Artigo Revisado por pares

What is the relationship between the acute muscle protein synthesis response and changes in muscle mass?

2014; American Physiological Society; Volume: 118; Issue: 4 Linguagem: Inglês

10.1152/japplphysiol.00609.2014

ISSN

8750-7587

Autores

Cameron J. Mitchell, Tyler A. Churchward‐Venne, David Cameron‐Smith, Stuart M. Phillips,

Tópico(s)

Muscle Physiology and Disorders

Resumo

ViewpointWhat is the relationship between the acute muscle protein synthesis response and changes in muscle mass?Cameron J. Mitchell, Tyler A. Churchward-Venne, David Cameron-Smith, and Stuart M. PhillipsCameron J. MitchellLiggins Institute, University of Auckland, Auckland, New Zealand; , Tyler A. Churchward-VenneDepartment of Human Movement Sciences, NUTRIM School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Centre, Maastricht, The Netherlands; and , David Cameron-SmithLiggins Institute, University of Auckland, Auckland, New Zealand; , and Stuart M. PhillipsExercise Metabolism Research Group, Department of Kinesiology, McMaster University, Hamilton, Ontario, CanadaPublished Online:15 Feb 2015https://doi.org/10.1152/japplphysiol.00609.2014This is the final version - click for previous versionMoreSectionsPDF (43 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat rates of synthesis of skeletal muscle protein pools (myofibrillar, mitochondrial, sarcoplasmic) are often directly measured through determination of the fractional synthetic rate (FSR) using stable isotope tracer labeled amino acids. This is accomplished by measuring the incorporation of tracer amino acid into muscle protein (bound enrichment), determining the enrichment of the precursor pool, and dividing the incorporation of amino acid tracer over a given period of time by the precursor enrichment, yielding a rate in percent per unit time (3, 22). Measures of muscle protein FSR, often referred to as muscle protein synthesis (MPS), have been routinely employed to examine the acute effects (i.e., several hours to 24 hours) of various exercise and nutritional stimuli. This begs the question as to whether acute early changes in MPS, particularly after resistance exercise (RE), relate to the magnitude of muscle hypertrophy in longer-term training studies? It has been proposed that chronic adaptation (i.e., muscle hypertrophy) with resistance training (RT) occurs as a result of summed periods of repeated acute exercise-induced positive protein balance where MPS exceeds muscle protein breakdown (MPB) (20). In such a scenario, one thesis is that the clearly established heterogeneity of the hypertrophic response to resistance training (8, 14, 15) may be explained, to some degree, by divergent responses of MPS to acute exercise stimuli; but is this the case? It is possible that variations in MPB are also important for the regulation of muscle hypertrophy; however, the measurement of MPB is methodologically challenging and thus is reported infrequently. The magnitude of change in MPB is also much smaller than MPS (7). Additionally, resistance exercise appears to regulate MPB and MPS in a concomitant manner (21). Thus we propose that although it would be ideal to measure the balance between MPS and MPB that MPS is likely to have a greater relationship with hypertrophy than MPB.To date, only a single study has reported the within-subject association between acute MPS rates after RE and skeletal muscle hypertrophy after prolonged RT (15). Another study attempted to correlated MPS measured 24 h after the first training session with muscle hypertrophy (14) In neither study was a linear correlation between MPS and hypertrophy observed (14, 15). The lack of a correlation between pretraining measures of MPS and muscle hypertrophy after prolonged training may lead one to question the value of acute measurements of MPS to yield insight into phenotypic adaptations after RT. Nonetheless, although acute MPS response is not always quantitatively related to muscle hypertrophy, there are a number of examples where MPS response after an acute intervention (nutrition and/or exercise) is aligned with changes in muscle hypertrophy in different subject cohorts. Multiple studies from our laboratory (2, 3, 8, 16, 27, 28, 31) and others (9, 10) have demonstrated that patterns of change in the acute (i.e., over several hours) MPS response after a single session of RE were aligned with the adaptive hypertrophic response after repeated exposure (i.e., for several weeks) to a similar dietary/exercise intervention. For example, the acute MPS response after post-RE consumption of milk versus a soy beverage (31) was qualitatively aligned with changes in lean body mass obtained after 12 weeks of RT and the same protein supplementation (8). In addition, the response of MPS after RE employing lower load contractions (3) and RE bouts employing greater volumes of work (3 sets versus 1 set) (2) were congruent with the hypertrophic response after a period of RT employing these training protocols (16). However, the magnitude of the acute response of MPS and the subsequent hypertrophy with the same stimuli in RT is highly variable between individuals. The source of such hypertrophic variability is likely due to an individual's inherited genetic predisposition, epigenetic influence, and transcriptional plasticity, all of which are likely further impacted by factors such as age, habitual physical activity, and training status. For example, multiple set training has been demonstrated to elicit a greater acute response of MPS (2) and training mediated muscle hypertrophy (12, 16) than single set training; however, a “hypertrophic responder” to resistance exercise may demonstrate a greater response both acutely (i.e., MPS) and in response to RT (i.e. muscle hypertrophy), after single set training, than a “nonresponder” to multiset RT. We propose that the response heterogeneity to RT (8, 14) is often overlooked but it is inherently hard to modify and highlights the importance of adequate sample size to detect differences in the hypertrophic response to various exercise/nutritional stimuli.In comparison to younger persons older persons have a lower MPS rates in response to protein feeding and exercise (5, 13, 17), a condition termed “anabolic resistance” (5). Reductions in loading/physical activity very quickly lead to reductions in anabolic sensitivity to feeding (1, 6, 26). Conversely, even relatively short-duration moderate intensity aerobic exercise performed 15 hours earlier improves the MPS response to meal feeding (25). We hypothesize that physical activity in the hours, possibly days, before measurement of MPS, as well as habitual levels of physical activity and training status, can have a significant impact on magnitude of the MPS response to feeding (25) and possibly exercise. To date, only a few studies have measured MPS in both the trained and untrained state within the same individuals (11, 24, 29). These studies have shown that RT generally reduces the duration of the acute MPS response to a session of RE preformed at the same relative intensity (11, 24); however, we do not know when in a RT program this change occurs. It is known, however, that the transcriptional response after the first exercise session is reflective of muscle damage and differs substantially from a second RE bout performed 48 h later (18). In addition, integrated daily MPS rates were shown to be lower after only two workouts during an 8-day resistance training period (29). Thus it appears that very little “training” is required to modify the acute transcriptional (18) and protein synthetic (11, 24, 29) responses to a bout of RE, at least at the same relative intensity. These observations (11, 18, 24, 29) suggest that acute measurement of the response of MPS to RE is not going to be useful in predicting longer-term capacity for adaption to RT within individuals because it does not represent a “typical” response over a RT program comprised of multiple training sessions (3–4 per week). Indeed, we reported that after the first training session the acute MPS response is not correlated with muscle hypertrophy after RT in the same individuals (15). There are multiple factors that might explain this observation (15): the short duration of the FSR measurement, subtle differences in proteolysis (7), or inherent variation in the measurement (23); however, we theorize that the most likely explanation for the discordance is that the magnitude and duration of the MPS response to acute RE is highly variable between individuals and can change considerably (11, 24, 29, 30) as RT progresses.It is important to point out that the physiological variability methodological variability and test retest reliability could obscure any relationship between acute MPS and hypertrophy. Muscle hypertrophy can be measured in a number of different ways including fiber cross-sectional area from histological section, lean mass from DXA, and cross sectional area or volume from MRI or CT scans. In our previous study (15), hypertrophy was measured by MRI-derived muscle cross-sectional area because in our experience and that of others (19) variability is ∼1%. Much less is known about reproducibility of MPS measure in the same subject, and it is conceivable variability inherent in the MPS methodology could obscure any potential relationship.Acute measurements of MPS response can provide important insight into the mechanistic underpinnings of divergent exercise and nutritional manipulations (3, 4, 10, 24, 31). Such measures have shown the ability to discriminate between gross differences in muscle contraction volume (2) and relative fatigue (3, 10) as well as differences in protein quality and amino acid composition (4, 31). Nonetheless, at an individual level a divergent acute response in MPS may be necessary but is not sufficient to conclude that a divergent muscle hypertrophic response will follow and similarly so for RT plus nutrition-induced changes in hypertrophy (14, 15). It is likely that a high degree of intraindividual variation in various factors with repeated exposure to the exercise stimulus. In conclusion, results from acute measures of MPS should continue to be regarded important indicators of the gross-level potential of a given exercise/nutritional intervention; however, long-term studies are necessary to elucidate the capacity to which an individual will respond in terms of altered phenotype (i.e., increased muscle mass) in response to chronic exposure to a given exercise/nutritional intervention.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the author(s).AUTHOR CONTRIBUTIONSAuthor contributions: C.J.M. and T.A.C.-V. drafted manuscript; C.J.M., T.A.C.-V., D.C.-S., and S.M.P. edited and revised manuscript; C.J.M., T.A.C.-V., D.C.-S., and S.M.P. approved final version of manuscript.REFERENCES1. Breen L, Stokes KA, Churchward-Venne TA, Moore DR, Baker SK, Smith K, Atherton PJ, Phillips SM. Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. J Clin Endocrinol Metab 98: 2604–2612, 2013.Crossref | PubMed | ISI | Google Scholar2. Burd NA, Holwerda AM, Selby KC, West DW, Staples AW, Cain NE, Cashaback JG, Potvin JR, Baker SK, Phillips SM. Resistance exercise volume affects myofibrillar protein synthesis and anabolic signalling molecule phosphorylation in young men. J Physiol 588: 3119–3130, 2010.Crossref | PubMed | ISI | Google Scholar3. Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, Holwerda AM, Parise G, Rennie MJ, Baker SK, Phillips SM. Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PloS One 5: e12033, 2010.Crossref | PubMed | ISI | Google Scholar4. Churchward-Venne TA, Breen L, Di Donato DM, Hector AJ, Mitchell CJ, Moore DR, Stellingwerff T, Breuille D, Offord EA, Baker SK, Phillips SM. Leucine supplementation of a low-protein mixed macronutrient beverage enhances myofibrillar protein synthesis in young men: a double-blind, randomized trial. Am J Clin Nutr 99: 276–286, 2014.Crossref | PubMed | ISI | Google Scholar5. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422–424, 2005.Crossref | PubMed | ISI | Google Scholar6. Glover EI. Immobilisation induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 24: 6049–6061, 2008.Crossref | ISI | Google Scholar7. Glynn EL, Fry CS, Drummond MJ, Dreyer HC, Dhanani S, Volpi E, Rasmussen BB. Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Am J Physiol Regul Integr Comp Physiol 299: R533–R540, 2010.Link | ISI | Google Scholar8. Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV, Phillips SM. Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Am J Clin Nutr 86: 373–381, 2007.Crossref | PubMed | ISI | Google Scholar9. Holm L, Reitelseder S, Pedersen TG, Doessing S, Petersen SG, Flyvbjerg A, Andersen JL, Aagaard P, Kjaer M. Changes in muscle size and MHC composition in response to resistance exercise with heavy and light loading intensity. J Appl Physiol 105: 1454–1461, 2008.Link | ISI | Google Scholar10. Holm L, van Hall G, Rose AJ, Miller BF, Doessing S, Richter EA, Kjaer M. Contraction intensity and feeding affect collagen and myofibrillar protein synthesis rates differently in human skeletal muscle. Am J Physiol Endocrinol Metab 298: E257–E269, 2010.Link | ISI | Google Scholar11. Kim PL, Staron RS, Phillips SM. Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J Physiol 568: 283–290, 2005.Crossref | PubMed | ISI | Google Scholar12. Krieger Single vs JW. multiple sets of resistance exercise for muscle hypertrophy: a meta-analysis. J Strength Conditioning Res 24: 1150–1159, 2010.Crossref | ISI | Google Scholar13. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587: 211–217, 2009.Crossref | PubMed | ISI | Google Scholar14. Mayhew DL, Kim JS, Cross JM, Ferrando AA, Bamman MM. Translational signaling responses preceding resistance training-mediated myofiber hypertrophy in young and old humans. J Appl Physiol 107: 1655–1662, 2009.Link | ISI | Google Scholar15. Mitchell CJ, Churchward-Venne TA, Parise G, Bellamy L, Baker SK, Smith K, Atherton PJ, Phillips SM. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PloS One 9: e89431, 2014.Crossref | PubMed | ISI | Google Scholar16. Mitchell CJ, Churchward-Venne TA, West DW, Burd NA, Breen L, Baker SK, Phillips SM. Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J Appl Physiol 113: 71–77, 2012.Link | ISI | Google Scholar17. Moore DR, Churchward-Venne TA, Witard O, Breen L, Burd NA, Tipton KD, Phillips SM. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci, in press.ISI | Google Scholar18. Murton AJ, Billeter R, Stephens FB, Des Etages SG, Graber F, Hill RJ, Marimuthu K, Greenhaff PL. Transient transcriptional events in human skeletal muscle at the outset of concentric resistance exercise training. J Appl Physiol (1985) 116: 113–125, 2014.Link | ISI | Google Scholar19. Nordez A, Jolivet E, Sudhoff I, Bonneau D, de Guise JA, Skalli W. Comparison of methods to assess quadriceps muscle volume using magnetic resonance imaging. J Magn Reson Imaging 30: 1116–1123, 2009.Crossref | ISI | Google Scholar20. Phillips SM. A brief review of critical processes in exercise-induced muscular hypertrophy. Sports Med 44, Suppl 1: 71–77, 2014.Crossref | PubMed | ISI | Google Scholar21. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol Endocrinol Metab 273: E99–E107, 1997.Link | ISI | Google Scholar22. Rennie MJ. An introduction to the use of tracers in nutrition and metabolism. Proc Nutr Soc 58: 935–944, 1999.Crossref | PubMed | ISI | Google Scholar23. Smith GI, Patterson BW, Mittendorfer B. Human muscle protein turnover–why is it so variable? J Appl Physiol 110: 480–491, 2011.Link | ISI | Google Scholar24. Tang JE, Perco JG, Moore DR, Wilkinson SB, Phillips SM. Resistance training alters the response of fed state mixed muscle protein synthesis in young men. Am J Physiol Regul Integr Comp Physiol 294: R172–R178, 2008.Link | ISI | Google Scholar25. Timmerman KL, Dhanani S, Glynn EL, Fry CS, Drummond MJ, Jennings K, Rasmussen BB, Volpi E. A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am J Clin Nutr 95: 1403–1412, 2012.Crossref | PubMed | ISI | Google Scholar26. Wall BT, Snijders T, Senden JM, Ottenbros CL, Gijsen AP, Verdijk LB, van Loon LJ. Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men. J Clin Endocrinol Metab 98: 4872–4881, 2013.Crossref | PubMed | ISI | Google Scholar27. West DW, Burd NA, Tang JE, Moore DR, Staples AW, Holwerda AM, Baker SK, Phillips SM. Elevations in ostensibly anabolic hormones with resistance exercise enhance neither training-induced muscle hypertrophy nor strength of the elbow flexors. J Appl Physiol 108: 60–67, 2009.Link | ISI | Google Scholar28. West DW, Kujbida GW, Moore DR, Atherton P, Burd NA, Padzik JP, De Lisio M, Tang JE, Parise G, Rennie MJ, Baker SK, Phillips SM. Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men. J Physiol 587: 5239–5247, 2009.Crossref | PubMed | ISI | Google Scholar29. Wilkinson DJ, Franchi MV, Brook MS, Narici MV, Williams JP, Mitchell WK, Szewczyk NJ, Greenhaff PL, Atherton PJ, Smith K. A validation of the application of D2O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am J Physiol Endocrinol Metab 306: E571–E579, 2014.Link | ISI | Google Scholar30. Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586: 3701–3717, 2008.Crossref | PubMed | ISI | Google Scholar31. Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85: 1031–1040, 2007.Crossref | PubMed | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: S. M. Phillips, The Dept. of Kinesiology, McMaster Univ., 1280 Main St. West, Hamilton Ontario L8S 4L8, Canada (e-mail: [email protected]ca). 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Atherton, and Kenneth Smith28 April 2020 | Journal of Applied Physiology, Vol. 128, No. 5Transition to a More even Distribution of Daily Protein Intake is Associated with Enhanced Fat Loss during a Hypocaloric & Physical Activity Intervention in Obese Older Adults6 January 2020 | The journal of nutrition, health & aging, Vol. 24, No. 2The effects of resistance training with or without peanut protein supplementation on skeletal muscle and strength adaptations in older individuals1 April 2022 | Journal of the International Society of Sports Nutrition, Vol. 17, No. 1Recent advances in understanding resistance exercise training-induced skeletal muscle hypertrophy in humans24 February 2020 | F1000Research, Vol. 9Revisiting the roles of protein synthesis during skeletal muscle hypertrophy induced by exerciseVandré Casagrande Figueiredo5 November 2019 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 317, No. 5Effect of a High Fat and High Protein Diet on Exercise-Induced Skeletal Muscle Hypertrophy in Rats3 October 2019 | International Journal of Nutrition, Vol. 4, No. 3Differential Stimulation of Post-Exercise Myofibrillar Protein Synthesis in Humans Following Isonitrogenous, Isocaloric Pre-Exercise Feeding19 July 2019 | Nutrients, Vol. 11, No. 7The age-related loss of skeletal muscle mass and function: Measurement and physiology of muscle fibre atrophy and muscle fibre loss in humansAgeing Research Reviews, Vol. 47Resistance exercise stimulates mixed muscle protein synthesis in lean and obese young adults16 July 2018 | Physiological Reports, Vol. 6, No. 14Biomarkers associated with low, moderate, and high vastus lateralis muscle hypertrophy following 12 weeks of resistance training5 April 2018 | PLOS ONE, Vol. 13, No. 4The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis27 December 2017 | European Journal of Applied Physiology, Vol. 118, No. 3Daily resistance-type exercise stimulates muscle protein synthesis in vivo in young menAndrew M. Holwerda, Kevin J. M. Paulussen, Maarten Overkamp, Joey S. J. Smeets, Annemie P. Gijsen, Joy P. B. Goessens, Lex B. Verdijk, and Luc J. C. van Loon12 January 2018 | Journal of Applied Physiology, Vol. 124, No. 1Native whey induces higher and faster leucinemia than other whey protein supplements and milk: a randomized controlled trial31 January 2017 | BMC Nutrition, Vol. 3, No. 1Leucine Supplementation in a Chronically Protein-Restricted Diet Enhances Muscle Weight and Postprandial Protein Synthesis of Skeletal Muscle by Promoting the mTOR Pathway in Adult RatsEngineering, Vol. 3, No. 5Within-day protein distribution does not influence body composition responses during weight loss in resistance-training adults who are overweightThe American Journal of Clinical Nutrition, Vol. 106, No. 5Light-load resistance exercise increases muscle protein synthesis and hypertrophy signaling in elderly menJakob Agergaard, Jacob Bülow, Jacob K. Jensen, Søren Reitelseder, Micah J. Drummond, Peter Schjerling, Thomas Scheike, Anja Serena, and Lars Holm1 April 2017 | American Journal of Physiology-Endocrinology and Metabolism, Vol. 312, No. 4Effects of phosphatidic acid supplementation on muscle thickness and strength in resistance-trained menApplied Physiology, Nutrition, and Metabolism, Vol. 42, No. 4Resistance Training–Induced Elevations in Muscular Strength in Trained Men Are Maintained After 2 Weeks of Detraining and Not Differentially Affected by Whey Protein SupplementationJournal of Strength and Conditioning Research, Vol. 31, No. 4Minimal dose of milk protein concentrate to enhance the anabolic signalling response to a single bout of resistance exercise; a randomised controlled trial1 April 2022 | Journal of the International Society of Sports Nutrition, Vol. 14, No. 1Protein intake for athletes and active adults: Current concepts and controversies14 August 2016 | Nutrition Bulletin, Vol. 41, No. 3No additional effect of different types of physical activity on 10-hour muscle protein synthesis in elderly men on a controlled energy- and protein-sufficient dietExperimental Gerontology, Vol. 79Protein Considerations for Optimising Skeletal Muscle Mass in Healthy Young and Older Adults23 March 2016 | Nutrients, Vol. 8, No. 4Role of Ingested Amino Acids and Protein in the Promotion of Resistance Exercise–Induced Muscle Protein AnabolismThe Journal of Nutrition, Vol. 146, No. 2Muscular adaptations in low- versus high-load resistance training: A meta-analysis20 December 2014 | European Journal of Sport Science, Vol. 16, No. 1The Skeletal Muscle Anabolic Response to Plant- versus Animal-Based Protein ConsumptionThe Journal of Nutrition, Vol. 145, No. 9Nutritional Supplements in Support of Resistance Exercise to Counter Age-Related SarcopeniaAdvances in Nutrition, Vol. 6, No. 4Last Word on Viewpoint: What is the relationship between the acute muscle protein synthetic response and changes in muscle mass?Cameron J. Mitchell, Tyler A. Churchward-Venne, David Cameron-Smith, and Stuart M. Phillips15 February 2015 | Journal of Applied Physiology, Vol. 118, No. 4Commentaries on Viewpoint: What is the relationship between acute measure of muscle protein synthesis and changes in muscle mass?15 February 2015 | Journal of Applied Physiology, Vol. 118, No. 4 More from this issue > Volume 118Issue 4February 2015Pages 495-497 Copyright & PermissionsCopyright © 2015 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00609.2014PubMed25257869History Published online 15 February 2015 Published in print 15 February 2015 Metrics

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