eaton, konner, shostak - 1988 - stone agers in the fast lane chronic degenerative diseases in...

7/27/2019 Eaton, Konner, Shostak - 1988 - Stone Agers in the Fast Lane Chronic Degenerative Diseases in Evolutionary Pers

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ANTHROPOLOGICAL COMMENTARY

Stone Agers in the Fast Lane: Chronic Degenerative Diseases inEvolutionary Perspective

S. BOYD EATON, M.D.MELVIN KONNER, Ph.D., M.D.MARJORIE SHOSTAKAtlanta, Georgia

From the Department of Anthropology, theSchool of Medicine, and the Institute of LiberalArts, Emory University, Atlanta, Georgia. Re-quests for reprints should be addressed to Dr. S.Boyd Eaton, Department of Anthropology, EmoryUniversity, Atlanta, Georgia 30322. Manuscriptsubmitted December 11, 1987, and accepted inrevjsed form February 5, 1988.

From a genetic standpoint, humans living today are Stone Age hunter-gatherers displaced through time to a world that differs from that forwhich our genetic constitution was selected. Unlike evolutionary mai-adaptation, our current discordance has little effect on reproductivesuccess; rather it acts as a potent promoter of chronic illnesses:atherosclerosis, essential hypertension, many cancers, diabetes meiti-tus, and obesity among others. These diseases are the results ofinteraction between genetically controlled biochemical processes anda myriad of bioculturai infiuenc&iifes tyie factors-that include nu-trition, exerc ise, and exposure to noxious substances. Although ourgenes have hardly changed, our culture has been transformed almostbeyond recognition during the past 10,000 years, especially since theindustrial Revolution. There is increasing evidence that the resultingmismatch fosters diseases of civil ization that together cause 75percent of ail deaths in Western nations, but that are rare amongpersons whose iifeways reflect those of our preagricu iturai ancestors.In todays Western nations, life expectancy is over 70 years-doublewhat it was in preindustrial times. Infant death rates are lower than everbefore and nearly 80 percent of al l newborn infants wi ll survive to age 65or beyond. Such vital statistics certify that the health of current popula-tions, at least in the affluent nations, is superior to that of any prior groupof humans. Accordingly, it seems counterintuitive to suggest that, incertain important respects, the collective human genome is poorlydesigned for modern life. Nevertheless, there is both epidemiologic andpathophysiologic evidence that suggests this may be so.In industr ialized nations, each persons health status is heav ily influ-enced by the interaction between his or her genetica lly controiled bio-chemis try and a collection of biobehaviora l influences that can be consid-ered lifestyle factors. These include nutrition, exercise, and exposure toharmful substances such as alcohol and tobacco. This report presentsevidence that the genetic makeup of humanity has changed little duringthe past 10,000 years, but that during the same period, our culture hasbeen transformed to the point that there is now a mismatch between ourancient, genetically controlled biology and certain important aspectsofour daily lives. This discordance is not genetic maladaptation in the termsof classic evolutionary science- it does not affect differential fertility.Rather, it promotes chronic degenerative diseases that have their mainclin ical expression in the post-reproductive period, but that togetheraccount for nearly 75 percent of the deaths occurring in affluent Westernnations.

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THE HUMAN GENOMEThe gene pool from which current humans derive theirindividual genotypes was formed during an evolutionaryexperience lasting over a billion years. The almost incon-ceivably protracted pace of genetic evolution is indicatedby paleontologic findings that reveal that an average spe-cies of late Cenozoic mammals persisted for more than amillion years [I], by biomolecular evidence indicating thathumans and chimpanzees now differ genetica lly by just1.6 percent even though the hominid-pongid divergenceoccurred seven million years ago [2], and by dentochron-ologic data showing that current Europeans are genetical-ly more l ike their Cro-Magnon ancestors than they are I/kc20th-century Africans or Asians [3]. Accordingly, it ap-pears that the gene pool has changed little since anatomi-cal ly modern humans, Homo sapiens sapiens, becamewidespread about 35,000 years ago and that, tram agenetic standpoint, current humans are sti ll late Paleolith-ic preagricu ltural hunter-gatherers.THE IMPACT OF CULTURAL CHANGESIt has been proposed that chronic degenerative disorders,sometimes referred to as the diseases of civilization,are promoted by discordance between our genetic make-up (which was selected over geologic eras, ultimately tofit the life circumstances of Paleolithic humans) and se-lected features of our current bioenvironmental milieu.The rapid cultural changes that have occurred during thepast !O,OOOyears have far outpaced any possible genet-ic adaptation, especia lly since much of this culturalchange has occurred only subsequent to the IndustrialRevolution of 200 years ago.The increasing industrialized affluence of the past twocenturies has affected human health both beneficially andadversely. Improved housing, sanitation, and medicalcare have ameliorated the impact of infection and trauma,the chief causes of mortality from the Paleolithic era until1909, w ith the result that average life expectancy is nowapproximately double what it was for preagricultural hu-mans. The importance of these positive influences canhardly be overstated; their effects have not only increasedlongevity, but also enhanced the quality of our lives incountless ways. But, on the other hand, the past centuryhas accelerated the biologic estrangement that has in-creas ingly differentiated humans from other mammalsover the entire two-million-year period since Homo habilisfirst appeared. Despite the increasing importance of cul-ture and technology during this time, the basic lifesty ieelements of Homo sapiens sapiens were st ill within thebroad continuum of general mammalian experience untilrecently. However, in todays Western nations, we haveso little need for exercise, consume foods so differentfrom those available to other mammals, and exposeourselves to such harmful agents as alcohol and tobacco

CHRONIC DEGENERATIVE DISEASES IN EVOLUTIONARY PERSPECTIVE-EATON ET AL

that we have crossed an epidemiologic boundary andentered a watershed in which disorders such as obesity,diabetes, hypertension, and certain cancers have be-come common in contrast to their rarity among remainingpreagricultural and other traditional humans.METHODSPertinent data on fitness, diet, and disease prevalence innon-industrial societies were reviewed, tabulated, and con-trasted with comparable data from industr ialized nations.The literature cited is based on studies of var ied traditionalgroups: pastoralists, rudimentary horticulturalists, and sim-ple agriculturalists, as well as technologically primitive hun-ter-gatherers. We would have preferred to ,present dataderived solely from studies of pure hunter-gatherers, sincethey are most analogous tc Paleolithic humans. Unfortu-nately, only a few such investigations have been per-formed, so that inclusion of selected non-foraging popula-tions constitutes a necessary first approximation. However,there is a continuum of human experience with regard tolifestyle factors that now affect diseaseprevalence, and onthis continuum, traditional peoples occupy positions muchcloser to those of our preagcicultural ancestors than tothose of affluent Westerners. In each case, the groupsanalyzed resemble late Paleolithic humans far more thanourselves with respect to factors (such as exercise require-ments and dietary levels of fat, sodium, and fiber) consid-ered likety to influence the prevalence of the disease entityunder consideration.THE LATE PALEOLITHIC LIFESnLEThe Late Paleolithic era, from 35,000 to 20,000 B.P.,may be considered the last time period during which thecollective human gene pool interacted with bioenviron-mental circumstances typica l of those for which it hadbeen originally se lected. It is because of this that the diet,exercise patterns, and social adaptations of that time havecontinuing relevance for us today.Nutrition. The diets of Paleotithic humans must havevaried greatly with latitude and season just as do those ofrecently studied hunter-gatherers; undoubtedly, therewere periods of relative plenty and others of shortage;certain ly there was no one universal subsistence pattern.However, the dietary requirements of all Stone Age menand women had.to be met by uncultivated vegetables andwild game exclusively; from this starting point, a numberof logically defensible nutritional generalizations can beextrapolated [4]. (1) The amount of protein; especiallyanimal protein, was very great. The mean, median, andmodal protein intake for 58 hunter-gatherer groups stud-ied in this century was 34 percent [4] and protein intake inthe Late Paleol ithic era may have been higher st ill [5,6].The current American diet derives 12 percent of its ener-gy from protein (Table I). (2) Because game animals areextremely lean, Paleolithic humans ate much less fat thando 2Oth-century Americans and Europeans, although

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more than is consumed in most Third-World countries. (3)Stone Age hunter-gatherers generally ate more polyun-saturated than saturated fat. (4) Their cholesterol intakewould ordinarily have equaled or exceeded that now com-mon in industria lized nations. (5 ) The amount of carbohy-drate they obtained would have varied inversely with theproportion of meat in their diet, but (6) in almost all casesthey would have obtained much more dietary fiber than domost Americans. (7) The availability of simple sugars,especially honey, would have varied seasonally. For atwo- to four-month period, the ir intake could have equaledthat of current humans, but for the remainder of the year itwould have been minimal. (8) The amounts of ascorbicacid, folate, vitamin B12, and iron available [7,8] to ourremote ancestors equaled, and like ly exceeded, thoseconsumed by todays Europeans and North Americans;probably this reflects a general abundance of micronutri-ents (with the possible exception of iodine in inland loca-tions). (9) In striking contrast to the pattern in todaysindustrialized nations [9], Paleolithic humans obtained farmore potassium than sodium from their food (as do allother mammals). On the average, their total daily sodiumintake was less than a gram-barely a quarter of thecurrent American average. (IO) Because they had nodomesticated animals, they had no dairy foods; despitethis, their calcium intake, in most cases, would have farexceeded that generally consumed in the 20th century.Physical Exercise. The hunter-gatherer way of life gen-erates high levels of physical fitness. Paleontologic inves-tigations and anthropologic observations of recent forag-ers [IO] document that among such people, strength andstamina are characte ristic of both sexes at all ages.Skeletal remains can be used for estimation of strengthand muscularity. The prominence of muscular insertionsites, the area of articular surfaces, and the corticalthickness and cross-sectional shape of long bone shaftsall reflect the forces exerted by the muscles acting onthem. Analyses of these features consistently show thatpreagricultural humans were more robust than their de-scendants, including the average inhabitants of todaysWestern nations. This pattern holds whether the popula-tion being studied underwent the shift to agriculture10,000 [I I] or only 1,000 [12] years ago, so it clearlyrepresents the results of habitual activity rather than ge-netic evolution. The fact that hunter-gatherers were de-monstrably stronger and more muscular than succeedingagriculturalists (who worked much longer hours) suggeststhat the intensity of intermittent peak demand on themusculoskeletal system is more important than the merenumber of hours worked for the development of muscu-larity.The endurance activi ties associated with both huntingand gathering involve considerable heat production. Thelong-standing importance of such behaviors for human-kind is apparently reflected in the unusual mechanisms for

TABLE I Late Paleolithic, Contemporary American,and Currently Recommended DietaryComoositionLate Contemporary

Paleolithic American CurrentDiet Diet Recommendations

Total dietary energy (percent)Protein 33 12 12Carbohydrate 46 46 58Fat 21Alcohol 4 (7%, l

30-P:S ratio 1.41 0.44 1.00Cholesterol (mg) 520 300-500 300Fiber (g) 100-150 19.7 30-60Sodium (mg) 690 2,300-6,900 l,lOO-3,300Calcium (mg) 1,500-2,000 740 800-1,600Ascorbic acid 440 67.7 600-W


Updated from Eaton and Konner 141. Data base now includes 43species of wild game and 153 types of wild plant food.* Inclusion of calories from alcohol would require concomitantreduction in calories from other nutrients-mainly carbohydrateand fat.P:S = polyunsaturated-to-saturated fat.

heat dissipation with which evolution has endowed us: weare among the very few animal species that can releaseheat by sweating; also, our hairless, exposed skin allowsheat to escape readily, especially during rapid movement,like running, when airflow over the skin is increased.These physiologic adaptations suggest the importance ofendurance activ ities in our evolutionary past [ 131, andevaluation of recent preliterate populations confirms thattheir daily activities develop superior aerobic fitness (Ta-bles II and Ill). Whereas actual measurements of maximaloxygen uptake capacity have been made almost exclu-sive ly on men, anthropologic observations suggest com-mensurate aerobic fitness for women in traditional cu l-tures as well [ 151.Alcoholic Beverages. Honey and many wild fruits canundergo natural fermentation, so the possibil ity that somepreagricultural persons had alcoholic beverages cannotbe excluded. However, widespread regular use of alcoholmust have been a very late phenomenon: of 95 preliteratesocieties studied in this century [ 161, fully 46, includingthe San (Bushmen), Eskimos, and Australian Aborigines,were unable to manufacture such beverages. It is estimat-ed that 7 to IO percent of the average adult Americansdaily energy intake is provided by alcohol; such levels arefar in excess of what Late Paleolith ic humans could haveconceivably obtained.In general, native alcoholic beverages are preparedperiodically and drunk immediately [ 171. Their availabilityis subject to seasonal fluctuation, and as products ofnatural fermentation, their potency is far less than that ofdistilled liquors. Their consumption is almost invariably



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TABLE I I Aerobic FitnessMaximal

Oxygen Uptake FitnessSubsistence Pattern Populat ion Average Age (ml/kg/minute) Category*

Hunter-gatherers

Rudimentary horticulturists

Simple agriculturistsPastoralists

Industrialized Westerners

* From [14].

Canadian lgloolik Eskimos 29.3Kalahari San (Bushmen) Young menVenezuelan Warao Indians Young menNew Guinea highlan d Lufas 25Mexican Tarahumara Indians 29.8Finnish Kautokeino Lapps 25-35Tanzanian Masai 32-43Canadian Caucasians 20-29Canadian Caucasians 30-39Canadian Caucasians 40-49

56.4 Superior47.1 Excellent51.2 Excellent67.0 Superior63.0 Superior53.0 Superior59.1 Superior40.8 Fair38.1 Fair34.9 Fair

TABLE III Fitness Classif ication for American M ales*

Ag e Very Poor Poor20-29 48.1

* Data modified from [ 141.

subject to strong socie tal conventions that iimit the fre-quency and place of consumption, degree of permissibleintoxication, and types of behavior that wil l be tolerated. Insmall-scale traditional preliterate societies, drinking tendsto be ritualized and cultura lly integrated [ 181. Solita ry,addictive, pathologic drinking behavior does not occur toany significan t extent; such behavior appears to be aconcomitant of complex, modern, industria lized societies[171.Tobacco Abuse. Recent hunter-gatherers such as theSan (Bushmen), Ache, and Hadza had no tobacco prior tocontact with more technologically advanced cultures, butthe Australian Aborig ines chew wild tobacco, so seasonaluse by Paleolithic humans in geographically limited areascannot be excluded. However, widespread tobacco usagebegan only after the appearance of agriculture in theAmer icas, perhaps 5,000 years ago. With European con-tact, the practice spread rapidly throughout the world.Pipes and cigars were the only methods employed forsmoking until the mid-19th century, when cigarettes fi rstappeared. Cigarettes had three crucial effects: they dra-matica lly increased per capita consumption among men;after World War I, they made smoking socially acceptablefor women; and they made inhalation of smoke the rulerather than the exception. Although the hazards of chew-

ing tobacco, snuff, pipes, and cigars are not insignificant,the major impact of tobacco abuse is a post-cigarettephenomenon of this century.

HOW ALTERED LIFESTYLE FACTORS AFFECTDISEASE PREVALENCEIn many, if not most, respects, the health of humans intodays affluent countries must surpass that of typicalStone Agers. Infant mortality, the rate of endemic infec-tious disease (especially parasitism), and the prevalenceof post-traumatic disab ility were all far higher 25,000years ago than they are at present. Sti ll, pathophysiologicand epidemiologic research conducted over the past 25years supports the concept that certain discrepanciesbetween our current lifesty le and that typical of preagricul-tural humans are important risk factors for the chronicdegenerative diseases that account for most mortality intodays Western nations. These diseases of civilizationare not new: Aretaeus described diabetes 2,000 yearsago, atherosclerosis has been found in Egyptian mum-mies, Paleolith ic Venus statuettes show that Cro-Ma-gnons could be obese, and the remains of 500-year-oldEskimo burials reveal that cancer afflicted hunter-gather-ers isolated from contact with more technologically ad-

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TABLE IV Triceps Skinfold Measurem ents in Males*Subsistence Pattern Population Ag e Thickness (mm)

Hunter-gatherers Australian Aborigines 25-29 4.7Kalahari San (Bushmen) Young men 4.6Canadian lgloolik Eskimos 20-29 4.4Congo Pigmies 20-29 5.5Tanzanian Hadza 25-34 4.9

Rudimentary horticulturists New Guinea TukisentaVenezuelan Warao IndiansNew Guinea BiakSolomon IslandersNew Guinea LufaSurinam Trio Indians

16-37Young men

2519-7021-35

21 and over35

Young men21 and over

20-30

5.05.95.35.45.16.0

Simple agriculturists

Mean

Peruvian Quechua IndiansJapanese AinuTarahumara IndiansRural Ethiopea n peasants

4.05.36.35.35.2

Industrialized Westerners Canadian Caucasians 20-29 11.2American Caucasians 18-24 9.0

Mean 10.1* As initially submitted, the manuscript included 236 supportive references. A copy of the original manuscript can be obtained by sending astamoed ($1.80). addressed envelooe (to accommodate 47 8% X 11 pages) to: EatonlKonnerlShostak, Department of Anthropology,Emo;y University, Atlanta, Georgia 30322.

van& cultures [19]. However, the lifestyle common in2Oth-century affluent Western industrialized nations hasgreatly increased the prevalence of these and other con-ditions. Before 1940, diabetes was rare in AmericanIndians [20], but now the Pimas have one of the worldshighest rates [21]; hypertension was unknown in EastAfricans before 1930, but now it is common [22]; and in19 12, primary malignant neoplasms of the lungs wereconsidered among the rarest forms of disease [23]. It isnot only because persons in industrialized countries livelonger that these illnesses have assumed new impor-tance. Young persons in the Western world commonlyharbor developing asymptomatic atherosclerosis [24],whereas youths in technologically primitive cultures donot [25,26]; the age-related rise in blood pressure sotypica l of affluent society is not seen in unacculturatedgroups [27]; and older members of preliterate culturesremain lean [28-301 in contrast to the increasing propor-tion of body fat that is almost universal among affluentWesterners [3 11.Obesity. Obesity is many disorders: its causes-genetic, neurochemical, and psychologic-interact in acomplex fashion to influence body energy regulation.Superimposed upon this underlying etiologic matrix, how-ever, are salient contrasts between the Late Paleolithicera and the 20th century that increase the likelihood ofexcessive weight gain (Table IV). (1) Most of our food i scalo rica lly concentrated in comparison with the wild game

and uncultivated fruits and vegetables that constituted thePaleolithic diet [4]. In general, the energy-satiety ratio ofour food is unnaturally high: in eating a given volume,,enough to create a feeling of fullness, Paleolithic humanswere like ly to consume fewer calor ies than we do today[32]. (2) Before the Neolithic Revolution, thirsty humansdrank water; most beverages consumed today provide asignificant caloric load while they quench our thirst. (3)The low levels of energy expenditure common in todaysaffluent nations may be more important than excessiveenergy intake for development and maintenance of obesi-ty [33]. Total food energy intake actually has an inversecorrelation with adiposity, but obese persons have pro-portionately even lower levels of energy expenditure[331-a low energy throughput state. Increased levelsof phys ical exercise raise energy expenditure proportion-ately more than ca loric intake [34] and may lower thebody weight set point.Diabetes Mellitus. Mortality statistics for New York Citybetween 1866 and 1923 show a distinct fa ll in the overa lldeath rate, but a steady, impressive rise in death ratesfrom diabetes. For the over-45 age group, there was alo-fold increase in the diabetic death rate during thisperiod [35]. This pattern anticipated the more recentexperience of Yemenite Jews moving to Israel [36], Alas-kan Eskimos [37], Australian Aborigines [38], AmericanIndians [39], and Pac ific Islanders of Micronesian, Mela-nesian, and Polynesian stock [40]. In these groups, dia-

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TABLE V Diabetes Prevalence*Subsistence Pattern Populat ion Prevalence (percent)

Hunter-gatherers



PastoralistsMean

Alaskan Athabaskan IndiansGreenland EskimosAlaskan EskimosPapua, New Guinea MelanesiansLoyalty Island MelanesiansRural MalaysiansRural villagers, IndiaNew Yemen ite immigrants, IsraelRural Melanesians, New Caledon iaPolynesians on PukapukaRural FigiansNomadic Broayas, North Africa

Industrialized Westerners Australia, Canada, Japan, United States

1.31.21.90.92.01.81.20.11.51.00.60.01.1

Range 3.0-lO.Otl See footnote to Table IV.t Data are from [41].

betic prevalence, if not the actual mortality rate, has risenrapidly and it has been observed that obesity and maturity-onset diabetes are among the first disorders to appearwhen unacculturated persons undergo economic devel-opment. At present, the overa ll prevalence of non-insulin-dependent d iabetes among adults in industrialized coun-tries ranges from 3 to 10 percent [4 I], but among recent-ly studied, unacculturated native populations that havemanaged to continue a traditional lifestyle, rates for thisdisorder range from nil to 2.0 percent (Table V).Like obesity, d iabetes mellitus is a family of relateddisorders, each of which reflects the interplay of geneticand environmental influences. But again, in comparisonwith Paleolithic experience, the lifestyle of affluent, indus-trialized countries potentiates underlying causal factors topromote maturity-onset diabetes by severa l mechanisms.(1) A 1980 World Health Organization expert committeeon diabetes concluded that the most powerful risk factorfor type II diabetes is obesity [42]. The obese personscommon in Western nations have reduced numbers ofcellular insulin receptors. They manifest a relative tissueresistance to insulin [43], and therefore their blood insulinlevels tend to be higher than those of lean persons. (2)Conversely, high-level physical fitness, characteristic ofaboriginal persons, is associated with an increased num-ber of insulin receptors and better insulin binding [44];these effects enhance the bodys sensi tivity to insul in[45]. Serum insulin levels are typically low in hunter-gatherers [46] and trained athletes [44]; cellula r insulinsensitivity can be improved by physical conditioning thatincreases cardiorespiratory fitness [47]. This effect isindependent from [47], but may be augmented by, anassociated effect on body weight and composition [43].(3) Diets containing ample amounts of non-nutrient fiber

and complex carbohydrate have been shown to lowerboth fasting and post-prandial blood glucose levels [48].Diets with high intakes of fiber and complex carbohy-drates are the rule among technologically primitive societ-ies, but are the exception in Western nations. Their rec-ommendation by the American Diabetes Assoc iation un-derscores the merit of these Paleolithic dietary practices.Hypertension. Across the globe, there are many cul-tures whose members do not have essential hypertensionnor experience the age-related rise in average bloodpressure that characterizes populations living in industrial-ized Western nations. These persons are not geneticallyimmune from hypertension since, when they adopt aWestern style of life, either by migration or acculturation,they develop, first, a tendency for their blood pressure torise with age and, second, an increasing incidence ofclin ica l hypertension [27,49]. These normotensive cul-tures exist in varied climatic circumstances-in the arc-tic, the rain forest, the desert, and the savanna-but theyshare a number of essential similarities, each of which isthe reciprocal of a postulated causal factor for hyperten-sion. These include diets low in sodium and high in potas-sium [50]. In addition, the pastoralists and those groupsstil l subsisting as hunter-gatherers have diets that providea high level of calcium [51]. These persons are slender[52], aerobically fit [53], and, at least in their unacculturat-ed state, have limited or no access to alcoholic beverages

More than 90 percent of the hypertension that occursin the United States and similar nations is idiopathic oressen tial in nature. Many theories about the origin ofthis hypertension have been advanced and it may repre-sent a family of conditions that share a final commonpathway resulting in blood pressure elevation. Although i ts

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TABLE VI Serum Cholesterol Values*Subsistence Pattern Popula tion Gender

Cholesterol ValueWdl)

Hunter-gatherers Tanzanian Hadza



Kalahari San (Bushmen)Kalahari San (Bushmen)Congo PygmiesAustralian AboriginesCanadian EskimosPalau MicronesiansNew Guinea ChimbuNew Guinea WabagBrazilian Xavante IndiansBrazalian Kren-Akorore IndiansSolomon Islands AitaSolomon Islands KwaioNew Guinea BomaiNew Guinea Yongamuggl

Mexican Tarahumara IndiansRural SamoansGuatemalan Mayan Indians

Pastoralists Kenyan SamburuKenyan Masai

MF

MFMF

MF

MF

MFMFMFMFMFMFMFMF

114105130109101III146132141160170130144107121100135142114125130I40139140136139167I80132143166135

* See footnote to Table IV.

causes remain obscure, its occurrence in most casesprobably reflects the interaction between individual genet-ic predispos ition and pertinent modifiable lifesty le charac-teristics. Accordingly, a promising approach to its preven-tion is suggested by the practices of traditional personswho are spared this disorder; the common features theyshare reflect components of our ancestral lifestyle .Atherosclerosis. Clinical and postmortem investigationsof arctic Eskimos [55X17], Kenyan Kikuyu [58], SolomonIslanders [59], Navajo Indians [60], Masai pastoralists[6 11, Australian Aborigines [62], Kalahari San (Bushmen)[30], New Guinea highland natives [63], Congo Pygmies[64], and persons from other preliterate societies revealthat, in the recent past, they experienced little or nocoronary heart disease. This is presumably because riskfactors for development of atherosclerosis were so un-common in such cultures. Like our Paleolithic ancestors,they traditionally lacked tobacco, rarely had hypertension,and led lives characterized by considerable physical exer-tion. In addition, their serum choles terol leve ls were low

(Table VI) . The experience of hunter-gatherers is of spe-cial interest in this regard: their diets are low in total fatand have more polyunsaturated than saturated fatty acids(a high polyunsaturated-to-saturated fat ratio), but containan amount of cholesterol similar to that in the currentAmerican diet. The low serum cholesterol levels foundamong them suggest that a low total fat intake togetherwith a high polyunsaturated-to-saturated fat ratio cancompensate for relative ly high total cholesterol intake[65]. This supposition is supported by the experience ofSouth African egg farm workers. Their diets include amean habitual cholesterol intake of 1,240 mg per day, butfat (polyunsaturated-to-saturated fat ratio = 0.78) pro-vides only 20 percent of total energy and their serumcholestero l levels average 18 1.4 mg/dl (with high-densitylipoprotein cholesterol = 61.8 mg/dl) [66].

The adverse changes that occur in atherosclerotic riskfactors when persons from societies with little such dis-ease become westernized recapitulate the pattern ob-served for the other diseases of civilization. The experi-



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CHRONIC DEGENERATIVE DISEASES IN. EVOLUTIONARY PERSPECTIVE--EATON ET AL

ences of Japanese [67], Chinese [68], and Samoans [69]migrating to the United States, of Yemenite Jews to Israel[70], and of Greenland Eskimos to Denmark [7 I] parallelthose of Kalahari Bushmen [72], Solomon Islanders [59],Ethiopean peasants [73], Canadian Eskimos [74], Austra-lian Aborig ines [38], and Masai Pasto ralists [75] who havebecome increasingly westernized in their own countries.Abnormalities of coagulability may contribute to boththe development and the acute clin ical manifestations ofatherosclerosis [76]. Platelet function has received con-siderable attention in this respect [77]. Fibrinolytic activityis enhanced by phys ical exercise [78], but decreased bysmoking cigarettes [79], obesity [80], and hyperlipopro-teinemia [81], so it is not surpris ing that preliterate peo-ples have more such activity than do average Westerners[82,83]. Platelet aggregation is influenced by hypercho-lesterolemia [84], by physical exercise [85], and by bloodlevels of long-chain polyunsaturated omega-3 class fattyacids [86]. The latter, in turn, are related to dietary intakeof fats containing these constituents; fish oils have espe-cia lly high concentrations of such fatty acids. Meat fromdomesticated animals i s deficient in this regard [87] butthe wild game consumed by our ancestors contained amoderate amount [4,87], poss ibly enough to induce bloodlevels comparable to those of the Japanese [88] or Dutch[89], although almost certa inly not those of the Eskimos1711.

acculturation of western and central Arctic Eskimos hasled to an increase in overall cancer morbidity togetherwith marked change in the relative frequency of spec ifictumor types. Between 1950 and 1980, the number ofproven salivary gland cancers decreased by two thirds,whereas lung cancers increased 550 percent [95]. Fur-thermore, tumor incidence in laboratory animals can bereadily altered by manipulating external factors rangingfrom radiation exposure to dietary composition.

On the basis of these observations, epidemiologistshave argued that it should be theoretically possible toreduce site-specific incidence for each type of cancer tothe lowest rate found in any population [96]. By summingthe lowest national or regional rates observed for eachcancer site, basal or naturally occurring minimal inci-dence rates can be developed. When these minimalrates are compared with the rates observed in countrieswhere each type of tumor is common, it appears that from70 to 90 percent of cancers are the result of environ-mental influences and hence potentially preventable[94,96].

Coronary atherosclerosis was apparently uncommonin the United States before about 1930 [90,91], but itsimportance thereafter rapidly increased to a peak in the196Os, then began a gradual decline. Whereas manyfactors ranging from changes in the diagnostic classifica-tion codes to improvements in treatment are involved inthese trends, both the epidemic and the decline havebeen linked to alterations in lifestyle-initia lly away fromand subsequently back toward the pattern that prevailedamong preagricultural humans [92].Cancer. The perception of cancer as a disease prim arilyrelated to the environment has been progress ivelystrengthened over the past decade [93]. Internationalstudies reveal large differences in cancer incidence ratesbetween countries; for example, age-standardized analy-ses reveal that Canadian women have seven times morebreast cancer than do non-Jewish women in Israel [94].Genetic variation cannot account for these major differ-ences, since groups migrating from an area with a char:acteristic pattern of cancer incidence rates acquire differ-ent rates typical of their new geographic location within afew generations. Age-standardized data show that Japa-nese men in Hawaii have 11 times more prostatic cancerthan do Japanese men in Japan and that black Americanshave 10 times more colon cancer than do black Nigerians[94]. Also, there have been large changes in incidencerates for many types of cancer within genetically stablepopulations: in Ireland, lung cancer mortality increased177 percent between 1950 and 1975 [94]. In Canada,

The factors considered most like ly to affect the devel-opment of cancer are tobacco abuse [93,97] and nutri-tional influences [98]. Extensive tobacco usage (and theregular consumption of alcoholic beverages) postdate theAgricultural Revolution, whereas current cancer-preven-tive nutritional recommendations [99,-l OO]-to avoidobesity, reduce total fat intake, consume a wide variety offruits and vegetables (including considerable dietary fiber,vitamin C, and vitamin A or beta-carotene), and to drinkalcohol only in moderation if at all-are a fairly accurate,if incomplete, summary of Paleolithic nutritional prac-tices.CONCLUSIONThe diseases considered, as well as others ranging fromdental caries to diver ticulosis, share important features. Ineach case, the condition is uncommon, rare, or almostunknown in cultures whose pertinent essential featuresmimic those of our Late Paleoli thic ancestors. However,in each instance, the prevalence of disease increasesdramatically when the previously unaffected societyadopts a Western lifestyle, whether by migration or accul -turation. Furthermore, extensive pathophysiologic re-search has identified bioenvironmental factors that arelike ly etiologic agents for each condition. Such factors(e.g., caloric concentration, tobacco abuse, sedentaryliving, diets high in fat and salt, and so on) are pervasive inaffluent industr ialized society, but not in traditional cu l-tures where the lifestyle is, in important ways, simi lar tothat of preagricu ltural humans-similar to that for whichthe current human genome was selected. These consid-erations are consistent with the hypothesis that discor-dance between our genes and the affluent 20thcenturylifestyle (defined to include diet, exercise, and exposure toharmful substances) accentuates underlying causal fac-

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tors and thereby promotes the chronic diseases of civili-zation.Of course, cancer, atherosclerosis, non-insulin-depen-dent diabetes mellitus, and other afflictions of affluenceare all disorders whose clin ica l manifestations becomeincreasingly common with advancing age; might not theprevalence of these conditions in 20th-century Westernnations result simply from the unprecedented life expec-tancy that characterizes these countries? The popula-tions greater age must certainly be a contributing factor,but the failure of young persons in traditional cultures toexhibit the early stages of these chronic diseases[58,10 I] contrasts with the experience of youths in West-ern nations [24], indicating that age is not the primarydeterminant. Furthermore, those persons in traditionalsocieties who do reach age 60 and beyond remain lean[28-301 and normotensive [271, while cl inical [57] andpostmortem [58] examinations reveal little or no signi fi-cant coronary atherosclerosis. Findings like these suggestthat chronic degenerative diseases need not be the inevi-table consequence of advancing years.

Evolution has endowed Homo sapiens with the ability toadapt and thrive under an extraordinary range of condi-tions, and this adaptability allows us to benefit enormously

from the manifold advantages of todays civilization. In20thcentury industria lized nations, parameters such asinfant mortality, childhood growth rates, and average lifeexpectancy all indicate a state of public health far exceeding that which was obtained in the Stone Age or at anytime thereafter until the current century. Indeed, morethan half the persons who have ever lived beyond age 65are alive today. Nevertheless, we can stil l profit from theexperience of our remote ancestors. We still carry theirinheritance-genes selected for their way of life, notours. Despite the achievements of science and technolo-gy, we remain collectively fearful of diseases that avail-able evidence suggests were uncommon, rare, or un-known in the Late Paleolithic era. In order to regainrelative freedom from these i llnesses, we need to take astep backward in time. For each disorder, we may antici-pate increasingly sophisticated and effective treatments,but the crucial corrective measure will almost certainly beprevention. This will entail reintroduction of essential ele-ments from the lifestyle of our Paleolithic ancestors.ACKNOWLEDGMENTWe are grateful to Debra Fey and Sharon Minors for theirassistance in preparing this manuscript.


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