TheProtein DebateLoren Cordain, PhDT. Colin Campbell, PhDPERFORMANCE MENUJOURNAL OF NUTRITION & ATHLETIC EXCELLENCE
IntroductionProtein plays a litany of roles in living systems: structural elements, peptide hormones,cell recognition, antibodies the list is staggering and continues to grow as ourunderstanding of biology expands. What, however, is the role of dietary proteinin health and disease in humans? Is the source, type and quantity intimately anddirectly tied to optimal physical development and continued wellbeing? Is itcausative or preventative of disease? How do we know, and how can we know?One would think this question should be straightforward and easily answered; asyou will soon see the question is anything but simple! In the pages that follow, twoscientists at the top of their respective ﬁelds--Dr. T. Colin Campbell, Professor ofNutritional Biochemistry at Cornell University, author of The China Study and Dr.Loren Cordain Professor, Department of Health & Exercise Science, Colorado StateUniversity, author of The Paleo Diet—make their competing cases for the role ofdietary protein in health and disease.Contents3 The Evolutionary Basis for the Therapeutic Effects of HighProtein DietsLoren Cordain, PhD17 How Much Protein is Needed?T. Colin Campbell, PhD21 Rebuttal to: How Much Protein is Needed?Loren Cordain, PhD26 Rebuttal to: The Evolutionary Basis for the TherapeuticEffects of High Protein DietsT. Colin Campbell, PhD
The Evolutionary Basis for theTherapeutic Effects of High Protein DietsLoren Cordain, Ph.D.ProfessorDepartment of Health and Exercise ScienceColorado State UniversityFort Collins, CO 80523
IntroductionAlthough humanity has been interested in diet andhealth for thousands of years, the organized, scientiﬁcstudy of nutrition has a relatively recent past. Forinstance, the world’s ﬁrst scientiﬁc journal devotedentirely to diet and nutrition, The Journal of Nutritiononly began publication in 1928. Other well knownnutrition journals have a more recent history still: TheBritish Journal of Nutrition (1947), The American Journalof Clinical Nutrition (1954), and The European Journalof Clinical Nutrition (1988).The ﬁrst vitamin was“discovered” in 1912 and the last vitamin (B12) wasidentiﬁed in 1948 (1). The scientiﬁc notion that omega3 fatty acids have beneﬁcial health effects dates backonly to the late 1970’s (2), and the characterization ofthe glycemic index of foods only began in 1981 (3).Nutritional science is not only a newly establisheddiscipline, but it is also a highly fractionated, contentiousﬁeld with constantly changing viewpoints on bothmajor and minor issues that impact public health.For example, in 1996 a task force of experts from theAmerican Society for Clinical Nutrition (ASCN) and theAmerican Institute of Nutrition (AIN) came out with anofﬁcial position paper on trans fatty acids stating,“We cannot conclude that the intake of trans fattyacids is a risk factor for coronary heart disease” (4).Fast forward 6 short years to 2002 and the NationalAcademy of Sciences, Institute of Medicine’s reporton trans fatty acids (5) stating,“Because there is a positive linear trendbetween trans fatty acid intake and total andLDL (“bad”) cholesterol concentration, andtherefore increased risk of cardiovascularheart disease, the Food and Nutrition Boardrecommends that trans fatty acid consumptionbe as low as possible while consuming anutritionally adequate diet”.These kinds of complete turnabouts anddivergence of opinion regarding diet and health arecommonplace in the scientiﬁc, governmental andmedical communities. The ofﬁcial U.S. governmentalrecommendations for healthy eating are outlined inthe “My Pyramid” program (6) which recently replacedthe “Food Pyramid”, both of which have been loudlycondemned for nutritional shortcomings by scientistsfrom the Harvard School of Public Health (7). Dietaryadvice by the American Heart Association (AHA) toreduce the risk of coronary heart disease (CHD) is tolimit total fat intake to 30% of total energy, to limitsaturated fat to 10% of energy and cholesterol to 300 mg/day while eating at least 2 servings of ﬁshper week (8). Although similar recommendationsare proffered in the USDA “My Pyramid”, weekly ﬁshconsumption is not recommended because theauthors of these guidelines feel there is only “limited”information regarding the role of omega 3 fatty acidsin preventing cardiovascular disease (6). Surprisingly,the personnel makeup of both scientiﬁc advisoryboards is almost identical. At least 30 million Americanshave followed Dr. Atkins advice to eat more fat andmeat to lose weight (9). In utter contrast, Dean Ornishtells us fat and meat cause cancer, heart disease andobesity, and that we would all would be a lot healthierif we were strict vegetarians (10). Who’s right andwho’s wrong? How in the world can anyone makeany sense out of this apparent disarray of conﬂictingfacts, opinions and ideas?In mature and well-developed scientiﬁc disciplinesthere are universal paradigms that guide scientists tofruitful end points as they design their experiments andhypotheses. For instance, in cosmology (the study ofthe universe) the guiding paradigm is the “Big Bang”concept showing that the universe began with anenormous explosion and has been expanding eversince. In geology, the “Continental Drift” modelestablished that all of the current continents at onetime formed a continuous landmass that eventuallydrifted apart to form the present-day continents.These central concepts are not theories for eachdiscipline, but rather are indisputable facts thatserve as orientation points for all other inquiry withineach discipline. Scientists do not know everythingabout the nature of the universe, but it is absolutelyunquestionable that it has been and is expanding. Thiscentral knowledge then serves as a guiding templatethat allows scientists to make much more accurateand informed hypotheses about factors yet to bediscovered.The study of human nutrition remains an immaturescience because it lacks a universally acknowledgedunifying paradigm (11). Without an overarchingand guiding template, it is not surprising that there issuch seeming chaos, disagreement and confusionin the discipline. The renowned Russian geneticistTheodosius Dobzhansky (1900-1975) said, “Nothing inbiology makes sense except in the light of evolution”(12). Indeed, nothing in nutrition seems to make sensebecause most nutritionists have little or no formaltraining in evolutionary theory, much less humanevolution. Nutritionists face the same problem asanyone who is not using an evolutionary model toevaluate biology: fragmented information and nocoherent way to interpret the data.All human nutritional requirements like thoseof all living organisms are ultimately geneticallydetermined. Most nutritionists are aware of this basicconcept; what they have little appreciation for is theprocess (natural selection) which uniquely shapedour species’ nutritional requirements. By carefullyexamining the ancient environment under which ourgenome arose, it is possible to gain insight into ourpresent day nutritional requirements and the range offoods and diets to which we are genetically adaptedvia natural selection (13-16). This insight can then beemployed as a template to organize and make senseout of experimental and epidemiological studies ofhuman biology and nutrition (11).THE PERFORMANCE MENU 4
The Dietary Protein Conundrum:How Much is Enough?An important dietary issue that has come under debatein recent years is the safety of high protein diets andtheir long term inﬂuence upon health and well being(17, 18). In the current U.S. diet the average proteinintake is 98.6 g/day (15.5 % of total energy) for menand 67.5 g/day (15.1 % of total energy) for women(19). Animal products provide approximately 75 % ofthe protein in the U.S. food supply followed by dairy,cereals, eggs, legumes, fruits and vegetables (20).Diets containing 20 % or more of their total energyas protein have been labeled “high protein diets”and those containing 30% or more energy as proteinhave been dubbed “very high protein diets” (18).Accordingly, a “high protein diet” for the averageU.S. male daily energy intake (2,618 kcal (19)) wouldcontain between 125 to 186 grams of protein per dayand for the average female (1,877 kcal (19)) between89 to 133 grams of protein per day.At this point, it should be noted that there is aphysiological limit to the amount of protein that canbe ingested before it becomes toxic (14, 21). Abyproduct of dietary protein metabolism is nitrogen,which in turn is converted into urea by the liver andthen excreted by the kidneys into the urine. The upperlimit of protein ingestion is determined by the liver’sability to synthesize urea. When nitrogen intake fromdietary protein exceeds the ability of the liver tosynthesize urea, excessive nitrogen (as ammonia) spillsinto the bloodstream causing hyperammonemia andtoxicity (14, 21). Additionally excess amino acids fromthe metabolism of high amounts of dietary proteinmay become toxic by entering the circulation causinghyperaminoacidemia (14, 21).The avoidance of the physiological effects ofprotein excess has been an important factor in shapingthe subsistence strategies of hunter-gatherers (22- 24).Multiple historical and ethnographic accounts havedocumented the deleterious health effects that haveoccurred when humans were forced to rely solely uponthe fat depleted, lean meat of wild animals (22). Excessconsumption of dietary protein from the lean meats ofwild animals leads to a condition referred to by earlyAmerican explorers as “rabbit starvation” which initiallyresults in nausea, then diarrhea and eventual death(22). Clinical documentation of this syndrome is virtuallynon-existent, except for a single case study (25).Using known maximal rates of urea synthesis (MRUS)in normal subjects [65 mg N/h - kg (body weight )0.75] (range 55-76), it is possible to calculate the maximalprotein intake, beyond which will exceed MRUS andresult in hyperammonemia and hyperaminoacidemia(21). The mean maximal protein intake for the averageweight U.S. male (189.4 lbs (26)) is then 270 g/day(range 233-322 g/day), and for an average weightfemale (162.8 lbs (26)), 246 g/day (range 208-288 g/day). Consequently, “very high protein diets” for theaverage U.S. male could range from 187 to 270 g/dayand for females, 134 to 246 g/day.So let’s summarize a few key points. The averageprotein intake in the U.S. is about 15 % of the normal dailycaloric intake. Diets labeled as “high protein” contain20-29 % protein of the normal daily caloric intake, anddiets with 30-40 % protein are branded “very highprotein”. It should be pointed out that this categorizationis completely arbitrary and based almost entirely uponcomparisons to the U.S. norm. A salient question froman evolutionary perspective would be, “Is the averageU.S. protein intake necessarily average or normal forour species?” For example, blood pressure in the U.S.and most other westernized countries is considered“normal” when systolic pressure is 120 mm Hg anddiastolic pressure is 80 mm Hg. However, in many nonwesternized people these values would be higher thannormal. Consider the data in Figure 1 below showingblood pressure in the Yanomamo Indians of Brazil, anon-salt consuming society. Not only is blood pressurelower than normal western values, but it stays uniformthroughout life and does not rise with age (27).Figure 1. Blood pressure in a group of 506 Brazilian IndiansIn order to objectively answer the question whetheror not high protein diets have detrimental or therapeutichealth effects compared to the U.S. norm (15 % totalenergy), it may be useful to frame this question inan evolutionary perspective before examining theexperimental and epidemiological evidence.High Protein Diets:The Evolutionary EvidenceThe Fossil EvidenceA number of lines of evidence suggest that meateating and high protein diets have been a componentof human nutrition since the very origins of our genusHomo. Beginning approximately 2.6 million years ago(MYA), the hominin species that eventually led to HomoTHE PERFORMANCE MENU 5
began to include more animal food in their diet. Anumber of lines of evidence support this viewpoint. First,the very ﬁrst stone tools (Oldowan lithic technology)appear in the fossil record 2.6 MYA (28), and there isclear cut evidence to show that these tools were usedto butcher and disarticulate animal carcasses (29, 30).Stone tool cut marks on the bones of prey animals andevidence for marrow extraction appear concurrentlyin the fossil record with the development of Oldowanlithic technology by at least 2.5 MYA (Figure 2) (30). It isnot entirely clear which speciﬁc early hominin speciesor group of species manufactured and used theseearliest of stone tools; however, Australopithecus garhiis a likely candidate (30, 31).The development of stone tools and the increaseddietary reliance on animal foods allowed early Africanhominins to colonize northern latitudes outside ofAfrica where plant foods would have been seasonallyrestricted. Early Homo skeletal remains and Oldowanlithic technology appear at the Dmanisi site in theRepublic of Georgia (40 N) by 1.75 MYA (32), andmore recently Oldowan tools dating to 1.66 MYA havebeen discovered at the Majuangou site in North China(40 N) (33). Both of these tool-producing homininswould likely have consumed considerably moreanimal food than pre-lithic hominins living in moretemperate African climates, and it is likely the majorityof their daily energy was obtained from animal foodsduring winter and early spring when plant food sourceswould have been scarce or unavailable.analogous to those of obligate carnivores such asfelines. Carnivorous diets reduce evolutionary selectivepressures that act to maintain certain anatomicaland physiological characteristics needed to processand metabolize high amounts of plant foods. In thisregard, hominins, like felines, have experienced areduction in gut size and metabolic activity along witha concurrent expansion of brain size and metabolicactivity as they included more energetically denseanimal food into their diets (16, 34, 35). Further, similarto obligate carnivores (36), humans maintain aninefﬁcient ability to chain elongate and desaturate 18carbon fatty acids to their product 20 and 22 carbonfatty acids (37). Since 20 and 22 carbon fatty acids areessential cellular lipids, then evolutionary reductions indesaturase and elongase activity in hominins indicatethat preformed dietary 20 and 22 carbon fattyacids (found only in animal foods) were increasinglyincorporated in lieu of their endogenously synthesizedcounterparts derived from 18 carbon plant fatty acids.Finally, our species has a limited ability to synthesizethe biologically important amino acid, taurine, fromprecursor amino acids (38, 39), and vegetariandiets in humans result in lowered plasma and urinaryconcentrations of taurine (40). Like felines (41, 42) theneed to endogenously synthesize taurine may havebeen evolutionarily reduced in humans becauseexogenous dietary sources of preformed taurine(found only in animal food) had relaxed the selectivepressure formerly requiring the need to synthesize thisconditionally essential amino acid.Another genetic adaptation to a highmeat diet involves the metabolism ofpurines. Purines are the nitrogenous basepairs which form the structural cross rungmolecules of both DNA and RNA. As DNAand RNA are broken down within cells,the purines then can be metabolizedinto uric acid by the liver and a few othertissues within the body. The liver receivespurines from two sources: 1) the diet, and2) the daily breakdown of the body’s owntissues. About 2/3 of the daily purine loadcomes from the body’s turnover of cells,while 1/3 comes from the diet (43). Whenthe combined purine load (from bothdiet and turnover of the body’s own cells)exceeds the kidney’s ability to excrete it,blood concentrations of uric acid rise,thereby increasing the risk for gout, aFigure 2. The earliest evidence for meat and marrow extraction datingpainful disease caused by formation ofto 2.5 million years ago (30).uric acid crystals in the joints. Althoughhigh protein, meat based diets containhigh amounts of purines and wouldbe expected to promote gout symptoms, proteinThe Genetic Evidenceingestion actually decreases blood uric acid levelsIn addition to the fossil evidence suggesting a trendby increasing uric acid excretion (44). This seeminglyfor increased animal food consumption, hominins mayparadoxical effect occurs because the kidneyhave experienced a number of genetic adaptationsincreases its excretion of uric acid when faced withto animal-based diets early in our genus’s evolutionelevated dietary purines (45). But more importantly,THE PERFORMANCE MENU 6
over the course of evolution, humans have evolveda genetic mutation which tends to prevent uric acidsynthesis in the liver. Humans avoid the overproductionof uric acid in the face of increasing dietary purineintake from meats by decreasing the activity of anenzyme called xanthine oxidoreductase (46), a keycatalyst in the ﬁnal synthesis of uric acid. Comparedto other animals, xanthine oxidase activity is almost100 times lower in humans (47). This evolutionaryadaptation has occurred because the gene codingfor xanthine oxidoreductase has been repressed (48).The ﬁnal proof of the pudding has been borne outby dietary interventions showing that high protein,low glycemic load diets actually normalized serumuric acid concentrations in 7 of 12 gout patients andsigniﬁcantly decreased gout attacks (49).The Isotopic Fossil EvidenceSince the evolutionary split between hominins andpongids (apes) approximately 7 million years ago, theavailable evidence shows that all species of homininsate an omnivorous diet composed of minimallyprocessed, wild-plant, and animal foods. In supportof this view is the omnivorous nature of chimpanzees,the closest living pongid link to hominins. Althoughchimpanzees (Pan paniscus and Pan troglodytes),our genetically closest nonhuman relatives, primarilyconsume a frugivorous diet, they still eat a substantialamount of meat obtained throughout the year fromhunting and scavenging (50-52). Observationalstudies of wild chimpanzees demonstrate that duringthe dry season meat intake is about 65 g per day foradults (51). Accordingly, it is likely that the very earliesthominins would have been capable of obtaininganimal food through hunting and scavenging in amanner similar to chimpanzees.Carbon isotope data also support the notion thatearly hominins were omnivorous. By about 3 millionyears ago MYA Australopithecus africanus obtaineda signiﬁcant portion of food from C4 sources (grasses,particularly seeds and rhizomes; sedges; invertebrates,including locusts and termites; grazing mammals;and perhaps even insectivores and carnivores)(53).Other fossils of early African hominins, includingAustralopithecus robustus and Homo ergaster,maintain carbon isotope signatures characteristic ofomnivores (54, 55). The ﬁnding of C4 in Australopithecusrobustus fossils refutes the earlier view that this homininwas vegetarian (54).There is little evidence to the contrary that animalfoods have always played a signiﬁcant role in the dietsof all hominin species. Increased reliance on animalfoods not only allowed for enhanced encephalization(brain expansion relative to body weight) and itsconcomitant behavioral sophistication (16, 34, 35), butthis dietary practice also permitted colonization of theworld outside of Africa. An unresolved issue surroundinghominin diets is the relative amounts of plant andanimal foods that were typically consumed.Before the advent of Oldowan lithic technologyabout 2.6 MYA quantitative estimates of hominin energyintake from animal food sources are unclear, other thanthey were likely similar to, or greater than, estimatedvalues (4%–8.5% total energy) for chimpanzees (51,56)). A
Diets containing 20 % or more of their total energy as protein have been labeled “high protein diets” and those containing 30% or more energy as protein have been dubbed “very high protein diets” (18). Accordingly, a “high protein diet” for the aver
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