Early Time-Restricted Feeding Improves 24-Hour Glucose Levels and Affects Markers of the Circadian Clock, Aging, and Autophagy in Humans
Abstract
1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Study Design
2.3. Continuous Glucose Monitoring
2.4. Serum Chemistry
2.5. Gene Expression
2.6. Statistical Methods
3. Results
3.1. Participant Characteristics
3.2. 24-Hour Glucose Levels
3.3. Glycemic Markers
3.4. Lipids
3.5. Hormones
3.6. Gene Expression
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Mattson, M.P.; Longo, V.D.; Harvie, M. Impact of intermittent fasting on health and disease processes. Ageing Res. Rev. 2017, 39, 46–58. [Google Scholar] [CrossRef] [PubMed]
- Harvie, M.; Howell, A. Potential Benefits and Harms of Intermittent Energy Restriction and Intermittent Fasting Amongst Obese, Overweight and Normal Weight Subjects-A Narrative Review of Human and Animal Evidence. Behav. Sci. 2017, 7, 4. [Google Scholar] [CrossRef]
- Tinsley, G.M.; Horne, B.D. Intermittent fasting and cardiovascular disease: Current evidence and unresolved questions. Fut. Cardiol. 2018, 14, 47–54. [Google Scholar] [CrossRef] [PubMed]
- Patterson, R.E.; Sears, D.D. Metabolic Effects of Intermittent Fasting. Annu. Rev. Nutr. 2017, 37, 371–393. [Google Scholar] [CrossRef] [PubMed]
- Antoni, R.; Johnston, K.L.; Collins, A.L.; Robertson, M.D. Effects of intermittent fasting on glucose and lipid metabolism. Proc. Nutr. Soc. 2017, 76(3), 361–368. [Google Scholar] [CrossRef]
- Longo, V.D.; Mattson, M.P. Fasting: Molecular mechanisms and clinical applications. Cell Metab. 2014, 19, 181–192. [Google Scholar] [CrossRef]
- Anton, S.D.; Moehl, K.; Donahoo, W.T.; Marosi, K.; Lee, S.A.; Mainous, A.G., 3rd; Leeuwenburgh, C.; Mattson, M.P. Flipping the Metabolic Switch: Understanding and Applying the Health Benefits of Fasting. Obesity 2018, 26, 254–268. [Google Scholar] [CrossRef]
- Cioffi, I.; Evangelista, A.; Ponzo, V.; Ciccone, G.; Soldati, L.; Santarpia, L.; Contaldo, F.; Pasanisi, F.; Ghigo, E.; Bo, S. Intermittent versus continuous energy restriction on weight loss and cardiometabolic outcomes: A systematic review and meta-analysis of randomized controlled trials. J. Transl. Med. 2018, 16, 371. [Google Scholar] [CrossRef]
- Seimon, R.V.; Roekenes, J.A.; Zibellini, J.; Zhu, B.; Gibson, A.A.; Hills, A.P.; Wood, R.E.; King, N.A.; Byrne, N.M.; Sainsbury, A. Do intermittent diets provide physiological benefits over continuous diets for weight loss? A systematic review of clinical trials. Mol. Cell Endocrinol. 2015, 418, 153–172. [Google Scholar] [CrossRef]
- Hatori, M.; Vollmers, C.; Zarrinpar, A.; DiTacchio, L.; Bushong, E.A.; Gill, S.; Leblanc, M.; Chaix, A.; Joens, M.; Fitzpatrick, J.A.; et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 2012, 15, 848–860. [Google Scholar] [CrossRef]
- Zarrinpar, A.; Chaix, A.; Yooseph, S.; Panda, S. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 2014, 20, 1006–1017. [Google Scholar] [CrossRef] [PubMed]
- Sherman, H.; Genzer, Y.; Cohen, R.; Chapnik, N.; Madar, Z.; Froy, O. Timed high-fat diet resets circadian metabolism and prevents obesity. FASEB J. 2012, 26, 3493–3502. [Google Scholar] [CrossRef] [PubMed]
- Wu, T.; Sun, L.; ZhuGe, F.; Guo, X.; Zhao, Z.; Tang, R.; Chen, Q.; Chen, L.; Kato, H.; Fu, Z. Differential roles of breakfast and supper in rats of a daily three-meal schedule upon circadian regulation and physiology. Chronobiol. Int. 2011, 28, 890–903. [Google Scholar] [CrossRef] [PubMed]
- Olsen, M.K.; Choi, M.H.; Kulseng, B.; Zhao, C.M.; Chen, D. Time-restricted feeding on weekdays restricts weight gain: A study using rat models of high-fat diet-induced obesity. Physiol. Behav. 2017, 173, 298–304. [Google Scholar] [CrossRef]
- Chaix, A.; Lin, T.; Le, H.D.; Chang, M.W.; Panda, S. Time-Restricted Feeding Prevents Obesity and Metabolic Syndrome in Mice Lacking a Circadian Clock. Cell Metab. 2019, 29, 303–319. [Google Scholar] [CrossRef] [PubMed]
- Cote, I.; Toklu, H.Z.; Green, S.M.; Morgan, D.; Carter, C.S.; Tumer, N.; Scarpace, P.J. Limiting feeding to the active phase reduces blood pressure without the necessity of caloric reduction or fat mass loss. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2018, 315, R751–R758. [Google Scholar] [CrossRef]
- Delahaye, L.B.; Bloomer, R.J.; Butawan, M.B.; Wyman, J.M.; Hill, J.L.; Lee, H.W.; Liu, A.C.; McAllan, L.; Han, J.C.; van der Merwe, M. Time-restricted feeding of a high-fat diet in male C57BL/6 mice reduces adiposity but does not protect against increased systemic inflammation. Appl. Physiol. Nutr. Metab. 2018, 43, 1033–1042. [Google Scholar] [CrossRef] [PubMed]
- Sutton, E.F.; Beyl, R.; Early, K.S.; Cefalu, W.T.; Ravussin, E.; Peterson, C.M. Early Time-Restricted Feeding Improves Insulin Sensitivity, Blood Pressure, and Oxidative Stress Even without Weight Loss in Men with Prediabetes. Cell Metab. 2018, 27, 1212–1221. [Google Scholar] [CrossRef] [PubMed]
- Ravussin, E.; Beyl, R.A.; Poggiogalle, E.; Hsia, D.S.; Peterson, C.M. Early Time-Restricted Feeding Reduces Appetite and Increases Fat Oxidation but Does Not Affect Energy Expenditure in Humans. Obesity 2019, in press. [Google Scholar]
- Kant, A.K.; Graubard, B.I. Association of self-reported sleep duration with eating behaviors of American adults: NHANES 2005–2010. Am. J. Clin. Nutr. 2014, 100, 938–947. [Google Scholar] [CrossRef] [PubMed]
- Belkacemi, L.; Selselet-Attou, G.; Louchami, K.; Sener, A.; Malaisse, W.J. Intermittent fasting modulation of the diabetic syndrome in sand rats. II. In vivo investigations. Int. J. Mol. Med. 2010, 26, 759–765. [Google Scholar]
- Sherman, H.; Frumin, I.; Gutman, R.; Chapnik, N.; Lorentz, A.; Meylan, J.; le Coutre, J.; Froy, O. Long-term restricted feeding alters circadian expression and reduces the level of inflammatory and disease markers. J. Cell. Mol. Med. 2011, 15, 2745–2759. [Google Scholar] [CrossRef]
- Belkacemi, L.; Selselet-Attou, G.; Bulur, N.; Louchami, K.; Sener, A.; Malaisse, W.J. Intermittent fasting modulation of the diabetic syndrome in sand rats. III. Post-mortem investigations. Int. J. Mol. Med. 2011, 27, 95–102. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Duncan, M.J.; Smith, J.T.; Narbaiza, J.; Mueez, F.; Bustle, L.B.; Qureshi, S.; Fieseler, C.; Legan, S.J. Restricting feeding to the active phase in middle-aged mice attenuates adverse metabolic effects of a high-fat diet. Physiol. Behav. 2016, 167, 1–9. [Google Scholar] [CrossRef]
- Sundaram, S.; Yan, L. Time-restricted feeding reduces adiposity in mice fed a high-fat diet. Nutr. Res. 2016, 36, 603–611. [Google Scholar] [CrossRef]
- Chung, H.; Chou, W.; Sears, D.D.; Patterson, R.E.; Webster, N.J.; Ellies, L.G. Time-restricted feeding improves insulin resistance and hepatic steatosis in a mouse model of postmenopausal obesity. Metabolism 2016, 65, 1743–1754. [Google Scholar] [CrossRef] [PubMed]
- Philippens, K.M.; von Mayersbach, H.; Scheving, L.E. Effects of the scheduling of meal-feeding at different phases of the circadian system in rats. J. Nutr. 1977, 107, 176–193. [Google Scholar] [CrossRef]
- Kudo, T.; Akiyama, M.; Kuriyama, K.; Sudo, M.; Moriya, T.; Shibata, S. Night-time restricted feeding normalises clock genes and Pai-1 gene expression in the db/db mouse liver. Diabetologia 2004, 47, 1425–1436. [Google Scholar] [CrossRef] [PubMed]
- Manzanero, S.; Erion, J.R.; Santro, T.; Steyn, F.J.; Chen, C.; Arumugam, T.V.; Stranahan, A.M. Intermittent fasting attenuates increases in neurogenesis after ischemia and reperfusion and improves recovery. J. Cereb. Blood Flow Metab. 2014, 34, 897–905. [Google Scholar] [CrossRef]
- Garcia-Luna, C.; Soberanes-Chavez, P.; de Gortari, P. Prepuberal light phase feeding induces neuroendocrine alterations in adult rats. J. Endocrinol. 2017, 232, 15–28. [Google Scholar] [CrossRef]
- Park, S.; Yoo, K.M.; Hyun, J.S.; Kang, S. Intermittent fasting reduces body fat but exacerbates hepatic insulin resistance in young rats regardless of high protein and fat diets. J. Nutr. Biochem. 2017, 40, 14–22. [Google Scholar] [CrossRef]
- Belkacemi, L.; Selselet-Attou, G.; Hupkens, E.; Nguidjoe, E.; Louchami, K.; Sener, A.; Malaisse, W.J. Intermittent fasting modulation of the diabetic syndrome in streptozotocin-injected rats. Int. J. Endocrinol. 2012, 2012, 962012. [Google Scholar] [CrossRef]
- Chaix, A.; Zarrinpar, A.; Miu, P.; Panda, S. Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab. 2014, 20, 991–1005. [Google Scholar] [CrossRef]
- Mitchell, S.J.; Bernier, M.; Mattison, J.A.; Aon, M.A.; Kaiser, T.A.; Anson, R.M.; Ikeno, Y.; Anderson, R.M.; Ingram, D.K.; de Cabo, R. Daily Fasting Improves Health and Survival in Male Mice Independent of Diet Composition and Calories. Cell Metab. 2019, 29, 221–228. [Google Scholar] [CrossRef]
- Smith, N.J.; Caldwell, J.L.; van der Merwe, M.; Sharma, S.; Butawan, M.; Puppa, M.; Bloomer, R.J. A Comparison of Dietary and Caloric Restriction Models on Body Composition, Physical Performance, and Metabolic Health in Young Mice. Nutrients 2019, 11(2), 350. [Google Scholar] [CrossRef]
- Sun, S.; Hanzawa, F.; Umeki, M.; Ikeda, S.; Mochizuki, S.; Oda, H. Time-restricted feeding suppresses excess sucrose-induced plasma and liver lipid accumulation in rats. PLoS ONE 2018, 13, e0201261. [Google Scholar] [CrossRef]
- Woodie, L.N.; Luo, Y.; Wayne, M.J.; Graff, E.C.; Ahmed, B.; O’Neill, A.M.; Greene, M.W. Restricted feeding for 9h in the active period partially abrogates the detrimental metabolic effects of a Western diet with liquid sugar consumption in mice. Metabolism 2018, 82, 1–13. [Google Scholar] [CrossRef]
- Sundaram, S.; Yan, L. Time-restricted feeding mitigates high-fat diet-enhanced mammary tumorigenesis in MMTV-PyMT mice. Nutr. Res. 2018, 59, 72–79. [Google Scholar] [CrossRef] [PubMed]
- Li, X.M.; Delaunay, F.; Dulong, S.; Claustrat, B.; Zampera, S.; Fujii, Y.; Teboul, M.; Beau, J.; Levi, F. Cancer inhibition through circadian reprogramming of tumor transcriptome with meal timing. Cancer Res. 2010, 70, 3351–3360. [Google Scholar] [CrossRef] [PubMed]
- Wu, M.W.; Li, X.M.; Xian, L.J.; Levi, F. Effects of meal timing on tumor progression in mice. Life Sci. 2004, 75, 1181–1193. [Google Scholar] [CrossRef] [PubMed]
- Gabel, K.; Hoddy, K.K.; Haggerty, N.; Song, J.; Kroeger, C.M.; Trepanowski, J.F.; Panda, S.; Varady, K.A. Effects of 8-hour time restricted feeding on body weight and metabolic disease risk factors in obese adults: A pilot study. Nutr. Healthy Aging 2018, 4, 345–353. [Google Scholar] [CrossRef] [PubMed]
- Antoni, R.; Robertson, T.M.; Robertson, M.; Johnston, J. A pilot feasibility study exploring the effects of a moderate time-restricted feeding intervention on energy intake, adiposity and metabolic physiology in free-living human subjects. J. Nutr. Sci. 2018, 7, 1–6. [Google Scholar] [CrossRef]
- Gasmi, M.; Sellami, M.; Denham, J.; Padulo, J.; Kuvacic, G.; Selmi, W.; Khalifa, R. Time-restricted feeding influences immune responses without compromising muscle performance in older men. Nutrition 2018, 51–52, 29–37. [Google Scholar] [CrossRef] [PubMed]
- Moro, T.; Tinsley, G.; Bianco, A.; Marcolin, G.; Pacelli, Q.F.; Battaglia, G.; Palma, A.; Gentil, P.; Neri, M.; Paoli, A. Effects of eight weeks of time-restricted feeding (16/8) on basal metabolism, maximal strength, body composition, inflammation, and cardiovascular risk factors in resistance-trained males. J. Transl. Med. 2016, 14, 290. [Google Scholar] [CrossRef] [PubMed]
- Gill, S.; Panda, S. A Smartphone App Reveals Erratic Diurnal Eating Patterns in Humans that Can Be Modulated for Health Benefits. Cell Metab. 2015, 22, 789–798. [Google Scholar] [CrossRef]
- Tinsley, G.M.; Forsse, J.S.; Butler, N.K.; Paoli, A.; Bane, A.A.; La Bounty, P.M.; Morgan, G.B.; Grandjean, P.W. Time-restricted feeding in young men performing resistance training: A randomized controlled trial. Eur. J. Sport Sci. 2017, 17, 200–207. [Google Scholar] [CrossRef]
- Stote, K.S.; Baer, D.J.; Spears, K.; Paul, D.R.; Harris, G.K.; Rumpler, W.V.; Strycula, P.; Najjar, S.S.; Ferrucci, L.; Ingram, D.K.; et al. A controlled trial of reduced meal frequency without caloric restriction in healthy, normal-weight, middle-aged adults. Am. J. Clin. Nutr. 2007, 85, 981–988. [Google Scholar] [CrossRef]
- Carlson, O.; Martin, B.; Stote, K.S.; Golden, E.; Maudsley, S.; Najjar, S.S.; Ferrucci, L.; Ingram, D.K.; Longo, D.L.; Rumpler, W.V.; et al. Impact of reduced meal frequency without caloric restriction on glucose regulation in healthy, normal-weight middle-aged men and women. Metabolism 2007, 56, 1729–1734. [Google Scholar] [CrossRef]
- Poggiogalle, E.; Jamshed, H.; Peterson, C.M. Circadian regulation of glucose, lipid, and energy metabolism in humans. Metabolism 2018, 84, 11–27. [Google Scholar] [CrossRef]
- Dallmann, R.; Viola, A.U.; Tarokh, L.; Cajochen, C.; Brown, S.A. The human circadian metabolome. Proc. Natl. Acad. Sci. USA 2012, 109, 2625–2629. [Google Scholar] [CrossRef]
- Gamble, K.L.; Berry, R.; Frank, S.J.; Young, M.E. Circadian clock control of endocrine factors. Nat. Rev. Endocrinol. 2014, 10, 466–475. [Google Scholar] [CrossRef]
- Tsang, A.H.; Astiz, M.; Friedrichs, M.; Oster, H. Endocrine regulation of circadian physiology. J. Endocrinol. 2016, 230, R1–R11. [Google Scholar] [CrossRef] [PubMed]
- Rabinovitz, H.R.; Boaz, M.; Ganz, T.; Jakubowicz, D.; Matas, Z.; Madar, Z.; Wainstein, J. Big breakfast rich in protein and fat improves glycemic control in type 2 diabetics. Obesity 2014, 22, E46–E54. [Google Scholar] [CrossRef] [PubMed]
- Jakubowicz, D.; Barnea, M.; Wainstein, J.; Froy, O. High caloric intake at breakfast vs. dinner differentially influences weight loss of overweight and obese women. Obesity 2013, 21, 2504–2512. [Google Scholar] [CrossRef]
- Reid, K.J.; Baron, K.G.; Zee, P.C. Meal timing influences daily caloric intake in healthy adults. Nutr. Res. 2014, 34, 930–935. [Google Scholar] [CrossRef]
- Ruiz-Lozano, T.; Vidal, J.; de Hollanda, A.; Scheer, F.A.; Garaulet, M.; Izquierdo-Pulido, M. Timing of food intake is associated with weight loss evolution in severe obese patients after bariatric surgery. Clin. Nutr. 2016, 35, 1308–1314. [Google Scholar] [CrossRef]
- Garaulet, M.; Gomez-Abellan, P.; Alburquerque-Bejar, J.J.; Lee, Y.C.; Ordovas, J.M.; Scheer, F.A. Timing of food intake predicts weight loss effectiveness. Int. J. Obes. 2013, 37, 604–611. [Google Scholar] [CrossRef]
- Keim, N.L.; Van Loan, M.D.; Horn, W.F.; Barbieri, T.F.; Mayclin, P.L. Weight loss is greater with consumption of large morning meals and fat-free mass is preserved with large evening meals in women on a controlled weight reduction regimen. J. Nutr. 1997, 127, 75–82. [Google Scholar] [CrossRef] [PubMed]
- Scheer, F.A.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA 2009, 106, 4453–4458. [Google Scholar] [CrossRef] [PubMed]
- Wefers, J.; van Moorsel, D.; Hansen, J.; Connell, N.J.; Havekes, B.; Hoeks, J.; van Marken Lichtenbelt, W.D.; Duez, H.; Phielix, E.; Kalsbeek, A.; et al. Circadian misalignment induces fatty acid metabolism gene profiles and compromises insulin sensitivity in human skeletal muscle. Proc. Natl. Acad. Sci. USA 2018, 115, 7789–7794. [Google Scholar] [CrossRef]
- Morris, C.J.; Purvis, T.E.; Hu, K.; Scheer, F.A. Circadian misalignment increases cardiovascular disease risk factors in humans. Proc. Natl. Acad. Sci. USA 2016, 113, E1402–E1411. [Google Scholar] [CrossRef] [PubMed]
- Morris, C.J.; Yang, J.N.; Garcia, J.I.; Myers, S.; Bozzi, I.; Wang, W.; Buxton, O.M.; Shea, S.A.; Scheer, F.A. Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proc. Natl. Acad. Sci. USA 2015, 112, E2225–E2234. [Google Scholar] [CrossRef] [PubMed]
- EasyGV. Available online: https://www.phc.ox.ac.uk/research/technology-outputs/easygv (accessed on 13 December 2018).
- Van Cauter, E.; Polonsky, K.S.; Scheen, A.J. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr. Rev. 1997, 18, 716–738. [Google Scholar] [CrossRef]
- Hibi, M.; Masumoto, A.; Naito, Y.; Kiuchi, K.; Yoshimoto, Y.; Matsumoto, M.; Katashima, M.; Oka, J.; Ikemoto, S. Nighttime snacking reduces whole body fat oxidation and increases LDL cholesterol in healthy young women. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 304, R94–R101. [Google Scholar] [CrossRef]
- Choi, H.R.; Kim, J.; Lim, H.; Park, Y.K. Two-Week Exclusive Supplementation of Modified Ketogenic Nutrition Drink Reserves Lean Body Mass and Improves Blood Lipid Profile in Obese Adults: A Randomized Clinical Trial. Nutrients 2018, 10(11), 1895. [Google Scholar] [CrossRef] [PubMed]
- Jakubowicz, D.; Wainstein, J.; Landau, Z.; Raz, I.; Ahren, B.; Chapnik, N.; Ganz, T.; Menaged, M.; Barnea, M.; Bar-Dayan, Y. Influences of Breakfast on Clock Gene Expression and Postprandial Glycemia in Healthy Individuals and Individuals With Diabetes: A Randomized Clinical Trial. Diabetes Care 2017, 40, 1573–1579. [Google Scholar] [CrossRef]
- Rahman, S.; Islam, R. Mammalian Sirt1: Insights on its biological functions. Cell Commun. Signal 2011, 9, 11. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Lopez, N.; Tarabra, E.; Toledo, M.; Garcia-Macia, M.; Sahu, S.; Coletto, L.; Batista-Gonzalez, A.; Barzilai, N.; Pessin, J.E.; Schwartz, G.J.; et al. System-wide Benefits of Intermeal Fasting by Autophagy. Cell Metab. 2017, 26, 856–871.e855. [Google Scholar] [CrossRef]
- Mani, K.; Javaheri, A.; Diwan, A. Lysosomes Mediate Benefits of Intermittent Fasting in Cardiometabolic Disease: The Janitor Is the Undercover Boss. Compr. Physiol. 2018, 8, 1639–1667. [Google Scholar] [CrossRef]
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Jamshed, H.; Beyl, R.A.; Della Manna, D.L.; Yang, E.S.; Ravussin, E.; Peterson, C.M. Early Time-Restricted Feeding Improves 24-Hour Glucose Levels and Affects Markers of the Circadian Clock, Aging, and Autophagy in Humans. Nutrients 2019, 11, 1234. https://doi.org/10.3390/nu11061234
Jamshed H, Beyl RA, Della Manna DL, Yang ES, Ravussin E, Peterson CM. Early Time-Restricted Feeding Improves 24-Hour Glucose Levels and Affects Markers of the Circadian Clock, Aging, and Autophagy in Humans. Nutrients. 2019; 11(6):1234. https://doi.org/10.3390/nu11061234
Chicago/Turabian StyleJamshed, Humaira, Robbie A. Beyl, Deborah L. Della Manna, Eddy S. Yang, Eric Ravussin, and Courtney M. Peterson. 2019. "Early Time-Restricted Feeding Improves 24-Hour Glucose Levels and Affects Markers of the Circadian Clock, Aging, and Autophagy in Humans" Nutrients 11, no. 6: 1234. https://doi.org/10.3390/nu11061234
APA StyleJamshed, H., Beyl, R. A., Della Manna, D. L., Yang, E. S., Ravussin, E., & Peterson, C. M. (2019). Early Time-Restricted Feeding Improves 24-Hour Glucose Levels and Affects Markers of the Circadian Clock, Aging, and Autophagy in Humans. Nutrients, 11(6), 1234. https://doi.org/10.3390/nu11061234