A time to fast

· Science

18 min read Original article ↗

Abstract

Nutrient composition and caloric intake have traditionally been used to devise optimized diets for various phases of life. Adjustment of meal size and frequency have emerged as powerful tools to ameliorate and postpone the onset of disease and delay aging, whereas periods of fasting, with or without reduced energy intake, can have profound health benefits. The underlying physiological processes involve periodic shifts of metabolic fuel sources, promotion of repair mechanisms, and the optimization of energy utilization for cellular and organismal health. Future research endeavors should be directed to the integration of a balanced nutritious diet with controlled meal size and patterns and periods of fasting to develop better strategies to prevent, postpone, and treat the socioeconomical burden of chronic diseases associated with aging.

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References and Notes

1

World Health Organization (WHO), “World health statistics 2018: Monitoring health for the SDGs” (WHO Report, WHO, 2018).

2

M. P. Mattson, D. B. Allison, L. Fontana, M. Harvie, V. D. Longo, W. J. Malaisse, M. Mosley, L. Notterpek, E. Ravussin, F. A. J. L. Scheer, T. N. Seyfried, K. A. Varady, S. Panda, Meal frequency and timing in health and disease. Proc. Natl. Acad. Sci. U.S.A. 111, 16647–16653 (2014). 10.1073/pnas.1413965111

3

S. Panda, Circadian physiology of metabolism. Science 354, 1008–1015 (2016). 10.1126/science.aah4967

4

J. R. Speakman, S. E. Mitchell, Caloric restriction. Mol. Aspects Med. 32, 159–221 (2011). 10.1016/j.mam.2011.07.001

5

C. Y. Liao, B. A. Rikke, T. E. Johnson, V. Diaz, J. F. Nelson, Genetic variation in the murine lifespan response to dietary restriction: From life extension to life shortening. Aging Cell 9, 92–95 (2010). 10.1111/j.1474-9726.2009.00533.x

6

R. L. Walford, D. Mock, R. Verdery, T. MacCallum, Calorie restriction in biosphere 2: Alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. J. Gerontol. A Biol. Sci. Med. Sci. 57, B211–B224 (2002). 10.1093/gerona/57.6.B211

7

K. M. Vitousek, F. P. Manke, J. A. Gray, M. N. Vitousek, Caloric restriction for longevity: II—The systematic neglect of behavioural and psychological outcomes in animal research. Eur. Eat. Disord. Rev. 12, 338–360 (2004). 10.1002/erv.604

8

K. M. Vitousek, J. A. Gray, K. M. Grubbs, Caloric restriction for longevity: I. Paradigm, protocols and physiological findings in animal research. Eur. Eat. Disord. Rev. 12, 279–299 (2004). 10.1002/erv.594

9

K. M. Vitousek, The case for semi-starvation. Eur. Eat. Disord. Rev. 12, 275–278 (2004). 10.1002/erv.593

10

V. D. Longo, S. Panda, Fasting, circadian rhythms, and time-restricted feeding in healthy lifespan. Cell Metab. 23, 1048–1059 (2016). 10.1016/j.cmet.2016.06.001

11

P. Rous, The influence of diet on transplanted and spontaneous mouse tumors. J. Exp. Med. 20, 433–451 (1914). 10.1084/jem.20.5.433

12

T. B. Osborne, L. B. Mendel, E. L. Ferry, The effect of retardation of growth upon the breeding period and duration of life of rats. Science 45, 294–295 (1917). 10.1126/science.45.1160.294

13

C. M. McCay, M. F. Crowell, L. A. Maynard, The effect of retarded growth upon the length of lifespan and upon the ultimate body size. J. Nutr. 10, 63–79 (1935). 10.1093/jn/10.1.63

14

L. M. Redman, S. R. Smith, J. H. Burton, C. K. Martin, D. Il’yasova, E. Ravussin, Metabolic slowing and reduced oxidative damage with sustained caloric restriction support the rate of living and oxidative damage theories of aging. Cell Metab. 27, 805–815.e4 (2018). 10.1016/j.cmet.2018.02.019

15

L. Fontana, L. Partridge, V. D. Longo, Extending healthy life span—from yeast to humans. Science 328, 321–326 (2010). 10.1126/science.1172539

16

C. López-Otín, M. A. Blasco, L. Partridge, M. Serrano, G. Kroemer, The hallmarks of aging. Cell 153, 1194–1217 (2013). 10.1016/j.cell.2013.05.039

17

D. K. Ingram, G. S. Roth, Calorie restriction mimetics: Can you have your cake and eat it, too? Ageing Res. Rev. 20, 46–62 (2015). 10.1016/j.arr.2014.11.005

18

F. Madeo, F. Pietrocola, T. Eisenberg, G. Kroemer, Caloric restriction mimetics: Towards a molecular definition. Nat. Rev. Drug Discov. 13, 727–740 (2014). 10.1038/nrd4391

19

J. R. Speakman, C. Hambly, Starving for life: What animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan. J. Nutr. 137, 1078–1086 (2007). 10.1093/jn/137.4.1078

20

D. K. Ingram, R. de Cabo, Calorie restriction in rodents: Caveats to consider. Ageing Res. Rev. 39, 15–28 (2017). 10.1016/j.arr.2017.05.008

21

C. Y. Liao, B. A. Rikke, T. E. Johnson, J. A. L. Gelfond, V. Diaz, J. F. Nelson, Fat maintenance is a predictor of the murine lifespan response to dietary restriction. Aging Cell 10, 629–639 (2011). 10.1111/j.1474-9726.2011.00702.x

22

S. J. Mitchell, J. Madrigal-Matute, M. Scheibye-Knudsen, E. Fang, M. Aon, J. A. González-Reyes, S. Cortassa, S. Kaushik, M. Gonzalez-Freire, B. Patel, D. Wahl, A. Ali, M. Calvo-Rubio, M. I. Burón, V. Guiterrez, T. M. Ward, H. H. Palacios, H. Cai, D. W. Frederick, C. Hine, F. Broeskamp, L. Habering, J. Dawson, T. M. Beasley, J. Wan, Y. Ikeno, G. Hubbard, K. G. Becker, Y. Zhang, V. A. Bohr, D. L. Longo, P. Navas, L. Ferrucci, D. A. Sinclair, P. Cohen, J. M. Egan, J. R. Mitchell, J. A. Baur, D. B. Allison, R. M. Anson, J. M. Villalba, F. Madeo, A. M. Cuervo, K. J. Pearson, D. K. Ingram, M. Bernier, R. de Cabo, Effects of sex, strain, and energy intake on hallmarks of aging in mice. Cell Metab. 23, 1093–1112 (2016). 10.1016/j.cmet.2016.05.027

23

R. J. Colman, R. M. Anderson, S. C. Johnson, E. K. Kastman, K. J. Kosmatka, T. M. Beasley, D. B. Allison, C. Cruzen, H. A. Simmons, J. W. Kemnitz, R. Weindruch, Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201–204 (2009). 10.1126/science.1173635

24

J. A. Mattison, G. S. Roth, T. M. Beasley, E. M. Tilmont, A. M. Handy, R. L. Herbert, D. L. Longo, D. B. Allison, J. E. Young, M. Bryant, D. Barnard, W. F. Ward, W. Qi, D. K. Ingram, R. de Cabo, Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489, 318–321 (2012). 10.1038/nature11432

25

J. A. Mattison, R. J. Colman, T. M. Beasley, D. B. Allison, J. W. Kemnitz, G. S. Roth, D. K. Ingram, R. Weindruch, R. de Cabo, R. M. Anderson, Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 8, 14063 (2017). 10.1038/ncomms14063

26

L. K. Heilbronn, L. de Jonge, M. I. Frisard, J. P. DeLany, D. E. Larson-Meyer, J. Rood, T. Nguyen, C. K. Martin, J. Volaufova, M. M. Most, F. L. Greenway, S. R. Smith, W. A. Deutsch, D. A. Williamson, E. Ravussin; Pennington CALERIE Team, Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: A randomized controlled trial. JAMA 295, 1539–1548 (2006). 10.1001/jama.295.13.1539

27

C. K. Martin, M. Bhapkar, A. G. Pittas, C. F. Pieper, S. K. Das, D. A. Williamson, T. Scott, L. M. Redman, R. Stein, C. H. Gilhooly, T. Stewart, L. Robinson, S. B. Roberts, Effect of calorie restriction on mood, quality of life, sleep, and sexual function in healthy nonobese adults: The CALERIE 2 randomized clinical trial. JAMA Intern. Med. 176, 743–752 (2016). 10.1001/jamainternmed.2016.1189

28

E. Ravussin, L. M. Redman, J. Rochon, S. K. Das, L. Fontana, W. E. Kraus, S. Romashkan, D. A. Williamson, S. N. Meydani, D. T. Villareal, S. R. Smith, R. I. Stein, T. M. Scott, T. M. Stewart, E. Saltzman, S. Klein, M. Bhapkar, C. K. Martin, C. H. Gilhooly, J. O. Holloszy, E. C. Hadley, S. B. Roberts; CALERIE Study Group, A 2-year randomized controlled trial of human caloric restriction: Feasibility and effects on predictors of health span and longevity. J. Gerontol. A Biol. Sci. Med. Sci. 70, 1097–1104 (2015). 10.1093/gerona/glv057

29

J. Rochon, C. W. Bales, E. Ravussin, L. M. Redman, J. O. Holloszy, S. B. Racette, S. B. Roberts, S. K. Das, S. Romashkan, K. M. Galan, E. C. Hadley, W. E. Kraus; CALERIE Study Group, Design and conduct of the CALERIE study: Comprehensive assessment of the long-term effects of reducing intake of energy. J. Gerontol. A Biol. Sci. Med. Sci. 66, 97–108 (2011). 10.1093/gerona/glq168

30

D. C. Willcox, B. J. Willcox, W.-C. Hsueh, M. Suzuki, Genetic determinants of exceptional human longevity: Insights from the Okinawa Centenarian Study. Age (Dordr.) 28, 313–332 (2006). 10.1007/s11357-006-9020-x

31

L. Fontana, T. E. Meyer, S. Klein, J. O. Holloszy, Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans. Proc. Natl. Acad. Sci. U.S.A. 101, 6659–6663 (2004). 10.1073/pnas.0308291101

32

L. Fontana, S. Klein, Aging, adiposity, and calorie restriction. JAMA 297, 986–994 (2007). 10.1001/jama.297.9.986

33

E. M. Mercken, S. D. Crosby, D. W. Lamming, L. JeBailey, S. Krzysik-Walker, D. T. Villareal, M. Capri, C. Franceschi, Y. Zhang, K. Becker, D. M. Sabatini, R. de Cabo, L. Fontana, Calorie restriction in humans inhibits the PI3K/AKT pathway and induces a younger transcription profile. Aging Cell 12, 645–651 (2013). 10.1111/acel.12088

34

D. M. Kristan, Calorie restriction and susceptibility to intact pathogens. Age (Dordr.) 30, 147–156 (2008). 10.1007/s11357-008-9056-1

35

N. D. Hunt, G. D. Li, M. Zhu, M. Miller, A. Levette, M. E. Chachich, E. L. Spangler, J. S. Allard, D. H. Hyun, D. K. Ingram, R. de Cabo, Effect of calorie restriction and refeeding on skin wound healing in the rat. Age (Dordr.) 34, 1453–1458 (2012). 10.1007/s11357-011-9321-6

36

A. J. Dirks, C. Leeuwenburgh, Caloric restriction in humans: Potential pitfalls and health concerns. Mech. Ageing Dev. 127, 1–7 (2006). 10.1016/j.mad.2005.09.001

37

V. A. Acosta-Rodríguez, M. H. M. de Groot, F. Rijo-Ferreira, C. B. Green, J. S. Takahashi, Mice under caloric restriction self-impose a temporal restriction of food intake as revealed by an automated feeder system. Cell Metab. 26, 267–277.e2 (2017). 10.1016/j.cmet.2017.06.007

38

F. J. Roe, P. N. Lee, G. Conybeare, D. Kelly, B. Matter, D. Prentice, G. Tobin, The Biosure Study: Influence of composition of diet and food consumption on longevity, degenerative diseases and neoplasia in Wistar rats studied for up to 30 months post weaning. Food Chem. Toxicol. 33 (suppl. 1), S1–S100 (1995). 10.1016/0278-6915(95)80200-2

39

S. M. Solon-Biet, A. C. McMahon, J. W. O. Ballard, K. Ruohonen, L. E. Wu, V. C. Cogger, A. Warren, X. Huang, N. Pichaud, R. G. Melvin, R. Gokarn, M. Khalil, N. Turner, G. J. Cooney, D. A. Sinclair, D. Raubenheimer, D. G. Le Couteur, S. J. Simpson, The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab. 19, 418–430 (2014). 10.1016/j.cmet.2014.02.009

40

M. Hatori, C. Vollmers, A. Zarrinpar, L. DiTacchio, E. A. Bushong, S. Gill, M. Leblanc, A. Chaix, M. Joens, J. A. J. Fitzpatrick, M. H. Ellisman, S. Panda, Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 15, 848–860 (2012). 10.1016/j.cmet.2012.04.019

41

H. Sherman, I. Frumin, R. Gutman, N. Chapnik, A. Lorentz, J. Meylan, J. le Coutre, O. Froy, Long-term restricted feeding alters circadian expression and reduces the level of inflammatory and disease markers. J. Cell. Mol. Med. 15, 2745–2759 (2011). 10.1111/j.1582-4934.2010.01160.x

42

L. N. Woodie, Y. Luo, M. J. Wayne, E. C. Graff, B. Ahmed, A. M. O’Neill, M. W. Greene, 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 82, 1–13 (2018). 10.1016/j.metabol.2017.12.004

43

A. Chaix, A. Zarrinpar, P. Miu, S. Panda, Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab. 20, 991–1005 (2014). 10.1016/j.cmet.2014.11.001

44

S. J. Mitchell, M. Bernier, J. A. Mattison, M. A. Aon, T. A. Kaiser, R. M. Anson, Y. Ikeno, R. M. Anderson, D. K. Ingram, R. de Cabo, Daily fasting improves health and survival in male mice independent of diet composition and calories. Cell Metab. S1550-4131(18)30512-6 (2018). 10.1016/j.cmet.2018.08.011

45

O. Carlson, B. Martin, K. S. Stote, E. Golden, S. Maudsley, S. S. Najjar, L. Ferrucci, D. K. Ingram, D. L. Longo, W. V. Rumpler, D. J. Baer, J. Egan, M. P. Mattson, Impact of reduced meal frequency without caloric restriction on glucose regulation in healthy, normal-weight middle-aged men and women. Metabolism 56, 1729–1734 (2007). 10.1016/j.metabol.2007.07.018

46

S. Gill, S. Panda, A smartphone app reveals erratic diurnal eating patterns in humans that can be modulated for health benefits. Cell Metab. 22, 789–798 (2015). 10.1016/j.cmet.2015.09.005

47

T. Moro, G. Tinsley, A. Bianco, G. Marcolin, Q. F. Pacelli, G. Battaglia, A. Palma, P. Gentil, M. Neri, A. Paoli, 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. 14, 290 (2016). 10.1186/s12967-016-1044-0

48

K. S. Stote, D. J. Baer, K. Spears, D. R. Paul, G. K. Harris, W. V. Rumpler, P. Strycula, S. S. Najjar, L. Ferrucci, D. K. Ingram, D. L. Longo, M. P. Mattson, A controlled trial of reduced meal frequency without caloric restriction in healthy, normal-weight, middle-aged adults. Am. J. Clin. Nutr. 85, 981–988 (2007). 10.1093/ajcn/85.4.981

49

G. M. Tinsley, J. S. Forsse, N. K. Butler, A. Paoli, A. A. Bane, P. M. La Bounty, G. B. Morgan, P. W. Grandjean, Time-restricted feeding in young men performing resistance training: A randomized controlled trial. Eur. J. Sport Sci. 17, 200–207 (2017). 10.1080/17461391.2016.1223173

50

K. Gabel, K. K. Hoddy, N. Haggerty, J. Song, C. M. Kroeger, J. F. Trepanowski, S. Panda, K. A. Varady, Effects of 8-hour time restricted feeding on body weight and metabolic disease risk factors in obese adults: A pilot study. Nutr. Healthy Aging 4, 345–353 (2018). 10.3233/NHA-170036

51

H. A. Raynor, F. Li, C. Cardoso, Daily pattern of energy distribution and weight loss. Physiol. Behav. 192, 167–172 (2018). 10.1016/j.physbeh.2018.02.036

52

D. Jakubowicz, M. Barnea, J. Wainstein, O. Froy, High caloric intake at breakfast vs. dinner differentially influences weight loss of overweight and obese women. Obesity (Silver Spring) 21, 2504–2512 (2013). 10.1002/oby.20460

53

T. Yoshizaki, Y. Tada, A. Hida, A. Sunami, Y. Yokoyama, J. Yasuda, A. Nakai, F. Togo, Y. Kawano, Effects of feeding schedule changes on the circadian phase of the cardiac autonomic nervous system and serum lipid levels. Eur. J. Appl. Physiol. 113, 2603–2611 (2013). 10.1007/s00421-013-2702-z

54

H. Kahleova, L. Belinova, H. Malinska, O. Oliyarnyk, J. Trnovska, V. Skop, L. Kazdova, M. Dezortova, M. Hajek, A. Tura, M. Hill, T. Pelikanova, Eating two larger meals a day (breakfast and lunch) is more effective than six smaller meals in a reduced-energy regimen for patients with type 2 diabetes: A randomised crossover study. Diabetologia 57, 1552–1560 (2014). 10.1007/s00125-014-3253-5

55

E. F. Sutton, R. Beyl, K. S. Early, W. T. Cefalu, E. Ravussin, C. M. Peterson, Early time-restricted feeding improves insulin sensitivity, blood pressure, and oxidative stress even without weight loss in men with prediabetes. Cell Metab. 27, 1212–1221.e3 (2018). 10.1016/j.cmet.2018.04.010

56

R. I. Versteeg, D. J. Stenvers, D. Visintainer, A. Linnenbank, M. W. Tanck, G. Zwanenburg, A. K. Smilde, E. Fliers, A. Kalsbeek, M. J. Serlie, S. E. la Fleur, P. H. Bisschop, Acute effects of morning light on plasma glucose and triglycerides in healthy men and men with type 2 diabetes. J. Biol. Rhythms 32, 130–142 (2017). 10.1177/0748730417693480

57

C. R. Marinac, L. Natarajan, D. D. Sears, L. C. Gallo, S. J. Hartman, E. Arredondo, R. E. Patterson, Prolonged nightly fasting and breast cancer risk: Findings from NHANES (2009–2010). Cancer Epidemiol. Biomarkers Prev. 24, 783–789 (2015). 10.1158/1055-9965.EPI-14-1292

58

C. R. Marinac, S. H. Nelson, C. I. Breen, S. J. Hartman, L. Natarajan, J. P. Pierce, S. W. Flatt, D. D. Sears, R. E. Patterson, Prolonged nightly fasting and breast cancer prognosis. JAMA Oncol. 2, 1049–1055 (2016). 10.1001/jamaoncol.2016.0164

59

T. Finkel, The metabolic regulation of aging. Nat. Med. 21, 1416–1423 (2015). 10.1038/nm.3998

60

C. L. Goodrick, D. K. Ingram, M. A. Reynolds, J. R. Freeman, N. Cider, Effects of intermittent feeding upon body weight and lifespan in inbred mice: Interaction of genotype and age. Mech. Ageing Dev. 55, 69–87 (1990). 10.1016/0047-6374(90)90107-Q

61

K. Xie, F. Neff, A. Markert, J. Rozman, J. A. Aguilar-Pimentel, O. V. Amarie, L. Becker, R. Brommage, L. Garrett, K. S. Henzel, S. M. Hölter, D. Janik, I. Lehmann, K. Moreth, B. L. Pearson, I. Racz, B. Rathkolb, D. P. Ryan, S. Schröder, I. Treise, R. Bekeredjian, D. H. Busch, J. Graw, G. Ehninger, M. Klingenspor, T. Klopstock, M. Ollert, M. Sandholzer, C. Schmidt-Weber, M. Weiergräber, E. Wolf, W. Wurst, A. Zimmer, V. Gailus-Durner, H. Fuchs, M. Hrabě de Angelis, D. Ehninger, Every-other-day feeding extends lifespan but fails to delay many symptoms of aging in mice. Nat. Commun. 8, 155 (2017). 10.1038/s41467-017-00178-3

62

C. Lee, L. Raffaghello, S. Brandhorst, F. M. Safdie, G. Bianchi, A. Martin-Montalvo, V. Pistoia, M. Wei, S. Hwang, A. Merlino, L. Emionite, R. de Cabo, V. D. Longo, Fasting cycles retard growth of tumors and sensitize a range of cancer cell types to chemotherapy. Sci. Transl. Med. 4, 124ra27 (2012). 10.1126/scitranslmed.3003293

63

R. M. Anson, Z. Guo, R. de Cabo, T. Iyun, M. Rios, A. Hagepanos, D. K. Ingram, M. A. Lane, M. P. Mattson, Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc. Natl. Acad. Sci. U.S.A. 100, 6216–6220 (2003). 10.1073/pnas.1035720100

64

R. Singh, D. Lakhanpal, S. Kumar, S. Sharma, H. Kataria, M. Kaur, G. Kaur, Late-onset intermittent fasting dietary restriction as a potential intervention to retard age-associated brain function impairments in male rats. Age (Dordr.) 34, 917–933 (2012). 10.1007/s11357-011-9289-2

65

J. A. Baur, K. J. Pearson, N. L. Price, H. A. Jamieson, C. Lerin, A. Kalra, V. V. Prabhu, J. S. Allard, G. Lopez-Lluch, K. Lewis, P. J. Pistell, S. Poosala, K. G. Becker, O. Boss, D. Gwinn, M. Wang, S. Ramaswamy, K. W. Fishbein, R. G. Spencer, E. G. Lakatta, D. Le Couteur, R. J. Shaw, P. Navas, P. Puigserver, D. K. Ingram, R. de Cabo, D. A. Sinclair, Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337–342 (2006). 10.1038/nature05354

66

J. C. Newman, A. J. Covarrubias, M. Zhao, X. Yu, P. Gut, C.-P. Ng, Y. Huang, S. Haldar, E. Verdin, Ketogenic diet reduces midlife mortality and improves memory in aging mice. Cell Metab. 26, 547–557.e8 (2017). 10.1016/j.cmet.2017.08.004

67

M. N. Roberts, M. A. Wallace, A. A. Tomilov, Z. Zhou, G. R. Marcotte, D. Tran, G. Perez, E. Gutierrez-Casado, S. Koike, T. A. Knotts, D. M. Imai, S. M. Griffey, K. Kim, K. Hagopian, M. Z. McMackin, F. G. Haj, K. Baar, G. A. Cortopassi, J. J. Ramsey, J. A. Lopez-Dominguez, A ketogenic diet extends longevity and healthspan in adult mice. Cell Metab. 27, 1156 (2018). 10.1016/j.cmet.2018.04.005

68

P. Puchalska, P. A. Crawford, Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metab. 25, 262–284 (2017). 10.1016/j.cmet.2016.12.022

69

V. A. Catenacci, Z. Pan, D. Ostendorf, S. Brannon, W. S. Gozansky, M. P. Mattson, B. Martin, P. S. MacLean, E. L. Melanson, W. Troy Donahoo, A randomized pilot study comparing zero-calorie alternate-day fasting to daily caloric restriction in adults with obesity. Obesity (Silver Spring) 24, 1874–1883 (2016). 10.1002/oby.21581

70

K. K. Hoddy, C. M. Kroeger, J. F. Trepanowski, A. Barnosky, S. Bhutani, K. A. Varady, Meal timing during alternate day fasting: Impact on body weight and cardiovascular disease risk in obese adults. Obesity (Silver Spring) 22, 2524–2531 (2014). 25251676

71

K. A. Varady, S. Bhutani, E. C. Church, M. C. Klempel, Short-term modified alternate-day fasting: A novel dietary strategy for weight loss and cardioprotection in obese adults. Am. J. Clin. Nutr. 90, 1138–1143 (2009). 10.3945/ajcn.2009.28380

72

F. M. Safdie, T. Dorff, D. Quinn, L. Fontana, M. Wei, C. Lee, P. Cohen, V. D. Longo, Fasting and cancer treatment in humans: A case series report. Aging 1, 988–1007 (2009). 10.18632/aging.100114

73

J. F. Trepanowski, C. M. Kroeger, A. Barnosky, M. C. Klempel, S. Bhutani, K. K. Hoddy, K. Gabel, S. Freels, J. Rigdon, J. Rood, E. Ravussin, K. A. Varady, Effect of alternate-day fasting on weight loss, weight maintenance, and cardioprotection among metabolically healthy obese adults: A randomized clinical trial. JAMA Intern. Med. 177, 930–938 (2017). 10.1001/jamainternmed.2017.0936

74

Y. Yokoyama, K. Onishi, T. Hosoda, H. Amano, S. Otani, Y. Kurozawa, A. Tamakoshi, Skipping breakfast and risk of mortality from cancer, circulatory diseases and all causes: Findings from the Japan Collaborative Cohort Study. Yonago Acta Med. 59, 55–60 (2016). 27046951

75

I. Uzhova, V. Fuster, A. Fernández-Ortiz, J. M. Ordovás, J. Sanz, L. Fernández-Friera, B. López-Melgar, J. M. Mendiguren, B. Ibáñez, H. Bueno, J. L. Peñalvo, The importance of breakfast in atherosclerosis disease: Insights from the PESA study. J. Am. Coll. Cardiol. 70, 1833–1842 (2017). 10.1016/j.jacc.2017.08.027

76

S. Brandhorst, I. Y. Choi, M. Wei, C. W. Cheng, S. Sedrakyan, G. Navarrete, L. Dubeau, L. P. Yap, R. Park, M. Vinciguerra, S. Di Biase, H. Mirzaei, M. G. Mirisola, P. Childress, L. Ji, S. Groshen, F. Penna, P. Odetti, L. Perin, P. S. Conti, Y. Ikeno, B. K. Kennedy, P. Cohen, T. E. Morgan, T. B. Dorff, V. D. Longo, A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 22, 86–99 (2015). 10.1016/j.cmet.2015.05.012

77

C.-W. Cheng, V. Villani, R. Buono, M. Wei, S. Kumar, O. H. Yilmaz, P. Cohen, J. B. Sneddon, L. Perin, V. D. Longo, Fasting-mimicking diet promotes Ngn3-driven β-cell regeneration to reverse diabetes. Cell 168, 775–788.e12 (2017). 10.1016/j.cell.2017.01.040

78

M. Wei, S. Brandhorst, M. Shelehchi, H. Mirzaei, C. W. Cheng, J. Budniak, S. Groshen, W. J. Mack, E. Guen, S. Di Biase, P. Cohen, T. E. Morgan, T. Dorff, K. Hong, A. Michalsen, A. Laviano, V. D. Longo, Fasting-mimicking diet and markers/risk factors for aging, diabetes, cancer, and cardiovascular disease. Sci. Transl. Med. 9, eaai8700 (2017). 10.1126/scitranslmed.aai8700

79

I. Y. Choi, L. Piccio, P. Childress, B. Bollman, A. Ghosh, S. Brandhorst, J. Suarez, A. Michalsen, A. H. Cross, T. E. Morgan, M. Wei, F. Paul, M. Bock, V. D. Longo, A diet mimicking fasting promotes regeneration and reduces autoimmunity and multiple sclerosis symptoms. Cell Reports 15, 2136–2146 (2016). 10.1016/j.celrep.2016.05.009

80

A. J. McLean, D. G. Le Couteur, Aging biology and geriatric clinical pharmacology. Pharmacol. Rev. 56, 163–184 (2004). 10.1124/pr.56.2.4

81

B. A. Rikke, J. E. Yerg 3rd, M. E. Battaglia, T. R. Nagy, D. B. Allison, T. E. Johnson, Strain variation in the response of body temperature to dietary restriction. Mech. Ageing Dev. 124, 663–678 (2003). 10.1016/S0047-6374(03)00003-4

82

A. Diaz-Ruiz, M. Lanasa, J. Garcia, H. Mora, F. Fan, A. Martin-Montalvo, A. Di Francesco, M. Calvo-Rubio, A. Salvador-Pascual, M. A. Aon, K. W. Fishbein, K. J. Pearson, J. M. Villalba, P. Navas, M. Bernier, R. de Cabo, Overexpression of CYB5R3 and NQO1, two NAD+-producing enzymes, mimics aspects of caloric restriction. Aging Cell 17, e12767 (2018). 10.1111/acel.12767