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19
From Biologic Rhythms to Chronomes Relevant for Nutrition

Franz Halberg,1 Erhard Haus, and Germaine Cornélissen

Not Eating Enough, 1995

Pp. 361–372. Washington, D.C.

National Academy Press

INTRODUCTION

Any one physiologic variable is characterized by a spectrum of rhythms that are genetically anchored, socioecologically synchronized (by the cycles of an environmental niche), and influenced by heliogeophysical effects. Influences can be objectively quantified in terms of cross-spectral coherences. Synchronization is studied (e.g., by shifts of meal timing, such as on shift work, and/or the entire daily routine, such as after transmeridian flights) when different chronome components may adjust at differing rates in any one variable. Blood pressure and heart rate, for instance, reveal a slow adjustment of a built-in approximately 7-d rhythmicity in the face of a rather rapid adjustment of the circadian component in the same variables. Shifts in meal timing have different effects upon different physiologic variables and thus alter internal relations among rhythms at different organization levels, as documented for the

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Franz Halberg, University of Minnesota, Chronobiology Laboratories, Minneapolis, MN 55455



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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations 19 From Biologic Rhythms to Chronomes Relevant for Nutrition Franz Halberg,1 Erhard Haus, and Germaine Cornélissen Not Eating Enough, 1995 Pp. 361–372. Washington, D.C. National Academy Press INTRODUCTION Any one physiologic variable is characterized by a spectrum of rhythms that are genetically anchored, socioecologically synchronized (by the cycles of an environmental niche), and influenced by heliogeophysical effects. Influences can be objectively quantified in terms of cross-spectral coherences. Synchronization is studied (e.g., by shifts of meal timing, such as on shift work, and/or the entire daily routine, such as after transmeridian flights) when different chronome components may adjust at differing rates in any one variable. Blood pressure and heart rate, for instance, reveal a slow adjustment of a built-in approximately 7-d rhythmicity in the face of a rather rapid adjustment of the circadian component in the same variables. Shifts in meal timing have different effects upon different physiologic variables and thus alter internal relations among rhythms at different organization levels, as documented for the 1   Franz Halberg, University of Minnesota, Chronobiology Laboratories, Minneapolis, MN 55455

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations circadian chronome components of humans and rodents (Figures 19-1, 19-2, and 19-3). MEAL TIMING IN TERMS OF CALORIES AND SEDENTARY LIMITED MOTOR ACTIVITY It seems possible to better exploit what is being eaten by scheduling meals. Food consumption could be scheduled for a time when it is physiologically (Goetz et al., 1976; Halberg, 1983, 1989; Halberg et al., 1976, Hirsch et al., 1975; Jacobs et al., 1975) and logistically most useful for body weight maintenance. Specifically, as a countermeasure in the face of underconsumption of rations by workers in the field (such as soldiers), at least one meal should be timed by taking into account the studies carried out in Minnesota on meal timing (Goetz et al., 1976), some of them sponsored by the U.S. Army Institute of Environmental Medicine and the U.S. Army Natick Research, Development and Engineering Center (NRDEC) (Hirsch et al., 1975; Jacobs et al., 1975). These investigations, which compare a single daily meal consumed as a breakfast versus one eaten as a dinner, clearly show a relative FIGURE 19-1 Differential displacement of circadian hormonal timing as a result of changing a single daily meal from breakfast to dinner. Whereas the circadian rhythm of circulating cortisol is only slightly affected by the timing of a single daily meal, considerable phase-shifts are observed for the case of growth hormone, insulin, and glucagon. SOURCE: © Franz Halberg (1970), used with permission.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-2 Consuming a single daily meal as breakfast only versus dinner only affects the timing of the circadian chronome component differently for different physiologic variables in humans. The single daily meal was 2,000 kcal given for 7-d spans. Breakfast (B), solid line. Dinner (D), broken line. SOURCE: © Franz Halberg (1970), used with permission.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-3 Effects on circadian rhythmic variables in mice of different lighting schedules, early light phase (early-L) and early dark phase (early-D), SOURCE: © Franz Halberg (1970), used with permission. gain in body weight at dinner only versus breakfast only (a statement equivalent to that of a relative body weight loss on breakfast only versus dinner only) (Figures 19-4, 19-5, 19-6, and 19-7). Since in these studies physiologic and psychologic performance were investigated, as were metabolic and endocrine variables, a first recommendation is the completion of analyses of these data (Goetz et al., 1976; Halberg, 1983, 1989; Halberg et al., 1976; Hirsch et al., 1975; Jacobs et al., 1975) on the consequences (concerning body weight and other physiologic and psychologic performance) of consuming one single large meal within 1 hour of awakening (breakfast only) or not before 12 hours after awakening (dinner only). A second recommendation is to extend the scope of the paradigm tested earlier concerning a single meal per day, with several scenarios applied to The Meal, Ready-to-Eat (MRE).

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-4 Meal timing and body weight. In two separate studies of the effect of meal timing on body weight, nine men and nine women consumed either a fixed 2,000 kcal meal or a single free-choice meal as breakfast (B) or dinner (D) (for 1 week on a fixed-calorie meal or 3 weeks on a free-choice meal). Body weight remained more or less unchanged on dinner only; a decrease of about 1 kg/wk was noted on breakfast only. The rate of body weight change also differed significantly (P < 0.01) between the two schedules. SOURCE: © Franz Halberg (1980), used with permission. Timing the Kinds of Calories Specifically, if one had the means, one should repeat the single meal per day study with and without exercise while concomitantly varying the proportions of carbohydrate, fat, and protein, both in the absence of snacks and then with the stepwise systematic addition of timed snacks. With more modest resources, the next step should be tests in the field with exercising and nonexercising individuals consuming three MREs as breakfast, lunch, and dinner versus consuming one-half of an MRE for breakfast, the other one-half MRE for lunch, and two MREs for dinner.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-5 Relative body weight loss on breakfast only versus dinner only for each subject participating in the two studies described in Figure 19-4. Only one volunteer gained weight on breakfast versus dinner. Overall, the difference in relative body weight loss on breakfast (B) versus dinner (D) is statistically significant (P < 0.05), whether a fixed 2,000 kcal meal or a single free-choice meal is consumed. Weight change (kg/wk) on D subtracted from that on B. In the study on one free-choice meal per day, subjects are only breakfast for 3 weeks and only dinner for 3 weeks. In the study on one fixed 2,000 kcal meal per day, subjects ate only breakfast for 1 week and only dinner for 1 week. Note that mean relative weight loss is greater on fixed than on free-choice meal. SOURCE: © Franz Halberg (1980), used with permission. Meal and Performance Timing In view of a circadian rhythm in the response to exercise (Halberg et al., 1988; Levine et al., 1977), any effect of meal timing on performance could be assessed by having the exercising group complete a standardized routine, for example on a bicycle ergometer. The routine could be repeated at 3-h intervals; at awakening; at 3, 6, 9, and 12 hours thereafter; and at betime. This lab has tested on four subjects a more rigorous schedule, namely exercise at 7 a.m., 10 a.m., 1 p.m., 4 p.m., 7 p.m., 10 p.m., and 1 a.m. each day for up to a month. It would be important to concomitantly evaluate mental performance and alertness on the different schedules. Several studies in his lab have shown that body weight loss may not necessarily be accompanied by a decrease in performance.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-6 Appetite (here defined as choice and amount of food) modifies the effect of meal timing on body weight. Relative body weight loss on breakfast only (B) as compared to dinner only (D) is less when meal is free choice rather than fixed. Therefore, to minimize body weight loss when a single meal is consumed, it may be preferable not to fix the ration but to offer a choice. An overall summary of relative body weight loss on breakfast only versus dinner only in the two studies described in Figures 19-4 and 19-5 indicates that the decrease in relative body weight was more pronounced when a fixed 2,000 kcal meal was imposed than when volunteers could choose what they ate. †, weight change (kg/wk) on B subtracted from that on D. SOURCE: © Franz Halberg (1980), used with permission. Meal Timing and the Body's Time Structure (Chronome) The Minnesota-Natick studies (Goetz et al., 1976; Halberg et al., 1976; Hirsch et al., 1975; Jacobs et al., 1975) have shown that meal timing is a way to shift physiologic rhythms and that it may amplify the expression of the circadian system, as do certain drugs such as acetyl-L-carnitine (Cornélissen et al., 1992; Portela et al., 1993). It would be worthwhile to determine the most favorable configuration of rhythms in order to assure the peak alertness and performance (e.g., of rangers or pilots) during the most critical times of duty, even if these schedules may be associated with some body weight loss, notably in situations where field duties are of limited duration. Note that at least in the experimental laboratory, food restriction (e.g., to 70 percent of what is consumed ad lib) is associated with a prolongation (Nelson and Halberg, 1986a, b), not a shortening, of the lifespan and also with a lower incidence of mammary cancers (Halberg et al., 1986b).

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations FIGURE 19-7 Appetite (choice and amount of food) modifies effect of meal timing on body weight. The lesser body weight loss on breakfast (B) versus dinner (D) observed on a free-choice versus a fixed 2,000 kcal meal occurred while calorie consumption on the free-choice meal was less (not more) than 2,000 kcal per meal. *, weight change on B subtracted from that on D. SOURCE: © Franz Halberg (1980), used with permission. RECOMMENDATIONS Analysis of Available Data Current data suggest that a major meal should be eaten upon conclusion of a daily tour of duty; that is, if the duty starts in the morning, the major meal should be in the evening, or vice versa. In other words, scheduling should be by activity time rather than clock hour. This concept should be explained in an appropriate communication to commanding officers, so that it is reinforced by them and they are able to set a good example, which benefits themselves and their troops. In the interim, the wealth of data accumulated in the Minnesota-Natick studies and additional data to be obtained should be used to assess the relationship between performance and body weight change. This

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations effort would benefit from further experimental studies in the laboratory and in the field. Such retrospective analyses are recommended, and the sooner the better. Endocrine and performance data are available in Minnesota from meal-timing studies that have thus far been the subject only of a technical report (Graeber et al., 1978). Data collected, for example by L. A. Stephenson and M. A. Kolka at NRDEC on the adrenal cycle (Personal communication, 1993), would benefit from a chronobiologic assessment that can provide an individualized assessment of statistical significance. Prospective Studies on Optimization of Dietary Supplements Autopsies on very young American soldiers killed in battle during the Korean War revealed some vascular changes and suggested the need for prophylaxis by that age if not earlier (for review, see Halberg et al., 1986a). The methods of chronobiology allow level of risk to be detected by means of chronophysiologic monitoring (instead of relying on time-specified spot checks, biopsies, and autopsies) (Cornélissen et al., 1993; Halberg et al., 1993). Differences in dynamic features of blood pressure variation are found between the offspring of parents with and without high blood pressure and/or other cardiovascular disease (Halberg et al., 1990). Such differences as a function of family history of cardiovascular diseases are found early in life: shortly after birth and in adolescents. An unduly amplified circadian rhythm of blood pressure can be interpreted as presenting a heightened risk for vascular disease, notably stroke and nephropathy (Otsuka, 1994). Thus arises the opportunity for the Army to identify a portion of the population at risk and develop procedures for preventing a further deterioration of the vascular system and preferably for reversing changes that are already in place. Dietary modification, such as the use of supplements, is one approach toward this goal. Much chronobiologic evidence from cooperative studies reveals the need to time the administration of dietary supplements according to rhythms. It has, for instance, become apparent that the effects of aspirin may be circadian stage-dependent, notably some prophylactic effects that may be related to the antiplatelet activity of aspirin (Cornélissen et al., 1991; Prikryl et al., 1991, 1993). Host tolerance of aspirin is also time-dependent (Siegelova et al., 1993). The best compromise between efficacy and tolerance must therefore be sought for prophylactic uses of aspirin. The same considerations apply to carnitine preparations that have a circadian stage-dependent effect upon blood pressure and heart rate (Cornélissen et al., 1994; Portela et al., 1993). Documenting this putative time-dependence on an appropriate scale and implementing the study of other dietary supplements given to recruits at the beginning of the tour of duty may be within the scope of Army nutrition. Such a study would gain from including an echocardiogram and a 7-d ambulatory blood pressure and heart rate profile at the outset, with the

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations measurements repeated 1 year later. The risk indices reflected by the pattern of blood pressure variation could thus be correlated with left ventricular mass and other indices of the heart morphology obtained by echocardiography (Cornélissen et al., 1994; Kumagai et al., 1992). If, in addition, the recruits can be persuaded to keep a precise diary of when and what they eat, it might be possible to study associations between any alteration of the cardiovascular chronomes and patterns in the relative consumptions of carbohydrate, fat, protein, and/or dietary supplements. Further guidelines may thus be derived for making recommendations of what to eat when. Given the age of recruits, this may be the best opportunity to carry out such nutritional studies with an aim toward prevention and self-help according to a chronobiologic approach now being advocated by the American Association for the Advancement of Science in a newly released report (Cornélissen, 1994; Culotta, 1993). AUTHORS' NOTE As an aside, the first author was most happy during the post-World War II years in Austria to receive U.S. Army rations in the form of CARE packages. These were—and in the authors' opinion still are—invaluable, the difference in circumstances notwithstanding. If it is impossible a priori to know how much food will be consumed by military personnel, and if a complete consumption of the ration cannot be realized, it seems reasonable that rations could be packaged so that unused portions can be saved and consumed at a later time or recycled for human and/or other use rather than discarded as waste. This would be a step beyond the technology that makes possible shelf-stable meals that do not require refrigeration before opening, but also a step far beyond our competence. REFERENCES Cornélissen, G. 1994. Standards for science education in U.S. schools spelled out. Chronobiologia 21:164. Cornélissen, G., F. Halberg, P. Prikryl, E. Dankova, J. Siegelova, and J. Dusek 1991. International womb-to-womb chronome group: Prophylactic aspirin treatment: The merits of timing. J. Am. Med. Assoc. 266:3128–3129. Cornélissen, G., G. Francesetti, M. Gecele, A. Meluzzi, G. Bartolomucci, and F. Halberg 1992. Metachronanalysis: Acetyl-L-carnitine advances circadian aspect of circulating cortisol chronome of elderly depressed patients. New Trends Exp. Clin. Psychiatry 8:95–101. Cornélissen, G., P. Delmore, C. Bingham, G. Rutledge, Y. Kumagai, I. Kuwajima, Y. Suzuki, K. Kuramoto, K. Otsuka, P.T. Scarpelli, B. Tarquini, M. Cagnoni, L. Garcia, R.M. Zaslavskaya, E. Syutkina, F. Carandente, S.I. Rapoport, Y.A. Romanov, K. Tamura, E. Bakken, and F. Halberg 1993. A response to the health care crisis: A ''health start" from "womb to tomb." Chronobiologia 10:277–291.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations Cornélissen, G., E. Halberg, F. Halverg, R.M. Zaslavskaya, I. Logvinenko, A. Konkova, O. Shekhaeva, and G. Bartolomucci 1994. The cost-effective chronobiologic trial documented by the effects of L-carnitine. Chronobiologia 21:333–334. Culotta, E. 1993. Curriculum reform: Project 2061 offers a benchmark. Science 262:498–499. Goetz, F.C., J. Bishop, F. Halberg, R.B. Sothern, R. Brunning, B. Senske, B. Greenberg. D. Minors, P. Stoney, I.D. Smith, G.D. Rosen, D. Cressey, E. Haus, and M. Apfelbaum 1976. Timing of single daily meal influences relations among human circadian rhythms in urinary cyclic AMP and hemic glucagon, insulin and iron. Experientia (Basel) 32:1081–1084. Graeber, R.C., R. Gatty, F. Halberg, and H. Levine 1978. Human eating behavior: Preferences, consumption patterns, and biorhythms. Technical Report TR-78-022. Natick, Mass.: U.S. Army Natick Research and Development Command. Halberg, F. 1983. Chronobiology and nutrition. Contemp. Nutr. 8 (9):2 pp. (unpaginated). 1989. Some aspects of the chronobiology of nutrition: More work is needed on "when to eat." J. Nutr. 119:333–343. Halberg, F., E. Halberg, and F. Carandente 1976. Chronobiology and metabolism in the broader context of timely intervention and timed treatment. Pp. 45–95 in Diabetes Research Today. Meeting of the Minkowski Prize Winners, Symposia Medica Hoechst 12 (Capri). Stuttgart/New York: F.K. Schattauer Verlag. Halberg, F., E. Haus, E. Halberg, G. Cornélissen, P. Scarpelli, B. Tarquini, M. Cagnoni, D. Wilson, K. Griffiths, H. Simpson, E. Balestra, and L. Reale 1986a. Chronobiologic challenges in social medicine: Illustrative tasks in cardiology and oncology. Pp. 13–42 in Proceedings of the Second International Conference on the Medico-Social Aspects of Chronobiology, F. Halberg, L. Reale, and B. Tarquini, eds. Rome: Instituto Italiano di Medicina Sociale. Halberg, F., S. Sánchez, and W. Nelson 1986b. Rhythm scrambling and tumorigenesis in CD2F1 mice. Pp. 59–61 in III International Symposium, Social Diseases and Chronobiology, B. Tarquini and R. Vergassola, eds., Florence: Centro Stampa Palogi. Halberg, F., G. Cornélissen, E. Halberg, J. Halberg, P. Delmore, M. Shinoda, and E. Bakken 1988. Chronobiology of Human Blood Pressure. Medtronic Continuing Medical Education Seminars, 4th ed. Minneapolis: Medtronic, Inc. Halberg, F., G. Cornélissen, and E. Bakken 1990. Caregiving merged with chronobiologic outcome assessment, research and education in health maintenance organizations (HMOs). Progress in Clinical and Biological Research 341B:491–549. Halberg, F. G. Cornélissen, A. Carandente, E. Bakken, and E. Young 1993. Chronobiologic perspectives of international health care reform for the future of children. Chronobiologia 20:269–275. Hirsch, E., E. Halberg, F. Halberg, F.C. Goetz, D. Cressey, H. Wendt, R. Sothern, E. Haus, P. Stoney, D. Minors, G. Rosen, B. Hill, M. Hilleren, and K. Garett 1975. Body weight change during 1 week on a single daily 2,000-calorie meal consumed as breakfast (B) or dinner (D), Chronobiologia 2(suppl. 1):31–32. Jacobs, H., M. Thompson, E. Halberg, F. Halberg, R.C. Graeber, H. Levine, and E. Haus 1975. Relative body weight loss on limited free-choice meal consumed as breakfast rather than dinner. Chronobiologia 2(suppl. 1):33.

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Not Eating Enough: Overcoming Underconsumption of Military Operational Rations Kumagai, Y., T. Shiga, K. Sunaga, G. Cornélissen, A. Ebihara, and F. Halberg 1992. Usefulness of circadian amplitude of blood pressure in predicting hypertensive cardiac involvement. Chronobiologia 19:43–58. Levine, H., W. Saltzman, J. Yankaskas, and F. Halberg 1977. Circadian stage-dependent effect of exercise upon blood pressure in clinically healthy men. Chronobiologia 4:129–130. Nelson, W., and F. Halberg 1986a. Meal-timing, circadian rhythms and lifespan of mice. J. Nutr. 116:2244–2253. 1986b. Schedule-shifts, circadian rhythms and lifespan of freely-feeding and meal-fed mice. Physiol. Behav. 38:781–788. Otsuka, K., G. Cornélissen, and F. Halberg 1994. Elevated risk of nephropathy in normotensives with an excessive circadian blood pressure amplitude. IV Reunion de Grupos de Chronobiologia. December 6–7, La Coruña, Spain. Portela, A., G. Cornélissen, M. Blank, Y. Kumagai, C. Bingham, G. Bartolomucci, and F. Halberg 1993. Circadian stage-dependence of acetyl-L-carnitine effects on blood pressure and heart rate clinically healthy subjects. Chronobiologia 20:63–76. Prikryl, P., J. Siegelova, G. Cornélissen, J. Dusek, E. Dankova, B. Fiser, J. Vacha, S. Ferrazzani, A. Tocci, A. Caruso, G. Rao, H. Fink, F. Halberg, and International Womb-to-Tomb Chronome Initiative Group 1991. Chronotherapeutic treatment—daily low-dose aspirin. University of Minnesota/Medtronic Chronobiology Seminar Series, no. 3. Minneapolis: Medtronic, Inc. Prikryl, P., J. Siegelova, G. Cornélissen, J. Dusek, E. Dankova, B. Fiser, J. Vacha, S. Ferrazzani, A. Tocci, A. Caruso, G. Rao, H. Fink, and F. Halberg 1993. Chronotherapeutic pilot on 6 persons may guide tests on thousands: Toward a circadian optimization of prophylactic treatment with daily low-dose aspirin. Pp. 113–117 in Chronocardiology and Chronomedicine: Humans in Time and Cosmos, K. Otsuka, G. Cornélissen, and F. Halberg, eds. Tokyo: Life Science Publishing. Siegelova, J., P. Prikryl, G. Cornélissen J. Moore, and F. Halberg 1993. Chronobiologic approach to therapeutic efficacy overriding sole tolerance consideration. Pp. 118–120 in Chronocardiology and Chronomedicine: Humans in Time and Cosmos, K. Otsuka, G. Cornélissen, and F. Halberg, eds. Tokyo: Life Science Publishing.