscle glycogen was different (P < 0.05) pre-exercise (HIGH: 583 ± 158, LOW + LEU: 271 ± 85 mmol kg(-1) dw) but decreased (P < 0.05) to comparable levels at exhaustion (≈100 mmol kg(-1) dw). Despite differences (P < 0.05) in exercise capacity (HIGH: 158 ± 29, LOW + LEU: 100 ± 17 min), exercise induced (P < 0.05) comparable AMPKα2 (3-4-fold) activity, PGC-1α (13-fold), p53 (2-fold), Tfam (1.5-fold), SIRT1 (1.5-fold), Atrogin 1 (2-fold), and MuRF1 (5-fold) gene expression at 3 h post-exercise. Exhaustive exercise suppressed p70S6K activity to comparable levels immediately post-exercise (≈20 fmol min(-1) mg(-1)). Despite elevated leucine availability post-exercise, p70S6K activity remained suppressed (P < 0.05) 3 h post-exercise in LOW + LEU (28 ± 14 fmol min(-1) mg(-1)), whereas muscle glycogen resynthesis (40 mmol kg(-1) dw h(-1)) was associated with elevated (P < 0.05) p70S6K activity in HIGH (53 ± 30 fmol min(-1) mg(-1)). We conclude: (1) CHO restriction before and during exercise induces "work-efficient" mitochondrial-related cell signaling but; (2) post-exercise CHO and energy restriction maintains p70S6K activity at basal levels despite feeding leucine-enriched protein. Our data support the practical concept of "fuelling for the work required" as a potential strategy for which to amalgamate train-low paradigms into periodized training programs.
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Keeping glycogen (and energy) at critically low post-exercise levels (< 100 mmol/kg dw) may reduce the regulation of protein synthesis pathways.
“and keeping glycogen (and energy) at critically low post-exercise levels (i.e. < 100 mmol/kg dw) may reduce the regulation of protein synthesis pathways [48].”
From Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis (2018) · cites this paper as [48]
The Discussion (page unavailable) suggests that keeping glycogen and energy intake critically low may impair pathways regulating post-exercise muscle protein synthesis. But the paper does not establish the claimed <100 mmol/kg dw cutoff: the Results (page unavailable) describe post-exercise glycogen as <120 mmol/kg dw, and the Abstract reports approximately 100 mmol/kg dw. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAll participants cycled for longer in the high pre-exercise muscle glycogen trial versus the low trial, with average exercise capacity increased by 60 min.
“All participants cycled for longer in the high trial versus the low trial, with average exercise capacity increased by 60 min.”
From Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis (2018) · cites this paper as [48]
Identical cell signalling and post-exercise gene responses (e.g. AMPK-PGC-1α) were observed between high and low pre-exercise muscle glycogen trials despite less work performed in the low glycogen trial.
“We observed identical cell signalling and post-exercise gene responses between trials (e.g. AMPK-PGC-1α) despite the completion of less work performed in the low glycogen trial.”
From Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis (2018) · cites this paper as [48]
During periods in which CHO availability was strategically reduced ('training low') there was an increase of molecular markers related to endurance training-induced adaptation.
“Several studies demonstrated that during periods in which CHO availability was strategically reduced (known as “training low”) there was an increase of molecular markers related to endurance training-induced adaptation [31,32].”
From Carbohydrate Availability and Physical Performance: Physiological Overview and Practical Recommendations (2019) · cites this paper as [32]
It could be important to differentiate between the optimal nutrition to compete and to train.
“Considering these responses, it could be important to differentiate between the optimal nutrition to compete and to train [32].”
From Carbohydrate Availability and Physical Performance: Physiological Overview and Practical Recommendations (2019) · cites this paper as [32]
The sleep-low strategy allows athletes to perform high intensity training sessions supported by high CHO availability while enhancing metabolic adaptation associated with low glycogen availability.
“The “sleep-low” (SL) strategy represents one such sequence of periodized CHO availability, which allows athletes to perform high intensity training sessions supported by high CHO availability while enhancing metabolic adaptation associated with low glycogen availability [14,15,16,17].”
From Periodization of carbohydrate intake: short-term effect on performance (2016) · cites this paper as [17]
Previous studies on training with low glycogen availability typically report higher activity of enzymes involved in fat metabolism, changes in transcription for adaptive genes, or factors involved in mitochondrial biogenesis.
“Typically, these studies report higher activity of enzymes involved in fat metabolism [12,13], and changes in transcription for adaptive genes [14] or factors involved in mitochondrial biogenesis [17].”
From Periodization of carbohydrate intake: short-term effect on performance (2016) · cites this paper as [17]
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Considerations for ultra-endurance activities: part 1- nutrition
Costa, R. J. S., Hoffman, M. D., & Stellingwerff, T. (2019) · Research in Sports Medicine · doi:10.1080/15438627.2018.1502188 · Cited by 83 · see citing works
Considerations for ultra-endurance activities: part 2 – hydration
Hoffman, M. D., Stellingwerff, T., & Costa, R. J. S. (2018) · Research in Sports Medicine · doi:10.1080/15438627.2018.1502189 · Cited by 83 · see citing works
Exogenous Ketone Supplements in Athletic Contexts: Past, Present, and Future
Evans, M., McClure, T. S., Koutnik, A. P., & Egan, B. (2022) · Sports Medicine · doi:10.1007/s40279-022-01756-2 · Cited by 76 · see citing works
Periodization of carbohydrate intake: short-term effect on performance
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Rothschild, J. A., Kilding, A. E., & Plews, D. J. (2020) · Nutrients · doi:10.3390/nu12113473 · Cited by 67 · see citing works
From Paper to Podium: Quantifying the Translational Potential of Performance Nutrition Research
Close, G. L., Kasper, A. M., & Morton, J. P. (2019) · Sports Medicine · doi:10.1007/s40279-018-1005-2 · Cited by 64 · see citing works
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Anderson, L. J., Naughton, R. J., Close, G. L., Michele, R. D., Morgans, R., Drust, B., & Morton, J. P. (2017) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2016-0265 · Cited by 51 · see citing works
Hearris, M. A., Hammond, K. M., Seaborne, R. A. E., Stocks, B., Shepherd, S. O., Philp, A., Sharples, A. P., Morton, J. P., & Louis, J. B. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00913.2018 · Cited by 50 · see citing works
Costello, N. B., Deighton, K., Preston, T., Matu, J., Rowe, J., Sawczuk, T., Halkier, M., Read, D. B., Weaving, D., & Jones, B. (2018) · European Journal of Applied Physiology · doi:10.1007/s00421-018-3846-7 · Cited by 44 · see citing works
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Dietary Fuels in Athletic Performance
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Energy and Macronutrient Considerations for Young Athletes
Hannon, M. P., Close, G. L., & Morton, J. P. (2020) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000570 · Cited by 37 · see citing works
Fell, J. M., Hearris, M. A., Ellis, D. G., Moran, J. E. P., Jevons, E. F. P., Owens, D. J., Strauss, J. A., Cocks, M. S., Louis, J. B., Shepherd, S. O., et al. (2021) · The Journal of Physiology · doi:10.1113/jp281127 · Cited by 37 · see citing works
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Low-Carbohydrate Training Increases Protein Requirements of Endurance Athletes
Gillen, J. B., West, D. W. D., Williamson, E., Fung, H. J. W., & Moore, D. R. (2019) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002036 · Cited by 34 · see citing works
Carbohydrate Consumption and Periodization Strategies Applied to Elite Soccer Players
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Evolution of the use of sports supplements
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Factors Influencing AMPK Activation During Cycling Exercise: A Pooled Analysis and Meta-Regression
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Postexercise High-Fat Feeding Suppresses p70S6K1 Activity in Human Skeletal Muscle
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Fibre: The Forgotten Carbohydrate in Sports Nutrition Recommendations
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Nutritional Considerations for Female Athletes in Weight Category Sports
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The impact of sleeping with reduced glycogen stores on immunity and sleep in triathletes
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Ghiarone, T., Andrade‐Souza, V. A., LEARSI, S. K., Tomazini, F., Ataide‐Silva, T., Sansonio, A., Fernandes, M. P., Saraiva, K., de Figueiredo, R. C. B. Q., Tourneur, Y., et al. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00060.2019 · Cited by 25 · see citing works
Glycogen Utilization during Running: Intensity, Sex, and Muscle-Specific Responses
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Areta, J. L., Iraki, J., Owens, D. J., Joanisse, S., Philp, A., Morton, J. P., & Hallén, J. (2020) · Experimental Physiology · doi:10.1113/ep088795 · Cited by 20 · see citing works
Repeated muscle glycogen supercompensation with four days’ recovery between exhaustive exercise
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Ultrasound Does Not Detect Acute Changes in Glycogen in Vastus Lateralis of Man
Routledge, H. E., Bradley, W. J., Shepherd, S. O., Cocks, M. S., Erskine, R. M., Close, G. L., & Morton, J. P. (2019) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002052 · Cited by 19 · see citing works
Hearris, M. A., Owens, D. J., Strauss, J. A., Shepherd, S. O., Sharples, A. P., Morton, J. P., & Louis, J. B. (2020) · Experimental Physiology · doi:10.1113/ep088866 · Cited by 19 · see citing works
Human skeletal muscle methylome after low-carbohydrate energy-balanced exercise
Gorski, P. P., Turner, D. C., Iraki, J., Morton, J. P., Sharples, A. P., & Areta, J. L. (2023) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00029.2023 · Cited by 16 · see citing works
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Edwards, V. C., Myers, S., Wardle, S. L., Siddall, A. G., Powell, S. D., Needham‐Beck, S. C., Jackson, S., Greeves, J. P., & Blacker, S. D. (2022) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2021-0191 · Cited by 12 · see citing works
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Podlogar, T., Free, B. G., & Wallis, G. A. (2020) · European Journal of Sport Science · doi:10.1080/17461391.2020.1730447 · Cited by 11 · see citing works
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Knuiman, P., Hopman, M. T. E., Wouters, J. A., & Mensink, M. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00028 · Cited by 9 · see citing works
Features of the diet of athletes playing sports
Lobanov, V. G., Kasyanov, G. I., & Mazurenko, E. A. (2019) · Proceedings of the Voronezh State University of Engineering Technologies · doi:10.20914/2310-1202-2019-1-160-167 · Cited by 9 · see citing works
Yan, X., Dunne, D. M., Impey, S. G., Cunniffe, B., Lefevre, C. E., Mazorra, R., Morton, J. P., Tod, D., Close, G. L., Murphy, R., et al. (2022) · Contemporary Clinical Trials Communications · doi:10.1016/j.conctc.2022.100899 · Cited by 8 · see citing works
Best, R., Maulder, P. S., & BERGER, N. J. A. (2021) · Beverages · doi:10.3390/beverages7010009 · Cited by 7 · see citing works
Bennett, S. E., Tiollier, E., Brocherie, F., Owens, D. J., Morton, J. P., & Louis, J. B. (2021) · PLoS ONE · doi:10.1371/journal.pone.0260959 · Cited by 8 · see citing works
Dietary Manipulations Concurrent to Endurance Training
Rothschild, J. A., & Earnest, C. P. (2018) · Journal of Functional Morphology and Kinesiology · doi:10.3390/jfmk3030041 · Cited by 8 · see citing works
Allan, R., Sharples, A. P., Cocks, M. S., Drust, B., Dutton, J. J., Dugdale, H. F., Mawhinney, C., Clucas, A., Hawkins, W. C., Morton, J. P., et al. (2019) · Physiological Reports · doi:10.14814/phy2.14082 · Cited by 7 · see citing works
Margolis, L. M., Wilson, M. A., Whitney, C. C., Carrigan, C. T., Murphy, N. E., Hatch‐McChesney, A., & Pasiakos, S. M. (2021) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-021-00455-z · Cited by 8 · see citing works
Stables, R. G., Anderson, L. J., Sale, C., Hannon, M. P., Dunn, R. K., TANG, J. C. Y., Fraser, W. D., Costello, N. B., Close, G. L., & Morton, J. P. (2024) · European Journal of Applied Physiology · doi:10.1007/s00421-024-05574-4 · Cited by 7 · see citing works
Ramonas, A., Laursen, P. B., Williden, M., & Kilding, A. E. (2022) · European Journal of Sport Science · doi:10.1080/17461391.2022.2130097 · Cited by 7 · see citing works
Ramonas, A., Laursen, P. B., Williden, M., Chang, W., & Kilding, A. E. (2023) · European Journal of Applied Physiology · doi:10.1007/s00421-023-05162-y · Cited by 6 · see citing works
Turner, O., Chessor, R. J., & Mitchell, N. (2025) · Performance Nutrition · doi:10.1186/s44410-025-00001-x · Cited by 5 · see citing works
Jones, L. A., Leung, L., Barrett, J. S., Fortis, H. O., Strauss, J. A., & Shepherd, S. O. (2025) · European Journal of Applied Physiology · doi:10.1007/s00421-025-05995-9 · Cited by 5 · see citing works
Reposición del Glucógeno Muscular en la Recuperación del Deportista
Ordóñez, F. M., Grimaldi-Puyana, M., & Sánchez-Oliver, A. J. (2019) · SPORT TK-Revista EuroAmericana de Ciencias del Deporte · doi:10.6018/sportk.362071 · Cited by 5 · see citing works
Waterworth, S., Spencer, C. C., Porter, A. L., & Morton, J. P. (2020) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2019-0275 · Cited by 5 · see citing works
Energy intake, hydration status, and sleep of world-class male archers during competition
Esen, Ö., Walshe, I. H., & Goodall, S. (2024) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2024.2345358 · Cited by 4 · see citing works
Baleeiro, R. D. S., Guimarães, A. P., de Souza, P. M., Andrade, R. D. S., de Queiroz, K. B., Coelho, D. B., de Oliveira, E. C., & Becker, L. K. (2021) · Journal of Nutrition and Metabolism · doi:10.1155/2021/6683657 · Cited by 4 · see citing works
Exercise and Muscle Glycogen Metabolism
Ørtenblad, N., Nielsen, J., Morton, J. P., & Areta, J. L. (2022) · Physiology in health and disease · doi:10.1007/978-3-030-94305-9_5 · Cited by 4 · see citing works
Wei, R. J., Orbeta, L., Hatamiya, N. S., & Chang, C. J. (2023) · Current Sports Medicine Reports · doi:10.1249/jsr.0000000000001085 · Cited by 4 · see citing works
Wood, T. R., & Kelly, C. (2017) · Journal of Metabolic Health · doi:10.4102/jir.v2i1.20 · Cited by 3 · see citing works
Юрьевич, Л. Н. (2018) · Food Industry · doi:10.29141/2500-1922-2018-6-1-3 · Cited by 3 · see citing works
Ketogenic and High-Carbohydrate Diets in Cyclists and Triathletes
Kreutzer, A., Graybeal, A. J., Rack, P., Moss, K., Augsburger, G., Willis, J. L., Braun-Trocchio, R., & Shah, M. (2022) · Communications in Kinesiology · doi:10.51224/cik.2022.42 · Cited by 3 · see citing works
Carbohydrate Metabolism During Exercise
Hammond, K. M., Fell, M. J., Hearris, M. A., & Morton, J. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814593-7.00011-6 · Cited by 3 · see citing works
Greene, J. (2021) · Liverpool John Moores University · doi:10.24377/ljmu.t.00014802 · Cited by 3 · see citing works
Lis, D. M., & Strobel, N. (2026) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2025-0198 · Cited by 2 · see citing works
Kwak, S. E., Zheng, A., Arias, E. B., Wang, H., Pan, X., Yue, Y., Duan, D., & Cartee, G. D. (2024) · PLoS ONE · doi:10.1371/journal.pone.0295964 · Cited by 2 · see citing works
Zignoli, A., Martinez‐Gonzalez, B., Skroče, K., Lipman, D. J., Zisser, H., & Giorgi, A. (2024) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2024-0119 · Cited by 2 · see citing works
Managing Fatigue in Team Sports: A Brief Review of Concurrent Training Effects Within the Microcycle
Γραμμένου, Μ., & Nulty, C. D. (2025) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000903 · Cited by 2 · see citing works
Lost Metabolic Machinery During Ketosis? Depends Where You Are Looking
Wood, T. R. (2017) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000322 · Cited by 2 · see citing works
Leogrande, P., Jardines, D., Brito, D. M., de la Torre, X., Botrè, F., Luch, A., Diel, P., & Parr, M. K. (2024) · Journal of Chemometrics · doi:10.1002/cem.3594 · Cited by 1 · see citing works
SAKAMOTO, T., Ueda, S.-Y., & Nakahara, H. (2024) · Nutrients · doi:10.3390/nu16132138 · Cited by 1 · see citing works
Carbohydrate Mouth Rinsing Duration Impact on Fatigue and Recovery from Repeated Sprint Exercise
Tomko, P. M. (2017) · OhioLink ETD Center (Ohio Library and Information Network) · Cited by 1 · see citing works
Specificity of nutrition of representatives of artistic sports (problems and disadvantages)
Путро, Л., Котко, Д., Гончарук, Н. П., & Шевцов, С. О. (2020) · Scientific Journal of National Pedagogical Dragomanov University Series 15 Scientific and pedagogical problems of physical culture (physical culture and sports) · doi:10.31392/npu-nc.series15.2020.4(124).15 · Cited by 1 · see citing works
"The Basics of Carbohydrate Periodization for Athletes and Coaches"
Fernandes, H. S. (2022) · Biomedical Journal of Scientific & Technical Research · doi:10.26717/bjstr.2022.42.006789 · Cited by 1 · see citing works
Rothschild, J. A., Morton, J. P., Stewart, T. I., Kilding, A. E., & Plews, D. J. (2022) · medRxiv · doi:10.1101/2022.06.21.22276725 · Cited by 1 · see citing works
Nutritional Considerations for Concurrent Training
Etheridge, T., & Atherton, P. J. (2018) · Springer eBooks · doi:10.1007/978-3-319-75547-2_16
Wahyudi, H., Bawono, M. N., Pramono, M., Sudijandoko, A., Dewi, R. C., & Pudjijuniarto, P. (2023) · JOSSAE (Journal of Sport Science and Education) · doi:10.26740/jossae.v8n1.p29-36
Individualisation de la nutrition
Marquet, L.-A. (2022) · INSEP-Éditions eBooks · doi:10.4000/books.insep.3180
- Authors
- Impey, S. G., Hammond, K. M., Shepherd, S. O., Sharples, A. P., Stewart, C., Limb, M., Smith, K., Philp, A., Jeromson, S., Hamilton, D. L., Close, G. L., & Morton, J. P.
- Affiliations
- Liverpool John Moores University (GB)
- University of Nottingham (GB)
- University of Birmingham (GB)
- University of Stirling (GB)
- Corresponding author
- Morton, James P.
- ORCID
- Venue
- Physiological Reports
- Publisher
- Wiley
- Published
- 2016-05
- Volume
- 4
- Issue
- 10
- Pages
- e12803
- ISSN
- 2051-817X (ISSN-L)
- PMC
- PMC4886170
- OpenAlex
- W2403601928
- Cited by
- 109
- References
- 66
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 7 · 2023: 7 · 2022: 11 · 2021: 15 · 2020: 11 · 2019: 17 · 2018: 14 · 2017: 10 · 2016: 4
- FWCI
- 10.33
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Physiological Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Keele Research Repository (Keele University) (submittedVersion, cc-by)
- Liverpool John Moores University (submittedVersion)
- Deakin Research Online (Deakin University) (submittedVersion)
- Stirling Online Research Repository (University of Stirling) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Funders
- Science in Sport (plc)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
- Keywords
- carbohydrate restriction, endurance exercise, muscle glycogen, mitochondrial biogenesis, muscle protein synthesis, p70S6K, AMPK, PGC-1α, muscle atrophy, muscle hypertrophy, exercise capacity, glycogen resynthesis, protein supplementation, endurance athletes, signal transduction, gene expression
- MeSH terms
- Adult, Bicycling, Dietary Carbohydrates, Glycogen, Humans, Male, Physical Endurance, Exercise, Muscle, Skeletal, Cross-Over Studies, Diet, Carbohydrate-Restricted, Young Adult, Athletes
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