Contextualising maximal fat oxidation during exercise: Determinants and normative values

Frontiers in Physiology

Volumn 9, Issue MAY, 2018, Pages

  Maunder, Ed ^a   Plews, Daniel J ^a   Kilding, Andrew E ^a  

^a AUCKLAND UNIVERSITY OF TECHNOLOGY   (New Zealand)

Author keywords

Cycling; Exercise; Fat oxidation; Normative values; Running

Indexed keywords

BODY WEIGHT GAIN; CYCLING; DIETARY INTAKE; ENVIRONMENTAL TEMPERATURE; EXERCISE INTENSITY; FATTY ACID TRANSPORT; HUMAN; INSULIN SENSITIVITY; LIPID OXIDATION; LIPOLYSIS; LUNG GAS EXCHANGE; NUTRITIONAL STATUS; PHYSICAL PERFORMANCE; REVIEW; RUNNING; SEDENTARY LIFESTYLE; SEX DIFFERENCE; STEADY STATE; TRAINING;

EID: 85047402689     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2018.00599     Document Type: Review

References (156)

1. Achten, J., Gleeson, M., and Jeukendrup, A. E. (2002). Determination of exercise intensity that elicits maximal fat oxidation. Med. Sci. Sports Exerc. 34, 92-97. doi: 10.1097/00005768-200201000-00015
2. Achten, J., and Jeukendrup, A. E. (2003a). Maximal fat oxidation during exercise in trained men. Int. J. Sports Med. 24, 603-608. doi: 10.1055/s-2003-43265
3. Achten, J., and Jeukendrup, A. E. (2003b). The effect of pre-exercise carbohydrate feedings on the intensity that elicits maximal fat oxidation. J. Sports Sci. 21, 1017-1024. doi: 10.1080/02640410310001641403
4. Achten, J., and Jeukendrup, A. E. (2004). Relation between plasma lactate concentration and fat oxidation rates over a wide range of exercise intensities. Int. J. Sports Med. 25, 32-37. doi: 10.1055/s-2003-45231
5. Achten, J., Venables, M. C., and Jeukendrup, A. E. (2003). Fat oxidation rates are higher during running compared with cycling over a wide range of intensities. Metab. Clin. Exp. 52, 747-752. doi: 10.1016/S0026-0495(03)00068-4
6. Ahlborg, B., Bergström, J., Ekelund, L., and Hultman, E. (1967). Muscle glycogen and muscle electrolytes during prolonged phyiscal exercise. Acta Physiol. Scand. 70, 129-142. doi: 10.1111/j.1748-1716.1967.tb03608.x
7. Alkahtani, S. (2014). Comparing fat oxidation in an exercise test with moderate-intensity interval training. J. Sports Sci. Med. 13, 51-58
8. Alkahtani, S. A., King, N. A., Hills, A. P., and Byrne, N. M. (2013). Effect of interval training intensity on fat oxidation, blood lactate and the rate of perceived exertion in obese men. Springerplus 2:532. doi: 10.1186/2193-1801-2-532
9. Altman, D. G., and Bland, J. M. (2005). Standard Deviations and Standard Errors. Br. Med. J. 331:903. doi: 10.1136/bmj.331.7521.903
10. Ara, I., Larsen, S., Stallknecht, B., Guerra, B., Morales-Alamo, D., Andersen, J., et al. (2011). Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans. Int. J. Obes. 35, 99-108. doi: 10.1038/ijo.2010.123
11. Arkinstall, M. J., Bruce, C. R., Nikolopoulos, V., Garnham, A. P., and Hawley, J. A. (2001). Effect of carbohydrate ingestion on metabolism during running and cycling. J. Appl. Physiol. 91, 2125-2134. doi: 10.1152/jappl.2001.91.5.2125
12. Astorino, T. A., Edmunds, R. M., Clark, A., Gallant, R., King, L., Ordille, G. M., et al. (2017). Change in maximal fat oxidation in response to different regimes of periodized High-Intensity Interval Training (HIIT). Eur. J. Appl. Physiol. 117 745-55. doi: 10.1007/s00421-017-3535-y
13. Astorino, T. A., and Schubert, M. M. (2017). Changes in fat oxidation in response to various regimes of High Intensity Interval Training (HIIT). Eur. J. Appl. Physiol. 118, 51-63. doi: 10.1007/s00421-017-3756-0
14. Astorino, T. A., Schubert, M. M., Palumbo, E., Stirling, D., and McMillan, D. W. (2013). Effect of two doses of interval training on maximal fat oxidation in sedentary women. Med. Sci. Sports Exerc. 45, 1878-1886. doi: 10.1249/MSS.0b013e3182936261
15. Bagley, L., Slevin, M., Bradburn, S., Liu, D., Murgatroyd, C., Morrissey, G., et al. (2016). Sex differences in the effects of 12 weeks sprint interval training on body fat mass and the rates of fatty acid oxidation and VO2max during exercise. BMJ Open Sport Exerc. Med. 2:e000056. doi: 10.1136/bmjsem-2015-000056
16. Bergman, B. C., and Brooks, G. A. (1999). Respiratory gas-exchange ratios during graded exercise in fed and fasted trained and untrained men. J. Appl. Physiol. 86, 479-487. doi: 10.1152/jappl.1999.86.2.479
17. Bergström, J., Hermansen, L., Hultman, E., and Saltin, B. (1967). Diet, muscle glycogen and physical performance. Acta Physiol. Scand. 71, 140-150. doi: 10.1111/j.1748-1716.1967.tb03720.x
18. Bergström, J., and Hultman, E. (1967). A Study of the Glycogen Metabolism during Exercise in Man. Scand. J. Clin. Lab. Invest. 19, 218-228. doi: 10.3109/00365516709090629
19. Besnier, F., Lenclume, V., Gérardin, P., Fianu, A., Martinez, J., and Naty, N. (2015). Individualized exercise training at maximal fat oxidation combined with fruit and vegetable-rich diet in overweight or obese women: the lipoxmax-réunion randomized controlled trial. PLoS ONE 10:e0139246. doi: 10.1371/journal.pone.0139246
20. Biava, C., Grossman, A., and West, M. (1966). Ultrastructural observations on renal glycogen in normal and pathologic human kidneys. Lab. Invest. 15, 330-56
21. Billat, V. L., Mille-Hamard, L., Petit, B., and Koralsztein, J. P. (1999). The role of cadence on the VO2 slow component in cycling and running in triathletes. Int. J. Sports Med. 20, 429-437. doi: 10.1055/s-1999-8825
22. Bircher, S., Knechtle, B., and Knecht, H. (2005). Is the intensity of the highest fat oxidation at the lactate concentration of 2 Mmol L-1γ a comparison of two different exercise protocols. Eur. J. Clin. Invest. 35, 491-498. doi: 10.1111/j.1365-2362.2005.01538.x
23. Bogdanis, G. C., Vangelakoudi, A., and Maridaki, M. (2008). Peak fat oxidation rate during walking in sedentary overweight men and women. J. Sports Sci. Med. 7, 525-31
24. Bordenave, S., Flavier, S., Fédou, C., Brun, J. F., and Mercier, J. (2007). Exercise calorimetry in sedentary patients: procedures based on short 3 min steps underestimate carbohydrate oxidation and overestimate lipid oxidation. Diabetes Metabol. 33, 379-384. doi: 10.1016/j.diabet.2007.04.003
25. Bordenave, S., Metz, L., Flavier, S., Lambert, K., Ghanassia, E., Dupuy, A., et al. (2008). Training-induced improvement in lipid oxidation in type 2 diabetes mellitus is related to alterations in muscle mitochondrial activity: effect of endurance training in type 2 Diabetes. Diabetes Metabol. 34, 162-168. doi: 10.1016/j.diabet.2007.11.006
26. Borel, B., Coquart, J., Boitel, G., Duhamel, A., Matran, R., Delsart, P., et al. (2015). Effects of endurance training at the crossover point in women with metabolic syndrome. Med. Sci. Sports Exerc. 47, 2380-2388. doi: 10.1249/MSS.0000000000000674
27. Brun, J. F., Halbeher, C., Fédou, C., and Mercier, J. (2011). What are the limits of normality of the LIPOXmaxγ can it be predict without exercise calorimetry? Sci. Sports 26, 166-169. doi: 10.1016/j.scispo.2010.11.001
28. Burgomaster, K. A., Cermak, N. M., Phillips, S. M., Benton, C. R., Bonen, A., and Gibala, M. J. (2007). Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292: R1970-R1976. doi: 10.1152/ajpregu.00503.2006
29. Burgomaster, K. A., Heigenhauser, G. J. F., and Gibala, M. J. (2006). Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J. Appl. Physiol. 1, 2041-2047. doi: 10.1152/japplphysiol.01220.2005
30. Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobochuk, M., MacDonald, M. J., McGee, S. L., et al. (2008). Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586, 151-160. doi: 10.1113/jphysiol.2007.142109
31. Burgomaster, K. A., Hughes, S. C., Heigenhauser, G. J. F., Bradwell, S. N., and Gibala, M. J. (2005). Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. J. Appl. Physiol. 98, 1985-1990. doi: 10.1152/japplphysiol.01095.2004
32. Burke, L. M., Angus, D. J., Cox, G. R., Cummings, N. K., Febbraio, M. A., Gawthorn, K., et al. (2000). Effect of Fat Adaptation and Carbohydrate Restoration on Metabolism and Performance during Prolonged Cycling. J. Appl. Physiol. 89:2413-2421. doi: 10.1152/jappl.2000.89.6.2413
33. Campbell, S. E., Angus, D. J., and Febbraio, M. A. (2001). Glucose kinetics and exercise performance during phases of the menstrual cycle: effect of glucose ingestion. Am. J. Physiol. Endocrinol. Metabol. 281:E817-E825. doi: 10.1152/ajpendo.2001.281.4.E817
34. Carey, D. G. (2009). Quantifying differences in the "fat burning" zone and the aerobic zone: implications for training. J. Strength Cond. Res. 23, 2090-2095. doi: 10.1519/JSC.0b013e3181bac5c5
35. Casadio, J. R., Kilding, A. E., Cotter, J. D., and Laursen, P. B. (2017). From lab to real world: heat acclimation considerations for elite athletes. Sports Med. 47, 1467-1476. doi: 10.1007/s40279-016-0668-9
36. Chenevière, X., Borrani, F., Sangsue, D., Gojanovic, B., and Malatesta, D. (2011). Gender differences in whole-body fat oxidation kinetics during exercise. Appl. Physiol. Nut. Metabol. 36, 88-95. doi: 10.1139/H10-086
37. Chenevière, X., Malatesta, D., Gojanovic, B., and Borrani, F. (2010). Differences in whole-body fat oxidation kinetics between cycling and running. Eur. J. Appl. Physiol. 109, 1037-1045. doi: 10.1007/s00421-010-1443-5
38. Cohen, J. (1977). Statistical Power for the Behavioural Sciences. Oxford, UK: Routledge
39. Croci, I., Borrani, F., Byrne, N., Wood, R., Hickman, I., Chenevière, X., et al. (2014a). Reproducibility of Fatmax and Fat Oxidation Rates during Exercise in Recreationally Trained Males. PLoS ONE 9:e97930. doi: 10.1371/journal.pone.0097930
40. Croci, I., Hickman, I. J., Wood, R. E., Borrani, F., Macdonald, G. A., and Byrne, N. M. (2014b). Fat Oxidation over a range of exercise intensities: fitness versus fatness. Appl. Physiol. Nutr. Metab. 39, 1352-1359. doi: 10.1139/apnm-2014-0144
41. Dandanell, S., Husted, K., Amdisen, S., Vigelsø, A., Dela, F., Larsen, S., et al. (2017a). Influence of maximal fat oxidation on long-term weight loss maintenance in humans. J. Appl. Physiol. 123, 267-274. doi: 10.1152/japplphysiol.00270.2017
42. Dandanell, S., Præst, C. B., Søndergård, S. D., Skovberg, C., Dela, F., Larsen, S., et al. (2017b). Determination of the exercise intensity that elicits maximal fat oxidation in individuals with obesity. Appl. Physiol. Nutr. Metab. 42, 405-412. doi: 10.1139/apnm-2016-0518
43. D'Eon, T. M., Sharoff, C., Chipkin, S. R., Grow, D., Ruby, B. C., and Braun, B. (2002). Regulation of exercise carbohydrate metabolism by estrogen and progesterone in women. Am. J. Phys. Endocrinol. Metab. 283, E1046-E1055. doi: 10.1152/ajpendo.00271.2002
44. D'Eon, T. M., Souza, S. C., Aronovitz, M., Obin, M. S., Fried, S. K., and Greenberg, A. S. (2005). Estrogen regulation of adiposity and fuel partitioning: evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J. Biol. Chem. 280, 35983-35991. doi: 10.1074/jbc. M507339200
45. De Souza Silveira, R., Carlsohn, A., Langen, G., Mayer, F., and Scharhag-Rosenberger, F. (2016). Reliability and day-to-day variability of peak fat oxidation during treadmill ergometry. J. Int. Soc. Sports Nutr. 13:4. doi: 10.1186/s12970-016-0115-1
46. Devries, M. C. (2016). Sex-based differences in endurance exercise muscle metabolism: impact on exercise and nutritional strategies to optimize health and performance in women. Exp. Physiol. 2, 243-249. doi: 10.1113/EP085369
47. Egan, B., Dowling, P., O'Connor, P. L., Henry, M., Meleady, P., Zierath, J. R., et al. (2011). 2-D DIGE analysis of the mitochondrial proteome from human skeletal muscle reveals time course-dependent remodelling in response to 14 consecutive days of endurance exercise training. Proteomics 11, 1413-1428. doi: 10.1002/pmic.201000597
48. Egan, B., and Zierath, J. R. (2013). Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17, 162-84. doi: 10.1016/j.cmet.2012.12.012
49. Febbraio, M. A., Carey, M. F., Snow, R. J., Stathis, C. G., and Hargreaves, M. (1996). Influence of elevated muscle temperature on metabolism during intense, dynamic exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271, R1251-R1255. doi: 10.1152/ajpregu.1996.271.5.R1251
50. Febbraio, M. A., Lambert, D. L., Starkie, R. L., Proietto, J., and Hargreaves, M. (1998). Effect of epinephrine on muscle glycogenolysis during exercise in trained men. J. Appl. Physiol. 84, 465-470. doi: 10.1152/jappl.1998.84.2.465
51. Febbraio, M. A., Snow, R. J., Hargreaves, M., Stathis, C. G., Martin, I. K., and Carey, M. F. (1994a). Muscle metabolism during exercise and heat stress in trained men: effect of acclimation. J. Appl. Physiol. 76, 589-597. doi: 10.1152/jappl.1994.76.2.589
52. Febbraio, M. A., Snow, R. J., Stathis, C. G., Hargreaves, M., and Carey, M. F. (1994b). Effect of heat stress on muscle energy metabolism during exercise. J. Appl. Physiol. 77, 2827-2831. doi: 10.1152/jappl.1994.77.6.2827
53. Fletcher, G., Eves, F. F., Glover, E. I., Robinson, S. L., Vernooij, C. A., Thompson, J. L., et al. (2017). Dietary intake is independently associated with the maximal capacity for fat oxidation during exercise. Am. J. Clini. Nutr. 105, 864-872. doi: 10.3945/ajcn.116.133520
54. Frandsen, J., Vest, S., Larsen, S., Dela, F., and Helge, J. W. (2017). Maximal fat oxidation is related to performance in an ironman triathlon. Int. J. Sports Med. 38, 975-982. doi: 10.1055/s-0043-117178
55. Fritz, I. B., and Yue, K. T. N. (1963). Long-chain carnitine acyl-transferase and the role of acylcarnitine derivatives in the catalytic increase of fatty acid oxidation induced by carnitine. J. Lipid Res. 4, 279-88
56. Gagnon, D. D., Rintamäki, H., Gagnon, S. S., Cheung, S. S., Herzig, K. H., Porvari, K., et al. (2013). Cold exposure enhances fat utilization but not non-esterified fatty acids, glycerol or catecholamines availability during submaximal walking and running. Front. Physiol. 4:99. doi: 10.3389/fphys.2013.00099
57. Galloway, S. D. R., and Maughan, R. J. (1997). Effects of ambient temperature on the capacity to perform prolonged cycle exercise in man. Med. Sci. Sports Exerc. 29, 1240-1249. doi: 10.1097/00005768-199709000-00018
58. Gibala, M. J., Little, J. P., van Essen, M., Wilkin, G. P., Burgomaster, K. A., Safdar, A., et al. (2006). Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J. Physiol. 575, 901-911. doi: 10.1113/jphysiol.2006.112094
59. Gmada, N., Marzouki, H., Haboubi, M., Tabka, Z., Shephard, R. J., and Bouhlel, E. (2012). Crossover and maximal fat-oxidation points in sedentary healthy subjects: methodological issues. Diabetes Metab. 38, 40-45. doi: 10.1016/j.diabet.2011.07.004
60. González-Haro, C. (2011). Maximal fat oxidation rate and cross-over point with respect to lactate thresholds do not have good agreement. Int. J. Sports Med. 32, 379-385. doi: 10.1055/s-0031-1271763
61. Gonzalez-Haro, C., Galilea, P. A., Gonzalez-de-Suso, J. M., Drobnic, F., Escanero, J. F., and Chander, M. (2007). Maximal lipidic power in high competitive level triathletes and cyclists. Br. J. Sports Med. 41, 23-28. doi: 10.1136/bjsm.2006.029603
62. González, J. G. P., Guadalupe-Grau, A., González, F. G. R., Peralta, R. T., Morales-Alamo, D., Rodríguez-García, L., et al. (2017). Androgen receptor gene polymorphisms and maximal fat oxidation in healthy men: a longitudinal study. Nutr. Hosp. 34, 1089-98. doi: 10.20960/nh.885
63. Gonzalez, J. T., Fuchs, C. J., Betts, J. A., and van Loon, L. J. C. (2016). Liver glycogen metabolism during and after prolonged endurance-type exercise. Am. J. Physiol. Endocrinol. Metab. 311, E543-E553. doi: 10.1152/ajpendo.00232.2016
64. Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., and Bishop, D. J. (2016a). Mitochondrial adaptations to high-volume exercise training are rapidly reversed after a reduction in training volume in human skeletal muscle. FASEB J. 30, 3413-3423. doi: 10.1096/fj.201500100R
65. Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., and Bishop, D. J. (2016b). Training intensity modulates changes in PGC-1a and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle. FASEB J. 30, 959-970. doi: 10.1096/fj.15-276907
66. Guadalupe-Grau, A., Plenge, U., Helbo, S., Kristensen, M., Andersen, P. R., Fago, A., et al. (2014). Effects of an 8-Weeks erythropoietin treatment on mitochondrial and whole body fat oxidation capacity during exercise in healthy males. J. Sports Sci. 33, 570-578. doi: 10.1080/02640414.2014.951872
67. Harber, M. P., Kaminsky, L. A., Arena, R., Blair, S. N., Franklin, B. A., Myers, J., et al. (2017). Impact of cardiorespiratory fitness on all-cause and disease-specific mortality: advances since 2009. Prog. Cardiovasc. Dis. 60, 11-20. doi: 10.1016/j.pcad.2017.03.001
68. Hargreaves, M., Angus, D., Howlett, K., Conus, N. M., and Febbraio, M. A. (1996a). Effect of heat stress on glucose kinetics during exercise. J. Appl. Physiol. 81, 1594-1597. doi: 10.1152/jappl.1996.81.4.1594
69. Hargreaves, M., Dillo, P., Angus, D., and Febbraio, M. (1996b). Effect of fluid ingestion on muscle metabolism during prolonged exercise. J. Appl. Physiol. 80, 363-366. doi: 10.1152/jappl.1996.80.1.363
70. Hargreaves, M., McConell, G., and Proietto, J. (1995). Influence of muscle glycogen on glycogenolysis and glucose uptake during exercise in humans. J. Appl. Physiol. 78, 288-292. doi: 10.1152/jappl.1995.78.1.288
71. Haufe, S., Engeli, S., Budziarek, P., Utz, W., Schulz-Menger, J., Hermsdorf, M., et al. (2010). Determinants of exercise-induced fat oxidation in obese women and men. Horm. Metab. Res. 42, 215-221. doi: 10.1055/s-0029-1242745
72. Hermansen, L., Hultman, E., and Saltin, B. (1967). Muscle glycogen during prolonged severe exercise. Acta Physiol. Scand. 71, 129-139. doi: 10.1111/j.1748-1716.1967.tb03719.x
73. Holloszy, J. O. (2011). Regulation of mitochondrial biogenesis and GLUT4 expression by exercise. Comp. Physiol. 1, 921-940. doi: 10.1002/cphy.c100052
74. Hoppeler, H., Howald, H., Conley, K., Lindstedt, S. L., Claassen, H., Vock, P., et al. (1985). Endurance training in humans: aerobic capacity and structure of skeletal muscle. J. Appl. Physiol. 59, 320-327. doi: 10.1152/jappl.1985.59.2.320
75. Horowitz, J. F., Mora-Rodriguez, R., Byerley, L. O., and Coyle, E. F. (1997). Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am. J. Physiol. Endocrinol. Metab. 273, E768-E775. doi: 10.1152/ajpendo.1997.273.4.E768
76. Howald, H., Hoppeler, H., Claassen, H., Mathieu, O., and Straub, R. (1985). Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflug. Archiv. Eur. J. Physiol. 403, 369-376. doi: 10.1007/BF00589248
77. Hulston, C. J., Venables, M. C., Mann, C. H., Martin, C., Philp, A., Baar, K, et al. (2010). Training with low muscle glycogen enhances fat metabolism in well-trained cyclists. Med. Sci. Sports Exerc. 42, 2046-2055. doi: 10.1249/MSS.0b013e3181dd5070
78. Hultman, E. (1967). Physiological role of muscle glycogen in man, with special reference to exercise. Circ. Res. 20(3 Suppl. 1), I99-114
79. Hultman, E., and Bergström, J. (1967). Muscle glycogen synthesis in relation to diet studied in normal subjects. Acta Med. Scand. 182, 109-117. doi: 10.1111/j.0954-6820.1967.tb11504.x
80. Ipavec-Levasseur, S., Croci, I., Choquette, S., Byrne, N. M., Cowin, G., O'Moore-Sullivan, T. M., et al. (2015). Effect of 1-H moderate-intensity aerobic exercise on intramyocellular lipids in obese men before and after a lifestyle intervention. Appl. Physiol. Nutr. Metab. 40, 1262-1268. doi: 10.1139/apnm-2015-0258
81. Isacco, L., Thivel, D., Pereira, B., Duclos, M., and Boisseau, N. (2015). Maximal fat oxidation, but not aerobic capacity, is affected by oral contraceptive use in young healthy women. Eur. J. Appl. Physiol. 115, 937-945. doi: 10.1007/s00421-014-3075-7
82. Jensen, J., Rustad, P. I., Kolnes, A. J., and Lai, Y. C. (2011). The role of skeletal muscle glycogen breakdown for regulation of insulin sensitivity by exercise. Front. Physiol. 2:112. doi: 10.3389/fphys.2011.00112
83. Jeukendrup, A. E., and Wallis, G. A. (2005). Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int. J. Sports Med. 26(1 Suppl. 1), S28-37. doi: 10.1055/s-2004-830512
84. Knechtle, B., Müller, C., Willmann, F., Kotteck, K., Eser, P., and Knecht, H. (2004). Fat oxidation in men and women endurance athletes in running and cycling. Int. J. Sports Med. 25, 38-44. doi: 10.1055/s-2003-45232
85. Lambert, K. C., Aguer, M., Kitzmann, C., Fédou, C., Raynaud De Mauverger, E., et al. (2017). Whole-body lipid oxidation during exercise is correlated to insulin sensitivity and mitochondrial function in middle-aged obese men. Austin Diabetes Res. 2, 1-7
86. Lanzi, S., Codecasa, F., Cornacchia, M., Maestrini, S., Capodaglio, P., Brunani, A., et al. (2015). Short-term HIIT and fatmax training increase aerobic and metabolic fitness in men with class II, and III Obesity. Obesity 23, 1987-1994. doi: 10.1002/oby.21206
87. Lanzi, S., Codecasa, F., Cornacchia, M., Maestrini, S., Salvadori, A., Brunani, A., et al. (2014). Fat oxidation, hormonal and plasma metabolite kinetics during a submaximal incremental test in lean and obese adults. PLoS ONE 9:e88707. doi: 10.1371/journal.pone.0088707
88. Layden, D. D., Patterson, M. J., and Nimmo, M. A. (2002). Effects of reduced ambient temperature on fat utilization during submaximal exercise. Med. Sci. Sports Exerc. 34, 774-779. doi: 10.1097/00005768-200205000-00008
89. Lima-Silva, A. E., Bertuzzi, R. C. M., Pires, F. O., Gagliardi, J. F. L., Barros, R. V., Hammond, J., et al. (2010). Relationship between training status and maximal fat oxidation rate. J. Sports Sci. Med. 9, 31-35
90. Marchand, I., Tarnopolsky, M. A., Adamo, K. B., Bourgeois, J. M., Chorneyko, K., and Graham, T. E. (2007). Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise. J. Physiol. 580, 617-628. doi: 10.1113/jphysiol.2006.122457
91. Marzouki, H., Farhani, Z., Gmada, N., Tabka, Z., Shephard, R. J., and Bouhlel, E. (2014). Relative and absolute reliability of the crossover and maximum fat oxidation points during treadmill running. Sci. Sports 29, e107-e114. doi: 10.1016/j.scispo.2014.07.013
92. McBride, H. M., Neuspiel, M., and Wasiak, S. (2006). Mitochondria: more than just a powerhouse. Curr. Biol. 16, 551-560. doi: 10.1016/j.cub.2006.06.054
93. McCaig, R. H., and Gooderson, C. Y. (1986). Ergonomic and physiological aspects of military operations in a cold wet climate. Ergonomics 29, 849-857. doi: 10.1080/00140138608967197
94. McLaughlin, J. E., Howley, E. T., Bassett, D. R. Jr., Thompson, D. L., and Fitzhugh, E. C. (2010). Test of the classic model for predicting endurance running performance. Med. Sci. Sports Exerc. 42, 991-997. doi: 10.1249/MSS.0b013e3181c0669d
95. Meyer, C., Dostou, J. M., Welle, S. L., and Gerich, J. E. (2002). Role of human liver, kidney, and skeletal muscle in postprandial glucose homeostasis. Am. J. Physiol. Endocrinol. Metab. 282, E419-E427. doi: 10.1152/ajpendo.00032.2001
96. Meyer, T., Folz, C., Rosenberger, F., and Kindermann, W. (2009). The reliability of fatmax. Scandinav. J. Med. Sci. Sports 19, 213-221. doi: 10.1111/j.1600-0838.2008.00775.x
97. Mogensen, M., Vind, B. F., Højlund, K., Beck-Nielsen, H., and Sahlin, K. (2009). Maximal lipid oxidation in patients with Type 2 diabetes is normal and shows an adequate increase in response to aerobic training. Diabetes, Obes. Metab. 11, 874-883. doi: 10.1111/j.1463-1326.2009.01063.x
98. Mohebbi, H., Nourshahi, M., Ghasemikaram, M., and Safarimosavi, S. (2015). Effects of exercise at individual anaerobic threshold and maximal fat oxidation intensities on plasma levels of nesfatin-1 and metabolic health biomarkers. J. Physiol. Biochem. 71, 79-88. doi: 10.1007/s13105-015-0383-2
99. Montero, D., Cathomen, A., Jacobs, R. A., Flück, D., de Leur, J., Keiser, S., et al. (2015). Haematological rather than skeletal muscle adaptations contribute to the increase in peak oxygen uptake induced by moderate endurance training. J. Physiol. 593, 4677-4688. doi: 10.1113/JP270250
100. Mora-Rodríguez, R., Sanchez-Roncero, A., Fernández-Elías, V. E., Guadalupe-Grau, A., Ortega, J. F., Dela, F., et al. (2016). Aerobic exercise training increases muscle water content in obese middle-age men. Med. Sci. Sports Exerc. 48, 822-828. doi: 10.1249/MSS.0000000000000848
101. Nielsen, J., Cheng, A. J., Ørtenblad, N., and Westerblad, H. (2014). Subcellular distribution of glycogen and decreased tetanic Ca2+ in fatigued single intact mouse muscle fibres. J. Physiol. 592, 2003-2012. doi: 10.1113/jphysiol.2014.271528
102. Nielsen, J., Holmberg, H. C., Schrøder, H. D., Saltin, B., and Ørtenblad, N. (2011). Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J. Physiol. 589, 2871-2885. doi: 10.1113/jphysiol.2010.204487
103. Nielsen, J., Schrøder, H. D., Rix, C. G., and Ørtenblad, N. (2009). Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres. J. Physiol. 587, 3679-3690. doi: 10.1113/jphysiol.2009.174862
104. Nilsson, L. H. (1973). Liver glycogen content in man in the postabsorptive state. Scand. J. Clin. Lab. Invest. 32, 317-323. doi: 10.3109/00365517309084354
105. Nilsson, L. H., Fürst, P., and Hultman, E. (1973). Carbohydrate metabolism of the liver in normal man under varying dietary conditions. Scand. J. Clin. Lab. Invest. 32, 331-337. doi: 10.3109/00365517309084356
106. Nordby, P., Rosenkilde, M., Ploug, T., Westh, K., Feigh, M., Nielsen, N., et al. (2015). Independent effects of endurance training and weight loss on peak fat oxidation in moderately overweight men: a randomized controlled trial. J. Appl. Physiol. 118, 803-810. doi: 10.1152/japplphysiol.00715.2014
107. Nordby, P., Saltin, B., and Helge, J. W. (2006). Whole-body fat oxidation determined by graded exercise and indirect calorimetry: a role for muscle oxidative capacity? Scandinav. J. Med. Sci. Sports 16, 209-214. doi: 10.1111/j.1600-0838.2005.00480.x
108. Ørtenblad, N., Nielsen, J., Saltin, B., and Holmberg, H. C. (2011). Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J. Physiol. 589, 711-725. doi: 10.1113/jphysiol.2010.195982
109. Ørtenblad, N., Westerblad, H., and Nielsen, J. (2013). Muscle glycogen stores and fatigue. J. Physiol. 591, 4405-4413. doi: 10.1113/jphysiol.2013.251629
110. Oosthuyse, T., and Bosch, A. N. (2010). The effect of the menstrual cycle on exercise metabolism: implications for exercise performance in eumenorrhoeic women. Sports Med. 40, 207-227. doi: 10.2165/11317090-000000000-00000
111. Ørtenblad, N., and Nielsen, J. (2015). Muscle glycogen and cell function-location, location, location. Scandinav. J. Med. Sci. Sports 25(Suppl. 4), 34-40. doi: 10.1111/sms.12599
112. Orr, R. M., Johnston, V., Coyle, J., and Pope, R. (2015). Reported load carriage injuries of the australian army soldier. J. Occupat. Rehab. 25 (2). Springer US: 316-22
113. Oz, G., Henry, P. G., Seaquist, E. R., and Gruetter, R. (2003). Direct, noninvasive measurement of brain glycogen metabolism in humans. Neurochem. Int. 43, 323-329. doi: 10.1016/S0197-0186(03)00019-6
114. Parkin, J. M., Carey, M. F., Zhao, S., and Febbraio, M. A. (1999). Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J. Appl. Physiol. 86, 902-908. doi: 10.1152/jappl.1999.86.3.902
115. Pérez-Martin, A., Dumortier, M., Raynaud, E., Brun, J. F., Fédou, C., Bringer, J., et al. (2001). Balance of substrate oxidation during submaximal exercise in lean and obese people. Diabetes Metab. 27, 466-74
116. Perry, C. G. R., Heigenhauser, G. J. F., Bonen, A., and Spriet, L. L. (2008). High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl. Physiol. Nutr. Metab. 33, 1112-1123. doi: 10.1139/H08-097
117. Phinney, S. D., Bistrian, B. R., Evans, W. J., Gervino, E., and Blackburn, G. L. (1983). The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metab. Clin. Exp. 32, 769-776. doi: 10.1016/0026-0495(83)90106-3
118. Purdom, T., Kravitz, L., Dokladny, K., and Mermier, C. (2018). Understanding the factors that effect maximal fat oxidation. J. Int. Soc. Sports Nutr. 15:3. doi: 10.1186/s12970-018-0207-1
119. Racinais, S., Alonso, J. M., Coutts, A. J., Flouris, A. D., Girard, O., González-Alonso, J., et al. (2015). Consensus recommendations on training and competing in the heat. Br. J. Sports Med. 49, 1164-1173. doi: 10.1136/bjsports-2015-094915
120. Randell, R. K., Rollo, I., Roberts, T. J., Dalrymple, K. J., Jeukendrup, A. E., and Carter, J. M. (2017). Maximal fat oxidation rates in an athletic population. Med. Sci. Sports Exerc. 49, 133-140. doi: 10.1249/MSS.0000000000001084
121. Rigden, D. J., Jellyman, A. E., Frayn, K. N., and Coppack, S. W. (1990). Human adipose tissue glycogen levels and responses to carbohydrate feeding. Eur. J. Clin. Nutr. 44, 689-92
122. Robinson, S. L., Hattersley, J., Frost, G. S., Chambers, E. S., and Wallis, G. A. (2015). Maximal fat oxidation during exercise is positively associated with 24-hour fat oxidation and insulin sensitivity in young, healthy men. J. Appl. Physiol. 118, 1415-1422. doi: 10.1152/japplphysiol.00058.2015
123. Romijn, J. A., Coyle, E. F., Sidossis, L. S., Zhang, X. J., and Wolfe, R. R. (1995). Relationship between fatty acid delivery and fatty acid oxidation during strenuous exercise. J. Appl. Physiol. 79, 1939-1945. doi: 10.1152/jappl.1995.79.6.1939
124. Romijn, J. A., Gastaldelli, A., Horowitz, J. F., Endert, E., and Wolfe, R. R. (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am. J. Physiol. Endocrinol. Metab. 265, 380-391. doi: 10.1152/ajpendo.1993.265.3.E380
125. Rosenkilde, M. P., Nordby, L. B., Nielsen, B. M., and Stallknecht Helge, J. W. (2010). Fat oxidation at rest predicts peak fat oxidation during exercise and metabolic phenotype in overweight men. Int. J. Obes. 34, 871-77. doi: 10.1038/ijo.2010.11
126. Rosenkilde, M., Reichkendler, M. H., Auerbach, P., Bonne, T. C., Sjödin, A., Ploug, T., et al. (2015). Changes in peak fat oxidation in response to different doses of endurance training. Scandinav. J. Med. Sci. Sports 25, 41-52. doi: 10.1111/sms.12151
127. Ross, R., Blair, S. N., Arena, R., Church, T. S., Després, J. P., Franklin, B. A., et al. (2016). Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the american heart association. Circulation 134. e653-e699. doi: 10.1161/CIR.0000000000000461
128. Sahlin, K., Harris, R. C., Nylind, B., and Hultman, E. (1976). Lactate Content and pH in muscle samples obtained after dynamic exercise. Pflugers Archiv. Eur. J. Physiol. 367, 143-149. doi: 10.1007/BF00585150
129. Sahlin, K. M., Mogensen, M., Bagger, M., and Fernstro, Pedersen P. K. (2007). The potential for mitochondrial fat oxidation in human skeletal muscle influences whole body fat oxidation during low-intensity exercise. Am. J. Physiol. 292, E223-E230. doi: 10.1152/ajpendo.00266.2006
130. Scalzo, R. L., Peltonen, G. L., Binns, S. E., Shankaran, M., Giordano, G. R., Hartley, D. A., et al. (2014). Greater muscle protein synthesis and mitochondrial biogenesis in males compared with females during sprint interval training. FASEB J. 28, 2705-2714. doi: 10.1096/fj.13-246595
131. Schubert, M. M., Clarke, H. E., Seay, R. F., and Spain, K. K. (2017). Impact of 4 weeks of interval training on resting metabolic rate, fitness, and health-related outcomes. Appl. Physiol. Nutr. Metab. 42, 1073-1081. doi: 10.1139/apnm-2017-0268
132. Schwindling, S., Kindermann, W., and Meyer, T. (2014). Limited benefit of fatmax-test to derive training prescriptions. Int. J. Sports Med. 35, 280-285. doi: 10.1055/s-0033-1349106
133. Sidossis, L. S., Gastaldelli, A., Klein, S., and Wolfe, R. R. (1997). Regulation of Plasma Fatty Acid Oxidation during Low-and High-Intensity Exercise. Am. J. Physiol. 272, E1065-E1070. doi: 10.1152/ajpendo.1997.272.6.E1065
134. Snyder, A. C., O'Hagan, K. P., Clifford, P. S., Hoffmann, M. D., and Foster, C. (1993). Exercise responses to in-line skating: comparisons to running and cycling. Int. J. Sports Med. 14, 38-42. doi: 10.1055/s-2007-1021143
135. Soenen, S., Plasqui, G., Smeets, A. J., and Westerterp-Plantenga, M. S. (2010). Protein intake induced an increase in exercise stimulated fat oxidation during stable body weight. Physiol. Behav. 101, 770-774. doi: 10.1016/j.physbeh.2010.08.019
136. Spina, R. J., Chi, M. M., Hopkins, M. G., Nemeth, P. M., Lowry, O. H., and Holloszy, J. O. (1996). Mitochondrial enzymes increase in muscle in response to 7-10 days of cycle exercise. J. Appl. Physiol. 80, 2250-2254. doi: 10.1152/jappl.1996.80.6.2250
137. Spriet, L. L. (2014). New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 44(Suppl. 1), 87-96. doi: 10.1007/s40279-014-0154-1
138. Starkie, R. L., Hargreaves, M., Lambert, D. L., Proietto, J., and Febbraio, M. A. (1999). Effects of temperature on muscle metabolism during submaximal exercise in humans. Exp. Physiol. 84, 775-784. doi: 10.1111/j.1469-445X.1999.01815.x
139. Starritt, E. C., Howlett, R. A., Heigenhauser, G. J. F., and Spriet, L. L. (2000). Sensitivity of CPT I to malonyl-CoA in trained and untrained human skeletal muscle. Am. J. Physiol. 278, E462-E468. doi: 10.1152/ajpendo.2000.278.3.E462
140. Stisen, A. B., Stougaard, O., Langfort, J., Helge, J. W., Sahlin, K., and Madsen, K. (2006). Maximal fat oxidation rates in endurance trained and untrained women. Eur. J. Appl. Physiol. 98, 497-506. doi: 10.1007/s00421-006-0290-x
141. Talanian, J. L., Galloway, S. D. R., Heigenhauser, G. J. F., Bonen, A., and Spriet, L. L. (2007). Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J. Appl. Physiol. 102, 1439-1447. doi: 10.1152/japplphysiol.01098.2006
142. Talanian, J. L., Holloway, G. P., Snook, L. A., Heigenhauser, G. J. F., Bonen, A., and Spriet, L. L. (2010). Exercise training increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am. J. Physiol. 299, E180-E188. doi: 10.1152/ajpendo.00073.2010
143. Tan, S., Wang, J., Cao, L., Guo, Z., and Wang, Y. (2016). Positive effect of exercise training at maximal fat oxidation intensity on body composition and lipid metabolism in overweight middle-aged women. Clin. Physiol. Funct. Imaging 36, 225-230. doi: 10.1111/cpf.12217
144. Tolfrey, K., Jeukendrup, A. E., and Batterham, A. M. (2010). Group-and individual-level coincidence of the "Fatmax" and lactate accumulation in adolescents. Eur. J. Appl. Physiol. 109, 1145-1153. doi: 10.1007/s00421-010-1453-3
145. Tsujimoto, T., Sasai, H., Miyashita, M., Eto, M., So, R., Ohkubo, H., et al. (2012). Effect of weight loss on maximal fat oxidation rate in obese men. Obesity Research and Clinical Practice 6 (2). Asia Oceania Assoc. for the Study of Obesity: e111-19
146. van Loon, L. J. C., Greenhaff, P. L., Constantin-Teodosiu, D., Saris, W. H. M., and Wagenmakers, A. J. M. (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. J. Physiol. 536, 295-304. doi: 10.1111/j.1469-7793.2001.00295.x
147. van Loon, L. J. C., Jeukendrup, A. E., Saris, W. H., and Wagenmakers, A. J. (1999). Effect of training status on fuel selection during submaximal exercise with glucose ingestion. J. Appl. Physiol. 87, 1413-1420. doi: 10.1152/jappl.1999.87.4.1413
148. Venables, M. C., Achten, J., and Jeukendrup, A. E. (2005). Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J. Appl. Physiol. 98, 160-167. doi: 10.1152/japplphysiol.00662.2003
149. Venables, M. C., and Jeukendrup, A. E. (2008). Endurance training and obesity: effect on substrate metabolism and insulin sensitivity. Med. Sci. Sports Exerc. 40, 495-502. doi: 10.1249/MSS.0b013e31815f256f
150. Volek, J. S., Freidenreich, D. J., Saenz, C., Kunces, L. J., Creighton, B. C., Bartley, J. M., et al. (2016). Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism 65, 100-110. doi: 10.1016/j.metabol.2015.10.028
151. Wang, C. H., Wang, C. C., and Wei, Y. H. (2010). Mitochondrial dysfunction in insulin insensitivity: implication of mitochondrial role in type 2 diabetes. Ann. N. Y. Acad. Sci. U.S.A. 1201, 157-165. doi: 10.1111/j.1749-6632.2010.05625.x
152. Wasserman, D. H. (2009). Four Grams of Glucose. Am. J. Physiol. 296, E11-E21. doi: 10.1152/ajpendo.90563.2008
153. Webster, C. C., Noakes, T. D., Chacko, S. K., Swart, J., Kohn, T. A., and Smith, J. A. H. (2016). Gluconeogenesis during endurance exercise in cyclists habituated to a long-term low carbohydrate high-fat diet. J. Physiol. 594, 4389-4405. doi: 10.1113/JP271934
154. Wu, Y. T., Wu, S. B., and Wei, Y. H. (2014). Metabolic reprogramming of human cells in response to oxidative stress: implications in the pathophysiology and therapy of mitochondrial diseases. Curr. Pharm. Des. 20, 5510-5526. doi: 10.2174/1381612820666140306103401
155. Yeo, W. K., Paton, C. D., Garnham, A. P., Burke, L. M., Carey, A. L., and Hawley, J. A. (2008). Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. J. Appl. Physiol. 105, 1462-1470. doi: 10.1152/japplphysiol.90882.2008
156. Zurlo, F., Lillioja, S. A., Esposito-Del Puente, A., Nyomba, B. L., Raz, I., Saad, M. F., et al. (1990). Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-H RQ. Am. J. Physiol. 259, E650-E657. doi: 10.1152/ajpendo.1990.259.5.E650