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H. N. MUNRO Health-Related Aspects of Animal Products for Human Consumption I N T RODU CT I ON The human race is dependent on a supply of foods that resects two aspects in the development of man, aspects that are quite dissimilar in time scale. First, man has inherited requirements for nutrients that date back to the earliest animal cells, which emerged about 1 billion years ago (Munro, 19691. An examination of the nutrient needs of animal cells from single-celled protozoa through insects, fish, birds, and mammals, including man shows a strong qualitative similarity in requirements. From the constancy of this pattern, it can be concluded that the earliest animal cells must have eliminated the DNA correspond- ing to biosynthetic pathways for certain amino acids (the essential amino acids) and the B-complex vitamins. In this way, animal cells all became dependent on an outside source of complex organic nutrients: food. Man emerged some 2 million years ago, probably in central Africa, and spread slowly northward, arriving at the Mediterranean basin and the countries of the Middle East about half a million years ago. The second aspect was the development of agriculture and the do- mestication of animals, which took place in the Near East about 10,000 years ago-that is, only about 300 generations back. Radiocarbon dating shows that domestic cattle, pigs, and sheep were first raised in this area about 8000 B.C., when cereals also appear to have been cultivated for the first time. During the preceding 2 million years, man was a hunter and a gatherer, as shown in many parts of the world by cave paintings, carvings, and remains of food animals. Examination of 24
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Health-Related Aspects of Animal Products 25 people in modern hunter-gatherer communities shows that they have low blood pressures and low blood cholesterol values. We do not know how much the change in life-style toward de- pendence on crops and domesticated animals had to do with the emergence of degenerative diseases. It did, however, allow rapid growth of the world population. One final event completed the revolution. Shortly after the time of these agricultural developments in the Near East, a tribe living north of the Black Sea and speaking a primitive Indo-European language succeeded in domesticating the horse and took over the farming communities to the south. With its new means of locomotion and knowledge of agriculture, this Indo-European popula- tion spread during the last 4,000 years from India in the East to all of Europe in the West and by later exploration to North and South America and Australasia, giving rise to some 40 languages derived from the original Indo-European tongue (Barker, 19721. Thus, mobility resulted in the rapid spread of agricultural techniques capable of sustain- ing large populations. The history of recent developments in population growth and food supplies is well known. A survey by Thompson (1972) compares in- creases in population with increases in world production of cereal grains and red meat from 1950 through 1970. Cereal output roughly paralleled population increase up to 1965; during the next 5 years, output per capita increased. On the other hand, red meat production rose much more rapidly than population over the 20-year period, averaging 36 lb per capita per year in 1950 and 48 lb in 1970. The largest part of this gain occurred between 1950 and 1960. ~ . , RECENT TRENDS IN CONSUMPTION OF ANIMAL AND PLANT FOODS IN THE UNITED STATES Most of our information about patterns of food consumption in the United States comes from two sources. First, the U.S. Department of Agriculture (USDA) makes periodic surveys of the quantities of food- stufis sold for civilian consumption. Friend (1967) has summarized these data and has also computed the intakes of nutrients obtained from these various foods at different times during the period 1909-1965. Second, the USDA has also conducted household food-consumption sur- veys that provide information about the actual amounts of foods con- sumed by individuals (Agricultural Research Service, 1969~. Figures 1 and 2 show annual consumption per capita of various classes of foodstuffs sold to the U.S. public during the period 1909- 1965. Figure 1 shows that the annual intake of all meats was almost as
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26 250 200 : _ Meat ~ Ibs) 150 103 ~5 o 100 50 o 1 = 1909-13 2= 1925-29 3=1935-39 4= 1 947-49 5- 1957-59 6= 1 965 6 H. N. MUNRO Dairy Products (quarts) ~ // / // / // 4 5 6 / / / 7 2 7 Poultry & Fis _ / htibs, Eggs (lbs] / 7 ~2 _ 6 FIGURE 1 Annual U.S. consumption per capita of foods of animal origin over the period 1909-1965. The figures are for retail-weight equivalents. (Drawn from data compiled by Friend, 1967. )
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Health-Related Aspects of Animal Products 250 200 1 50 100 50 o 100 ~ _ , __ 2 3 Flour ~ Cereals (Ibs) Potatoes (Ibs) / / / / _ - 1 1 = 1909-13 2= 1925-29 3= 1935-39 4= 1947-49 5 = 1 957- 59 6= 1965 Fruit (Ibs) . / 3 Sugar (lids) | Fats ~ Oils(lbs) 50~ (Butter in black) ~ FIGURE 2 Annual U.S. consumption per capita of foods of plant origin, to- gether with fats and oils of mixed origins, over the period 1909-1965. The figures are for retail-weight equivalents. (Drawn from data compiled by Friend, 1967.) high in 1909 ( 141 lb per capita per year) as in 1965 ( 148 lb per capita) equivalent to about 180 g of meat per capita per day. However, this constancy obscures a change in type of meat; the proportion of meat consumed as beef shows a steady rise during this 60-year period. It will also be seen that the meat intake showed a temporary reduction
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28 H. N. MUNRO during the depression years of the late 1920's and 1930's. But poultry and fish did not reflect this drop in intake, and after 1947 intake rose sharply for poultry. Dairy products showed a steady gain during the period 1909-1949 but more recently have remained at a plateau level of intake. Intake of eggs showed no consistent trend in the period surveyed. Figure 2 gives a corresponding picture for foods of plant origin. A striking change in consumption habits is shown by the progressive re- duction in intake of potatoes, hours, and cereals, with a consequent fall in carbohydrate intake as starch. But intake of sugar has been stable at an annual rate of 110-120 lb per capita since before 1925; thus, in recent years intake of sugar has provided a larger proportion of the diminishing total intake of carbohydrate. Although the total consumption of fats and oils remained constant over the period, this conceals a steady and considerable reduction in butter intake and its replacement by vegetable fats and oils, especially since 1947. Fruits and vegetables displayed an increased availability per capita until the 1940's, when there was a decline in per capita consumption. In view of the increase in availability of dairy products and poultry, and the reduction in potatoes and flour during the period 1903-1965, it is not surprising that the proportion of energy intake from carbohydrate fell from 56% to 47% over these six decades and that fat intake rose from 32% to 41% (Table 11. Protein was constant at 11%-12%. In addition to nutrient calculations based on the use of foods by the U.S. civilian population, we have data based on direct household con- sumption surveys made in 1965 (Agricultural Research Service, 1969~. Table 2 shows the sources of energy in the diets of males studied in this survey. It is evident that 15%-16% of total energy intake comes from dietary protein-about 45% from fat and 40% from carbohydrate. This picture confirms the high proportion of energy derived from fat TABLE 1 Energy Available per Capita per Day from the U. S. Food Supply, 1909-1965 a Total Percentage of Energy Energy Year (kcal/day) Protein Carbohydrate Fat 1909-1913 3,490 12 56 32 1925-1929 3,470 11 54 35 1935-1939 3,270 11 53 36 1947-1949 3,230 12 49 39 1957-1959 3,140 12 47 41 1965 3,160 12 47 41 a SOURCE: Friend (1967).
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Health-Related Aspects of Animal Products 29 TABLE 2 Sources of Energy in the Diets of Males of Different Ages Computed from Household Surveys in 1965a Age Percentage of Energy Group (years ) Protein Carbohydrate Fat 12-14 15 43 43 18-19 1 6 41 44 35-54 16 37 45 65-74 16 39 44 SOURCE: Leveille ( 1975 ) . (Table 1~. Table 2 also shows that with increasing age there is a tendency for a smaller proportion of total energy to be derived from carbohydrate sources. More striking is the high proportion of energy from fat sources throughout life. We can now ask whether the average U.S. diet, as it has evolved to the present, provides adequate amounts of all nutrients, and what each group of foodstuffs has contributed to the pattern of nutrient supply. Leveille ~ 1975 ~ has made an interesting comparison between the intakes of various nutrients at different ages, as evaluated by the 1965 household food-consumption survey (Agricultural Research Service, 1969), and the requirements for these nutrients given in the 1974 edi- tion of Recommended Dietary Allowances (NRC, 19741. Table 3 sug- gests that the energy content of the diet of each age-group is about adequate and that all groups are consuming much more protein than they require. The average amount of calcium consumed is adequate for males but is probably less than desirable for older women. Iron intake is satisfactory for males but is inadequate for all groups of women except the elderly. Intakes of vitamins are adequate except for the thiamine intake of older women. The low thiamine intake of older women may not be significant; their total energy intake is low, and thus metabolic demands on the supply of thiamine are reduced. From this survey of food and nutrient patterns in the United States, it is apparent that we should consider the role of animal foods in relation to those nutrients that are likely to be either in excess (fat, protein) or in deficiency (calcium, iron) . SIGNIFICANCE OF ANIMAL SOURCES OF FAT The progressively higher content of fat in the U.S. diet has often been condemned as a leading cause of atherosclerosis. This conclusion is
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30 H. N. MUNRO V) o V' . a, ~ _ ._ o ._ o so i_ _ Cal Cal 3 o - ¢ Ct 4_ ._ a o C) o Ct Cat · ~ m ~ ¢ EM ~ 1 .O 53 O C) U. .O o . .= . . . - .> O C) ~ on ~ ~Cal ~ ~ ~ ~ m==X -00~0= . -0 00 v ~ ~ O ~ ~ ~ ~ _ ~ ~- _4 _1 - ~ ~ ~ ~ _ ~ ~ ~ ~ ~ _ ~ O 0 00 ~ ~ X oN ~ O ~D O O0 -] 4 ~ ~ ~ ~ o o oo ~D sD ~ ~0 ~ 0\ ~ _4 _1 t ~4 O ~ oo oo cr x x cq ~ cr. - ~ w~ ~ ~ _1 - w) ~ :; ~ oo ~ tm -' - ~ kD _ _, _ - , oY - - - . c) . . o v, -
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Health-Related Aspects of Animal Products 31 based on evaluation of cholesterol levels in the blood. Attempts have accordingly been made to reduce intake of total fat, in particular by replacing saturated fats with polyunsaturated fats of vegetable origin. To this can be added the admonition to reduce cholesterol intake. Pro- grams of this kind have been advocated to stem the increasing incidence of coronary heart disease. For example, the American Heart Association ~ 1973 ~ made the following dietary recommendations: In most persons, but not all, the level of cholesterol and other fats in the blood can be decreased and maintained at a lower value by conscientious and long-term adherence to a suitable diet. In most individuals, this would entail: ( 1 ) A significantly decreased intake of saturated fat; (2) A significantly increased intake of polyunsaturated fat, with polyunsaturated fats being substituted for saturated fats in the diet wherever possible (3) A decreased intake of cholesterol-containing foods; (4) A caloric intake adjusted to achieve and maintain desirable weight. If we accept these general conclusions, it is legitimate to ask how extensive changes in life-style have to be in order to significantly de- crease the chances of coronary heart disease. Since the effects of differ- ent fats are thought to affect the incidence of coronary disease through alterations in blood cholesterol levels, it is customary to compare the action of fats for cholesterol-lowering action. For example, Vergroesen (1972) compared the changes in serum cholesterol content of varying fat mixtures fed to volunteers receiving 40% of their energy intake as fat. These fat mixtures provided 10% palmitic and stearic acids, 14% oleic acid, and 76% linoleic acid. Over a 4-week period, there was a 20% reduction below the initial cholesterol level. When half of the linoleic acid was replaced by oleic acid, the fall in cholesterol level was only 10%; there was no reduction when half of the linoleic acid was replaced by elaidic, lauric, or myristic acid. Although there is no general agreement regarding quantitation of the effects of various combinations of fatty acids on serum cholesterol content, the above data emphasize the need for the polyunsaturates to predominate in order to achieve an extensive reduction. This is reflected in the "Keys equation" (Keys et al., 1959; Anderson et al., 1961), in which the change in the cholesterol content of serum in milligrams per 100 milliliters resulting from an alteration in dietary fat composition can be predicted to be 2.68 times the change in saturated fat (percentage of total calories) minus 1.23 times the change in polyunsaturated fat (percentage of total calories). Thus, in order to prevent an elevation in serum cholesterol level, the equation requires two thirds of the dietary fat to be taken as poly- unsaturates. A more detailed but essentially compatible equation is provided by Hegsted et al. ~ 1965 ~ .
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32 H. N. MUNRO The role of the ratio of polyunsaturates to saturated fatty acids is confirmed in long-term studies on controlled populations (Turpeinen et al., 1968; Dayton et al., 1969; McGandy et al., 19721. In the study of Turpeinen et al. (1968), for example, the diet of patients at one mental hospital was changed for a 6-year period while a second hospital served as control. Then the roles of the two hospitals were switched for a further 6 years. In the control diet, the ratio of polyunsaturated to saturated fatty acids was about 0.2:1, whereas the experimental diet provided a ratio of about 1.5:1; the latter diet also provided somewhat less cholesterol. During the first period, serum cholesterol levels fell about 50 mg per 100 ml on the experimental diet; during the second (reversal) phase, the difference between experimental and control groups was about 30 mg per 100 ml. The incidence of coronary heart disease in the group on the experimental diet was half that of the group on the control diet (Karvonen, 19721. In order to achieve such effects, extensive changes in eating habits are required, and these demand considerable self-discipline. In the New York Anti-Coronary Club trial of prevention (Christakis et al., 1966a,b), beef, mutton, and pork were restricted to four meals a week; poultry and veal were eaten four or five times a week; and fish was eaten at least four times a week. Margarine rich in polyunsaturates and vegetable oils was emphasized, ice cream and cheese were avoided, and whole milk was replaced by skim milk. Against this background of experimental evidence, we can consider the current American intake of fat. An examination of the trends in fat intakes between 1909 and 1965 (Table 4) shows that the increase in dietary fat during this period has come entirely front an increased consumption of vegetable fats. There was a considerable reduction in consumption of visible animal fats (butter, lard) during the period, whereas margarine and cooking and salad oils increased. This trend is confirmed by data on the percentage of dietary fat from different sourcesin the years 1959andl967 (Food Fats and Oils, 19681.This compilation (Table 5) shows a reduction in visible fats of animal origin and an increase from vegetable sources over the 8-year interval. Table 6 indicates the degree of saturation of the dietary fat during the period 1909-1965. Intake of saturated fatty acids was constant during this period; there was a slight rise in oleic acid (monounsaturated) intake and nearly a doubling in consumption of the polyunsaturated essential fatty acid, linoleic acid. In relation to total energy intake, linoleic acid intake increased from 2.7% of total caloric intake in 1909-1913 to 5.4~o in 1965, whereas saturated fatty acids accounted for 15.2%. If we apply the Keys equation to the 1965 diet, we are presented with a
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Health-Related Aspects of Animal Products _4 au ce ._ o v, I_ ._ 3 ct so a, ct ._ CQ cot 4 - ._ cry .= ~ ~ _ r C`:) t_4 ~ Con o CD r O '_ to U. O~ U. Ct 4_ 0 O V' _` ~0 - U, - Ct ¢ o U) 06 _ Ct 4 - 0.0 O .= ~ Cal ~ ~ I_ ~ . . . . . . ~ ~ ~ O ~ ~ _ ~ _ ~ .. .. to Ct ._ Ct V, g ~ _ ~ O. ~ _1 ~ ~0 O Ct ~0 Ct .= An: - 4 - a' a: Ct 00 ~ X ~ ~ ~ . · · . · - O ~ ~ ~ 00 ~ ~ ~ ~ x . . . . . . to ~ ~ en ~ ~ ~ ~ to . . . · · . ~ ~ ~ ~ ~ Go ~ ~ - ~ ~ - ~ . . . . . ~ ~ Oo ~ to Go ~ m ~ - 4 at 00 ct ._ - o Em 0 ~ ~ ~ ~ 0 0 0 ~ 0 0 0\ _ ~ _, _4 ON _. 0\ _ _! _ ~ _4 1 1 1 1 1 0 cry ~ ~ _. ~ ~ 33 ID 0\ _ . - o . ~0 cry
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34 H. N. MUNRO TABLE 5 Proportion of Total Daily Fat Intake Derived from Visible and Invisible Animal and Vegetable Fats a Percentage of Total Fat Intake Group of Fats 1959 h 1967 c Animal Visible ~12.8 8.2 Invisible e 54.1 51.7 Total 66.9 59.9 Vegetable Visible f 26.1 32.9 Invisible ~7.1 7.4 Total 33.2 40.3 a Derived from Food Fats and Oils (1968). b Total daily fat intake per capita, 146 g. c Total daily fat intake per capita, 148 g. d Butter and lard. e Dairy products, eggs, meat, poultry, fish. ~ Margarine, cooking and salad oils, shortening. g Beans, peas, soya, vegetables, grains. gross excess of saturated fatty acids, and in consequence the diet would be expected to raise serum cholesterol levels by 34 mg per 100 ml of serum. Much of this rise can be attributed to the saturated fats of meat products. This emphasis on fat derived from meat, poultry, and fish increases with age (Table 7) and must therefore contribute to the pro- gressive elevation of cholesterol level. As the U.S. male grows older, a greater proportion of dietary fat comes from meat, poultry, fish, and eggs and less from milk and milk products, grains, and legumes. It should be pointed out that coronary heart disease is not uniquely determined by intake of saturated fat and cholesterol. It has been TABLE 6 Trends in Fatty Acids Available per Capita per Daya Fatty Acids (g per day) Total Oleic Linoleic Year Saturated Acid Acid 1909-1913 50 52 11 1925-1929 53 55 13 1935-1939 53 55 13 1947-1949 54 58 15 1957-1959 55 58 17 1965 54 59 19 a SOURCE: Friend (1967).
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Health-Related Aspects of Animal Products 35 TABLE 7 Sources of Dietary Fat in the Diet of U.S. Males in 1965 a Age Group ( % ) Fat Source 12-14 18-19 35-54 65-74 Meat, poultry, fish33 37 44 41 Milk products21 18 12 13 Eggs4 44 6 8 Fats and oils13 13 15 15 Grains and legumes21 19 16 16 Fruits and vegetables6 7 7 7 ~ Derived from Agricultural Research Service (1969) by Leveille ( 1975). claimed that sucrose and the softness or hardness of the local water supply are important dietary factors. Factors associated with life-style are also determinants, as shown by the comparison between brothers in Ireland and Boston (Brown et al., 19701. This study shows that the Irish residents consumed more energy, total fat, and animal fat, yet they had half the incidence of coronary disease. Lees and Wilson (1971) summarized the evidence showing that high blood-lipid levels fall into at least five constitutional (hereditary) classes, two of which (Types II and IV) are common and react differently to diet. Type II patients show an increase in blood lipids in response to saturated fats, whereas Type IV carry an excess of blood lipids formed endogenously from dietary carbohydrate and thus respond to the carbohydrate content of the diet. SIGNIFICANCE OF PROTEIN INTAKE FROM ANIMAL FOODS It has already been shown (Table 3) that the intake of protein at all ages from 12 years upwards is considerably in excess of the recom TABLE 8 Dietary Protein Intake of U.S. Males of Various Ages a Recom- RDA · mended Met from Protein Consumption Dietary Animal Age Total Animal Plant Allowance Protein (years) (g/day) (% ) (do ) (g) (% ) 12-14 100 70 30 44 159 18-19 118 73 27 54 160 35-54 106 74 26 56 140 67-74 82 74 26 56 108 a Derived from Agricultural Research Service ( 1969 ) by Leveille ( 1975 ) .
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36 H. N. MUNRO mended dietary allowances (RDA). Table 8 provides estimates of actual intakes for males of different ages. Before the age of 55, daily intake exceeds 100 g, and drops only in the later years, a phenomenon noted in earlier data from Scotland (Munro, 19641. At all ages, animal sources provide nearly three-fourths of the total protein intake, and this alone ensures much more than the ADA at all ages. Examination of estimated protein intakes per capita during the past 60 years (Table 9) shows that total dietary protein content has not changed. However, this con- ceals a shift toward animal protein and away from protein of plant origin, because of progressively greater availability of poultry and dairy products (Figure 1) but diminishing consumption of potatoes, four, and other cereal products (Figure 2~. The overabundance of high-quality protein in the present U.S. diet is also emphasized by analysis of the daily intake of essential amino acids, shown in Table 10 in comparison with daily needs of the same amino acids by an adult. The requirements of adults are low (Munro, 1972), and in consequence the amount of essential amino acids in the average U.S. diet is several times greater than the amount required. ANIMAL FOODS AND MINERAL REQUIREMENTS As pointed out earlier (Table 3), the household survey of 1965 shows that intakes of calcium and iron by women tend to be below recom- mendations. The role of animal products in supplying these minerals and zinc will now be considered. Table 11 shows the amounts per capita of some minerals provided by the U.S. diet between 1909 and 1965. The problem of meeting iron requirements exerts a perennial fasci- nation, probably because it is the commonest deficiency in Western countries (Ten-State Nutrition Survey, 1968-1970) and because cor TABLE 9 Protein Available per Capita per Day in the United States Total Sources ( % ) Protein Year (g) Animal Vegetable 1909-1913 102 52 48 1925-1929 95 55 45 1935-1939 90 56 44 1947-1949 95 64 36 1957-1959 95 67 33 1965 96 68 32 a Derived from Friend (1967) .
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Health-Related Aspects of Animal Products 37 TABLE 10 Average Daily Consumption of Essential Amino Acids in the United States Compared with the Estimated Requirements of a 70-kg Adult U.S. Intake Adult Requirement Amino per Capita'' per Capita Acid (g/day) (g/day) Isoleucine 5.3 0.7 Leucine 8.2 0.9 Lysine 6.7 0.7 Methionine 2.1 0 9 c Phenylalanine 4.7 1 Oc Threonine 4.1 0.5 Tryptophan 1.2 0.2 Valine 5.7 0 9 a Data an food intake computed by Consumer and Food Economics Research Division, Agricul tural Research Service, USDA, 1970. b Adult requirement per capita calculated from estimated requirement per kilogram (Munro, 1972). c Requirement for methionine includes cystine, and requirement for phenylalanine includes tyrosine. recting the deficiency has proved to be difficult. Consequently, major dietary constituents must be viewed both as sources of iron and as factors influencing iron absorption from other dietary constituents. Animal foods serve in both capacities. The iron content of meats (Agri- cultural Research Service, 1970) indicates that the average amount of meats available in the diet (Figure 1)-180 g daily-should provide a significant proportion of the total iron needed (Table 111. The second feature of meat is its capacity to promote absorption of iron from in- organic sources. Using dinner rolls containing radioactive-Labeled ferrous TABLE 11 Minerals Available per Capita per Day from U.S. Foods a Iron h Calcium Magnesium Year (mg) (mg) (mg) 1909-1913 15.2 816 410 1925-1929 14.4 859 389 1935-1939 13.8 894 380 1947-1949 16.7 994 369 1957-1959 16.1 978 348 1965 16.5 961 340 a Derived from Friend (1967~. b Includes iron fortification.
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38 H. N. MUNRO sulfate, Cook et al. (1973) demonstrated that fasting subjects absorbed 6.3% of the dose and a similar amount when the roll was consumed in a meal containing meat. However, in a meal without meat, absorption fell to 2.1%. There appears to be no evidence regarding the amount of meat needed to achieve optimum stimulation of iron absorption. Any reduction in meat intake should therefore take account of its contribution to the iron requirements of man. First, it would be helpful to determine the least amount of meat that provides maximal promotion of iron absorption. Second, a possible avenue for reducing meat intake without losing the benefit of its iron content would be to raise the iron level of beef by appropriate treatment of the steer. We have shown that the skeletal and cardiac muscles of rats contain two forms of the iron-storage protein ferritin (tinder et al., 19731. Furthermore, when we injected iron dextran into the rats over a 7-day period, both forms of cardiac muscle ferritin doubled in amount and other (unidentified) forms of iron were deposited in the muscle cells (Table 121. Thus, if total beef intake is to be reduced, iron enrichment of beef as a means of maintaining or even improving the iron status of the population is worth considering. In addition to being a significant source of iron, meat is a major contributor to our daily intake of zinc. The average zinc intake of adults is about 12 mg per day (Halsted et al., 1974), which tends to fall below the recommended allowance for safety, which is 15 mg per day (NRC, 19741. Thus, there is reason to regard zinc intake, like iron intake, as marginally adequate. Meat is a major source of dietary zinc. The following shows the average amount of zinc in 100 g of each of the foods named: beef, 6.4 ma; chicken breast, l.1 ma; chicken leg, 2.8 ma; milk, 0.3 ma; TABLE 12 Effect of Iron Treatment on Iron Content of Rat Muscle (mg/100 g of Tissue) a Total Heme Ferritin Group Fe Fe Fe Males Control 8.2 8.9 0.3 Iron-treated 21.3 10.3 1.4 Females Control 12.1 10.8 0.3 Iron-treated 23.5 13.3 1.8 a sOuRcE: Binder e' a!. ( 1973 ) ~
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Health-Related Aspects of Animal Products 39 white bread, 0.6 ma; potatoes, 0.3 ma. Thus, it is difficult to substitute other foods for beef and maintain an adequate intake of zinc. There is now evidence that protein intake affects body calcium balance. Anand and Linksweiler (1974) studied urinary calcium excre- tion and calcium balance during 15-day periods in male subjects re- ceiving a diet that was constant except for the protein content, which was varied from 47 g through 95-142 g daily. These changes caused progressively greater urinary outputs of calcium, so that calcium bal- ance declined from +31 mg per day at the lowest protein intake through-58 mg to -120 mg daily at the highest protein level. Beef is a very poor source of dietary calcium but an important source of dietary protein. Excessive consumption of beef may result in depletion of body calcium because of the consequent high intake of protein with- out a compensatory increment in calcium intake. Of course, other foods of animal origin contribute calcium, notably milk. However, as implied in Table 7, intake of milk products declines in the older popu- lation as meat intake increases. It may be noted that skeletal depletion and fragility are health problems of older people. OTHER HEALTH-RELATED ASPECTS OF ANIMAL FOODS Many attempts have been made to relate regional variation in the incidence of diseases to differences in dietary patterns, particularly to intake of food of animal origin. For example, Knox (1973) correlated the regional frequency of various major diseases in Great Britain with the intakes of nutrients as measured by the British National Food Survey. He observed that ischemic heart disease was inversely related to intake of calcium and vitamin C and positively related to intake of fat and vitamin D. Several other degenerative diseases were similarly correlated with intakes of these nutrients, suggesting a general rela- tionship of disease to life-style. The problems of assessing dietary and other factors in the incidence of disease are illustrated by studies of the incidence of colonic cancer. This condition shows a distinct difference in geographic incidence; for example, the frequency of colonic cancer among Hawaiian Japanese is four times the frequency recorded in Japan (Berg et al., 19721. Pat- terns of dietary intake have been explored in relation to colonic cancer incidence (Berg et al., 1973; Drasar and Irving, 1973; Knox, 1973) and provide some evidence for implicating animal foods pro- viding protein and fat. It is postulated that a diet rich in meat gives rise to carcinogenic substances because of the action of the colonic micro- flora on the meat residues. A local action of such carcinogens is easily
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40 H. N. MUNRO conceivable, but it is more difficult to relate an identical relationship of animal food intake to breast cancer (Drasar and Irving, 19731. More- over, Leveille (1975) recently compared the incidence of colonic can- cer in the United States over the period 1935-1965 with changes in the intake of major food items during this period. His analysis (Table 13) demonstrates that, although the incidence of cancer rose steadily during this 30-year period in parallel with increasing intakes of beef, and of the combined intakes of meat, poultry, and fish, there was a compensatory reduction in intake of cereals and potatoes. Thus, it would be equally appropriate to relate the incidence of colonic cancer to lack of fiber in the diet. In general, diets rich in animal foods are low in fiber, and a comparison of the incidence of some major Western diseases in central Africa and other underdeveloped areas has prompted the conclusion that dietary fiber has a protective effect against cancer, atherosclerosis, and several other conditions (Burkitt, 1973; Trowell, 19731. Klevay ( 1974) postulates that dietary fiber lowers blood cholesterol levels through an alteration in the relative amounts of zinc and copper absorbed from the diet. However, direct tests of the action of administered fiber on blood cholesterol levels have been negative (Eastwood, 19691. Finally, animal fats have been implicated in multiple sclerosis, a disease of the nervous system that is notoriously difficult to study be- cause of the long periods of unpredictable improvement. Nevertheless, TABLE 13 Incidence of Cancer of Large Intestine in Connecticut Males and Relationship to U.S. Dietary Changes Gab C f Annual per Capita Consumption Large Meat, Intestine Poultry, (incidence/ Beef and Fish Cereal Potatoes Period 1~) (lb) (lb) (lb) (lb) 1935-1938 19.7 44 148 205 149 1939-1942 21.2 46 165 200 140 1943-1946 23.9 45 182 198 142 1947-1950 25.9 51 176 170 121 1950-1953 27.2 51 179 163 112 1954-1957 28.9 65 192 151 111 1958-1961 30.0 63 194 148 109 1962-1965 30.4 68 201 144 110 a SOURCE: Leveille ( 1975 ) . ~ Correlation coefficients of cancer incidence: with beef intake, +0.91; with meat, poultry, and fish intake, +0.94; with cereal intake, - 0.97; with potato intake, - 0.97.
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Health-Related Aspects of Animal Products 41 on the basis of a 20-year study, Swank (1970) claims that this condi- tion shows much less deterioration if the animal fat in the diet is re- placed by vegetable fats, combined with a general reduction in fat intake. CON C L U SION From the preceding presentation, we can consider the contribution of animal foods, notably beef, to the U.S. diet. Table 14 displays the nutrient content of the average diet in 1965 and the RDA of essential nutrients for an adult male (NRC, 19743. For comparison with these, the table gives the nutrient content of 3 oz of choice beef sirloin, in- cluding the fat. The average diet already provides more than adequate amounts of protein and energy, and too much saturated fat; hence, beef is not an important source of these nutrients and nonmeat foods would be an adequate substitute. However, on the credit side' beef has only a modest cholesterol content and makes a significant contribution to the daily intakes of iron, zinc, and niacin, all of which are available near or below requirements for some classes of the population. This evidence suggests that meat performs a significant function as a nutrient source but would be more nutritious if the saturated fat content could be reduced. Leveille (1975) has further emphasized that a reduction in fat content, from choice grade to good, is obtained by shortening the TABLE 14 Contribution of 3 oz (85 g) of Choice Beef Sirloin to Average U.S. Diet Adult Average 3 Oz Male Nutrient Diet a Beef b RDA c Protein (g)96 2056 Energy (kcal)3160 3302,700 Fat (g)145 27 Saturated54 13 Oleic59 12 Linoleic19 1 Cholesterol (mg)500 80 Calcium (mg)960 9800 Iron (mg)16.5 2.510 Zinc(mg)12 515 Niacin (mg)21 418 a Food availability per day in the United States in 1965 (calculated from Friend, 1967) with added estimates for cholesterol and zinc. b From Agricultural Research Service (1970). c From NRC ( 1974)
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42 H. N. MUNRO period of feeding and thus reducing the feed consumed by the steer by 20%-30~o, a considerable saving in grain intake. These conclusions represent minimal demands on current practices in animal husbandry. In order to cope with the much more difficult question of the relationship between intake of animal products and the incidence of chronic and degenerative diseases, it would be necessary to evaluate the available data much more rigorously than can be done in one brief review paper and to plan further targeted research. Both are major commitments for which several panels of experts would have to be recruited. To proceed with such plans would imply a serious commitment to implement any recommended changes. If the evidence of benefits from a change in animal fat is sufficiently persuasive, the recent Australian experimental method of changing the spectrum of beef fatty acids by feeding polyunsaturates protected against rumen digestion to beef cattle (Cook et al., 1970) could be explored further. This maneuver resulted in a rise in ratio of polyunsaturated to saturated fatty acids in the body fat from 0.1: 1 to 0.9: 1. In clinical trials, feeding this beef resulted in a lowering of plasma cholesterol levels (Nester et al., 19731. Feasibility trials of the commercial introduction of such beef are worth considering for the benefit of at least those in the population who desire such a change in the proportions of dietary fatty acid. ACKN OW L E DGM E N T I am grateful to Dr. G. A. Leveille for making available to me before publication his excellent manuscript (reveille, 1975) dealing with the role of animal foods in human nutrition. REFERENCES Agricultural Research Service. 1969. Food Intake and Nutritional Value of Diets of Men, Women, and Children in the United States; Spring 1965, Preliminary Report. ARs Publ. No. 62-18. USDA, Washington, D.C. 97 pp. Agricultural Research Service. 1970. Nutritive Value of Foods. Home and Garden Bull. No. 72. USDA, Washington, D.C. 41 pp. American Heart Association. 1973. Diet and Coronary Heart Disease. Anand, C. R., and H. M. Linksweiler. 1974. Effect of protein intake on calcium balance of young men given 500 mg calcium daily. J. Nutr. 104:695-700. Anderson, J. T., F. Grande, and A. Keys. 1961. Hydrogenated fats in the diet and lipids in the serum of man. J. Nutr. 75:388-394. Barker, C. L. 1972. The Story of Language, 5th ed. Pan Books, London. Berg, J. W., W. Haenszel, and S. S. Devesa. 1972. Epidemiology of gastro-intestinal cancer. Proc. 7th Int. Cancer Congr., pp. 459-464. Lippincott.
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Health-Related Aspects of Animal Products 43 Berg, J. W., M. A. Howell, and S. J. Silverman. 1973. Dietary hypotheses and diet-related research in the etiology of colon cancer. Health Serv. Rep. 88:915- 924. Brown, H. B. 1971. Food patterns that lower blood lipids in man. J. Am. Diet. Assoc. 58: 303-311. Brown, J., J. G. Bourke, G. F. Gearty, A. Finnegan, M. Hill, F. C. Hefferman-Fox, D. E. Fitzgerald, J. Kennedy, R. W. Childers, W. J. E. Jessup, M. F. Trulson, M. C. Latham, S. Cronin, M. B. McCann, R. E. Clancy, I. Gore, H. W. Stoudt, D. M. Hegsted, and F. J. Stare. 1970. Nutritional and epidemiologic factors related to heart disease. World Rev. Nutr. Dietet. 12: 1-42. Burkitt, D. P. 1973. Epidemiology of large bowel disease: the role of fibre. Proc. Nutr. Soc. 32:145-149. Christakis, G. S. H. Rinzler~ M. Archer, and E. Maslansky. 1966. Summary of the research activities of the anti-coronary club. Public Health Rep., Wash. 81: 6~70. Christakis, G. S. H. Rinzler, M. Archer, G. Winslow. S. Jampel, J. Stephenson, G. Friedman, H. Feint A. Kraus. and G. James. 1966. The anti-coronary club. A dietary approach to the prevention of coronary heart disease ~ seven-year report. Am. J. Public Health 56: 299-3 14. Cook, J. D., V. Minnich, C. V. Moore. A. Rasmussen, W. B. Bradley, and C. A. Finch. 1973. Absorption of fortification iron in bread. Am. J. Clin. Nutr. 26: 361-372. Cook, L. J., T. W. Scott, K. A. Ferguson, and I. W. McDonald. 1970. Production of poly-unsaturated ruminant body fats. Nature 228:178-179. Dayton, S.~ M. L. Pearce, S. Hashimoto, W. J. Dixon, and U. Tomiyasu. 1969. A controlled clinical trial of a diet high in unsaturated fat in preventing complica- tions of atherosclerosis. Circulation 40, Suppl. No. 2. 63 pp. Department of Health, Education, and Welfare (USDHEW). 1972. Ten-State Nutri- tion Survey, 1968-1970. Highlights. Publ. No. (NSM ) 72-8134. USDHEW, Washington. D.C. 12 pp. Drasar, B. S., and D. Trving. 1973. Environmental factors and cancer of the colon and breast. Brit. J. Cancer 27:167-172. Eastwood, M. A. 1969. Dietary fibre and serum-lipids. Lancet ii:1222-1224. Food and Nutrition Board, National Research Council. 1974. Recommended Di- etary Allowances, 8th rev. ed. National Academy of Sciences, Washington, D.C. 128pp. Friend, B. 1967. Nutrients in United States food supply. A review of trends. 1909- 1913 to 1965. Am. J. Clin. Nutr. 20:907-914. Halsted, J. A., J. C. Smith, and M. I. Irwin. 1974. A conspectus of research on z~nc requirements of man. J. Nutr. 104:345-378. Hegsted, D. M., R. B. McGandy, M. L. Myers, and F. J. Stare. 1965. Quantitative effects of dietary fat on serum cholesterol in man. Am. J. Clin. Nutr. 17:281- 295. Institute of Shortening and Edible Oils. 1968. Food Fats and Oils, 3d ed. Report of Technical Committee. Tnstitute of Shortening and Edible Oils, Washington, D.C. 18pp. Karvonen, M. J. 1972. Modification of the diet in primary prevention trials. Proc. Nutr.Soc.31:355-362. Keys, A., J. T. Anderson, and F. Grande. 1959. Serum cholesterol in man: diet fat and intrinsic responsiveness. Circulation; J. Am. Heart Assoc. 19:201-214.
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44 H. N. MUNRO Klevay, L. M. 1974. Letter: Coronary heart disease and dietary fiber. Am. J. Clin. Nutr. 27 (11 ) :1 202-1 203. Knox, E. G. 1973. Ischaemic-heart-disease mortality and dietary intake of calcium. Lancet i: 1465-1467. Lees, R. S., and D. E. Wilson. 1971. The treatment of hyperlipidemia. N. Engl. J. Med. 284:186-195. Leveille, G. A. 1975. Issues in human nutrition and their probable impact on foods of animal origin. J. Anim. Sci. 41:723-730. Linder, M. C., J. Moor, L. Scott, and H. N. Munro. 1973. Mechanism of sex difference in rat tissue iron stores. Biochim. Biophys. Acta 297:70-80. McGandy, R. B., B. Hall, C. Ford, and F. J. Stare. 1972. Dietary regulation of blood cholesterol in adolescent males: a pilot study. Am. J. Clin. Nutr. 25: 61-66. Munro, H. N. 1964. An introduction to nutritional aspects of protein metabolism. Pages 3-39 in H. N. Munro and J. B. Allison, eds. Mammalian Protein Metabo- lism, vol. II. Academic Press, New York. Munro, H. N. 1969. An introduction to protein metabolism during the evolution and development of mammals. Pages 3-19 in H. N. Munro, ed. Mammalian Protein Metabolism, vol. III. Academic Press, New York. Munro, H. N. 1972. Amino acid requirements and metabolism and their relevance to parenteral nutrition. Pages 34-67 in A. W. Wilkinson, ed. Parenteral Nutri- tion. Churchill-Livingston, Edinburgh. Nestel, P. J.? N. Havenstein, H. M. Whyte, T. W. Stott, and L. J. Cook. 1973. Lowering of plasma cholesterol and enhanced sterol excretion with the con- sumption of polyunsaturated ruminant fats. N. Engl. J. Med. 228:379-382. Swank, R. L. 1970. Multiple sclerosis: twenty years on low fat diet. Arch. Neural. 23 :460-474. Thompson, L. M. 1972. The world food supply in 1972. mu Nutrition Symposium on Proteins, pp. 251-272 (issued by Nutritional Sciences Council) Iowa State University, Ames. Trowell, H. 1973. Dietary fibre, ischaemic heart disease and diabetes mellitus. Proc. Nutr. Soc. 32: 151-157. Turpeinen, O., M. Miettinen, M. J. Karvonen, P. Roine, M. Pekkarinen, E. J. Lehtosuo, and P. Alivirta. 1968. Dietary prevention of coronary heart disease: long-term experiment. I. Observations on male subjects. Am. J. Clin. Nutr. 21: 255-276. Vergroesen, A. J. 1972. Dietary fat and cardiovascular disease: possible modes of action of linoleic acid. Proc. Nutr. Soc. 31 :323-329.
Representative terms from entire chapter: