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Low-fat diets are often advocated for weight reduction and to lower the risk of coronary heart disease and certain forms of cancer. However, there is no universal agreement about the value of low-fat diets. In this Clinical Debate, Connor and Connor argue in favor of the public health benefits of low-fat diets, whereas Katan, Grundy, and Willett present a different point of view.
The association between the dietary intake of fat and cholesterol and the extent of atherosclerosis and coronary heart disease has been recognized since 1907, when de Langen found little atherosclerosis in native Javanese but extensive atherosclerosis in the Dutch settlers in Java. (1) As might be expected, the diets of the two groups of people differed greatly in fat content. At almost the same time in Russia, Anitschkow produced extensive atherosclerosis in rabbits by feeding them cholesterol and fat. (2) In both humans and animals fed high-fat, high-cholesterol diets, serum cholesterol levels greatly increased. Subsequently, after World War II, Keys emphasized that mortality from coronary disease in various countries was directly related both to the amount of dietary fat consumed and to serum cholesterol levels. An extensive data base on this subject was reported in the Seven Countries Study. (3) Mortality from coronary disease also correlated well with dietary cholesterol intake in another analysis of data from 35 countries. (4)
Exceptions to these associations were observed, however. The intake of saturated fat and animal fat correlated better with the incidence of coronary disease than did total fat intake, as is now widely recognized. It was subsequently shown that saturated fats, as well as dietary cholesterol, elevate plasma total and low-density lipoprotein (LDL) cholesterol by down-regulating the LDL receptors in the liver. (5) Another exception was observed in Crete, where there was a high intake of olive oil (a monounsaturated fat) but a low rate of death due to coronary disease in a population adapted to a frugal lifestyle. (3) The Greenland Eskimos also had a low incidence of coronary disease despite a diet rich in fat and cholesterol. The Eskimo diet was protective against coronary disease because it contained n-3 fatty acids from fish and seal. (6) These fatty acids are antithrombotic and lower serum lipid levels.
Experiments in monkeys and other animals confirmed these epidemiologic observations. Feeding fat and cholesterol (e.g., eggs and butterfat) to rhesus monkeys produced high serum cholesterol levels and severe coronary atherosclerosis, (7) even myocardial infarction. That these conditions were largely reversible was documented when a low-fat, cholesterol-free diet was subsequently fed to the monkeys, proving that a drastic reduction in serum cholesterol levels would ultimately be followed by considerable reversal of coronary atherosclerotic lesions (from 60 percent to 20 percent occlusion). (7) Years later, angiographic evidence of improvement in lesions was found in humans treated with low-fat diets alone or with diet plus lipid-lowering drugs.
Various scientific bodies, including the American Heart Association (8) and the National Heart, Lung, and Blood Institute, (9) have recommended reductions in dietary fat intake to treat or prevent coronary disease. The suggested level of dietary fat is 30 percent or less of total energy intake, reduced from the previous high population intake of 40 percent in the 1960s. Even the American Cancer Society has suggested a 50 percent reduction in fat intake (from 40 to 20 percent of energy intake) to prevent cancer of the colon and breast and other cancers. (10) There is universal agreement that the dietary level of saturated fat should be greatly reduced, from the current intake of 11 percent to 6 to 8 percent of energy intake, along with a reduction in dietary cholesterol. Most recommendations have specified that the saturated fat eliminated from the diet be replaced by carbohydrates from grains, vegetables, legumes, and fruits. This change would diversify the diet and add protective constituents from plant sources.
If the saturated fat were replaced by monounsaturated or polyunsaturated fat, as some have suggested, the fasting serum total and LDL cholesterol levels would be decreased without significantly decreasing total fat intake. Is this an appropriate idea? The strategy of replacing fat with fat does not take into account the disadvantages of a high-fat diet. First, postprandial lipemia is atherogenic and directly reflects the amount of dietary fat ingested. (11) A lower-fat diet would reduce postprandial lipemia composed of chylomicrons and atherogenic remnants that circulate in the plasma after the ingestion of dietary fat. Second, although obesity remains an unsolved problem, there is good evidence that Americans who follow a low-fat diet high in plant foods lose weight more easily than those whose fat intake is higher. (12) Third, the energy cost of metabolizing a dense nutrient like fat is lower than the energy expenditure needed to metabolize carbohydrate from plants. Finally, the advantages of a lower-fat diet in the prevention of cancer and the control of hypertension are lost when saturated fat is replaced by other fats, rather than by vegetable foods.
Since 1980, the recommendations of scientific bodies have been translated for the public by the Department of Agriculture (USDA) and the Department of Health and Human Services and published every five years as "Dietary Guidelines for Americans," (13) and both the public and the food industry have attempted to follow them. According to the USDA's Continuing Survey of Food Intakes by Individuals, (14) dietary fat intake has decreased to about 33 percent of energy intake from a previous 40 percent, and dietary carbohydrate has increased from 45 to 52 percent of energy intake from the 1960s to 1995. These changes bring the average diet close to the goal of obtaining no more than 30 percent of energy intake from fat and 55 percent from carbohydrate. However, dietary fiber intake is still low at 15 g per day (the goal is 20 to 35 g per day).
The plethora of "fat-free" foods has offered people the opportunity to consume more sugar in, for example, sweet rolls, cookies, and frozen yogurt. According to recent USDA food-consumption data, (15) the intake of sugar and other refined sweeteners increased from about 55 kg (120 lb) per person per year in 1970 to 68 kg (150 lb) per person per year in 1995. There has been a small increase in the consumption of plant foods containing protective factors such as antioxidants, soluble fibers, and saponins from grains, legumes, vegetables, and fruits and in the intake of the n-3 fatty acids found in seafood, dark green vegetables, nuts, and oils, but all are short of the recommended goals.
Table 1 shows which of the recommended dietary changes for optimal health throughout life the U.S. population has adopted, as well as recommended changes not yet made. Although there has been progress, further steps need to be taken to achieve a more healthful diet.
There is little doubt that Americans have improved their health by lowering their dietary intake of fat and cholesterol. Serum cholesterol levels are lower, and mortality due to coronary disease is 20 to 30 percent lower than 25 years ago. The directions for change are clear, and further implementation of the currently recommended dietary goals is indicated.
William E. Connor, M.D.
Sonja L. Connor, M.S., R.D.
Oregon Health Sciences University
Portland, OR 97201-3098
Address reprint requests to Dr. William E. Connor at the Department of Medicine, L465, Oregon Health Sciences University, Portland, OR 97201-3098.
References
1.de Langen C. Het cholesteringegehalte van het bloed in Indie. Geneeskd Tijdschr Ned Indie 1922;62:1-4.
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2.Anitschkow N. Experimental arteriosclerosis in animals. In: Cowdry EV, ed. Arteriosclerosis. New York: MacMillan, 1933:271-322.
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3.Keys A. Seven Countries: a multivariate analysis of death and coronary heart disease. Cambridge, Mass.: Harvard University Press, 1980.
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4.Connor WE. Dietary cholesterol and the pathogenesis of atherosclerosis. Geriatrics 1961;16:407-15.
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5.Spady DK, Dietschy JM. Interaction of dietary cholesterol and triglycerides in the regulation of hepatic low density lipoprotein transport in the hamster. J Clin Invest 1988;81:300-9.
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6.Bang HO, Dyerberg J. Lipid metabolism and ischemic heart disease in Greenland Eskimos. In: Draper HH, ed. Advances in nutrition research. Vol. 3. New York: Plenum Press, 1980:1-22.
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7.Armstrong ML, Warner ED, Connor WE. Regression of coronary atheromatosis in rhesus monkeys. Circ Res 1970;27:59-67.
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8.American Heart Association. Dietary guidelines for healthy American adults: a statement for physicians and health professionals by the Nutrition Committee, American Heart Association. Circulation 1988;77:721A-724A.
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9.Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Summary of the Second Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel II). JAMA 1993;269:3015-23.
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10.The American Cancer Society 1996 Advisory Committee on Diet, Nutrition, and Cancer Prevention. Guidelines on diet, nutrition, and cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin 1996;46:325-41.
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11.Zilversmit DB. Atherogenesis: a postprandial phenomenon. Circulation 1979;60:473-85.
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12.Schaefer EJ, Lichtenstein AH, Lamon-Fava S, et al. Body weight and low-density lipoprotein cholesterol changes after consumption of a low-fat ad libitum diet. JAMA 1995;274:1450-5.
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13.Kennedy E, Meyers L, Layden W. The 1995 dietary guidelines for Americans: an overview. J Am Diet Assoc 1996;96:234-7.
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14.Department of Agriculture, Agricultural Research Service. Data tables: results from USDA's 1995 continuing survey of food intakes by individuals and 1995 diet and health knowledge survey: CSFI/DHKS 1995. Riverdale, Md.: Food Surveys Research Group, 1995 (CD-ROM).
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15.Department of Agriculture, Economic Research Service. Food consumption, prices, and expenditures, 1995. Stat Bull (in press).
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Excess intake of fat is considered an important cause of chronic diseases, but will a reduction in total dietary fat intake provide the health benefits implied by supporters of this strategy? We are concerned that popular belief and scientific evidence on this question have diverged to an alarming extent.
Studies in the 1950s and 1960s showed that replacing saturated fat with polyunsaturated fats lowered serum total cholesterol levels, (1) and clinical trials subsequently suggested that this dietary change may reduce the incidence of coronary heart disease. (2) Consequently, diets high in polyunsaturated fats were widely recommended for the prevention of coronary heart disease. However, concern developed about the safety of polyunsaturated fats, whereas the perception grew that carbohydrates were innocuous. The focus of recommendations therefore shifted to diets low in fat and high in carbohydrates. Interest in monounsaturated fat also increased, (3) but at present the dominant dietary advice is to replace foods high in total or saturated fat and cholesterol with high-carbohydrate foods such as pasta, potatoes, rice, and bread.
High-Carbohydrate Diets and Cholesterol Levels
Diets that lower serum total cholesterol levels are believed to lower the risk of coronary heart disease. This belief is justified if the cholesterol being lowered is LDL cholesterol; high LDL cholesterol levels cause coronary heart disease, and treatments that lower LDL cholesterol reduce the incidence of coronary heart disease. Replacement of saturated fats by unsaturated oils reduces mainly LDL cholesterol. (4) However, as illustrated in Figure 1, low-fat, high-carbohydrate diets lower not only LDL cholesterol but also high-density lipoprotein (HDL) cholesterol levels. (4) HDL cholesterol levels are lowered by both sugars and complex carbohydrates (starch), (5) and the depression of HDL cholesterol lasts for as long as the low-fat diet is eaten. (6,7)
This effect of carbohydrates on HDL cholesterol is a cause for concern. Low HDL cholesterol levels are strongly associated with coronary heart disease, and many factors that produce lower HDL cholesterol levels increase the risk of coronary heart disease; examples are smoking, obesity, lack of physical activity, abstinence from alcohol, and male sex. Premature coronary heart disease is seen in most genetic HDL-deficiency syndromes, (8) especially in those in which LDL cholesterol levels are normal or high. In trials of lipid-lowering agents, drug-induced changes in HDL cholesterol levels independently predicted changes in the risk of coronary heart disease. Also, the induction of high HDL cholesterol levels in animals retards atherogenesis, and the infusion of HDL protein retards the development of fatty streaks. (8) Thus, lowering HDL cholesterol levels usually increases the risk of coronary heart disease, and diets that lower HDL cholesterol levels must be viewed with concern.
People in China and rural Japan have both low total dietary fat intake and low rates of coronary heart disease. However, such populations are also highly active and extremely lean -- both factors that raise HDL cholesterol levels and reduce plasma triglyceride levels, thus offsetting the adverse changes caused by low-fat diets. The low rates of coronary heart disease in the Chinese and other rural populations may therefore be due largely to their high levels of physical activity and low body fat, plus their low intake of saturated and trans fats, rather than to low total fat intake. (Trans fats are created during the partial hydrogenation of oils; they raise LDL cholesterol and lower HDL cholesterol levels.)
Obesity
A major argument for low-fat diets is that they should promote weight reduction. Fat is calorically dense and often is hidden in food products. Theoretically, high-fat diets could facilitate the overconsumption of calories and promote weight gain; however, controlled trials have not supported this idea. In a free-living population, when calories from fat are intentionally restricted, they appear to be largely replaced by carbohydrate. A limited weight reduction is seen after people start a fat-restricted diet, but weight loss stops after a few months, and the long-term net weight loss is only 0.8 to 2.6 kg (Figure 2). (9) The prevalence of obesity has increased by one third in the United States since 1976, whereas the percentage of total energy intake from fat has declined. Thus, fat restriction does not invariably produce weight reduction; obesity is a complex problem that will not be solved solely by reducing the percentage of fat in the diet. (15)
Cancer
Evidence that dietary fat may cause cancer in humans derives primarily from comparisons of rich and poor nations; these comparisons, like those of the incidence of coronary heart disease, are potentially confounded by many differences in lifestyle. In large prospective studies, fat intake has had no overall relation to the risk of breast cancer. (16) For colon cancer, more detailed evidence suggests a role of red meat but not of total fat, and for prostate cancer associations have been seen with animal but not vegetable fat. (16)
The Alternatives to Low-Fat Diets
Replacement of fat by carbohydrates has not been shown to reduce the risk of coronary heart disease, (2) and benefits are unlikely, because this change similarly lowers HDL and LDL cholesterol (4) and reduces the intake of vitamin E and essential fatty acids. Beneficial effects of high-carbohydrate diets on the risk of cancer or on body weight have also not been substantiated. Alternatively, the replacement of fats high in saturated and trans fatty acids by unhydrogenated unsaturated oils improves the ratio of HDL to LDL cholesterol. Overweight persons can decrease their intake of saturated and trans fat by reducing their consumption of fat from dairy products, meats, and partially hydrogenated oils; they should also eat less sugar and highly refined starch. Carbohydrates should be consumed mainly in the form of fruits, vegetables, legumes, and whole grains. In people who are close to their ideal weight, saturated and trans fats could be replaced largely by unsaturated vegetable oils and highly refined carbohydrates by fruits, vegetables, and whole grains.
Everything we know about lipoproteins and heart disease tells us that such diets will reduce the risk of coronary heart disease. For oils high in polyunsaturated fats, this effect is supported by controlled clinical trials. (2) However, studies in animals have aroused concern about a relation between polyunsaturated fats and cancer, even though observations in humans are reassuring. At present it appears prudent to replace the majority of saturated and trans fats by oils high in monounsaturated fats such as rapeseed (canola) oil and olive oil. The experience in Mediterranean countries shows that diets high in monounsaturated fats can be attractive and that they are associated with longevity and a low incidence of coronary heart disease and cancer.
Finally, the intense focus on total fat intake not only is unlikely to be beneficial but also distracts people from lifestyle changes that can have real benefits. These include specific dietary reductions in saturated and trans fat, increases in the consumption of fruits, vegetables, and whole grains, and the prevention of excessive weight by greater physical activity and reductions in overall caloric intake.
We are indebted to Peter Zock, Ph.D., for advice and to Miranda Mul, M.Sc., for assistance in the preparation of the manuscript.
Martijn B. Katan, Ph.D.
Wageningen Agricultural University
6703 HD Wageningen, the Netherlands
Scott M. Grundy, M.D., Ph.D.
University of Texas Southwestern Medical Center
Dallas, TX 75235
Walter C. Willett, M.D., Dr.P.H.
Harvard School of Public Health
Boston, MA 02115
Address reprint requests to Dr. Katan at the Division of Human Nutrition and Epidemiology, Wageningen Agricultural University, Bomenweg 2, 6703 HD Wageningen, the Netherlands.
References
1.Keys A, Anderson JT, Grande F. Prediction of serum-cholesterol responses of man to changes in fats in the diet. Lancet 1957;2:959-66.
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2.Sacks FM. Dietary fats and coronary heart disease. J Cardiovasc Risk 1994;1:3-8.
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3.Grundy SM. Comparison of monounsaturated fatty acids and carbohydrates for lowering plasma cholesterol. N Engl J Med 1986;314:745-8.
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4.Mensink RP, Katan MB. Effect of dietary fatty acids on serum lipids and lipoproteins: a meta-analysis of 27 trials. Arterioscler Thromb 1992;12:911-9.
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5.Mensink RP, Katan MB. Effect of monounsaturated fatty acids versus complex carbohydrates on high-density lipoproteins in healthy men and women. Lancet 1987;1:122-5.
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6.Lee-Han H, Cousins M, Beaton M, et al. Compliance in a randomized clinical trial of dietary fat reduction in patients with breast dysplasia. Am J Clin Nutr 1988;48:575-86.
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7.Ernst N, Fisher M, Smith W, et al. The association of plasma high-density lipoprotein cholesterol with dietary intake and alcohol consumption. Circulation 1980;62:Suppl IV:IV-41-IV-52.
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8.Vega GL, Grundy SM. Hypoalphalipoproteinemia (low high density lipoprotein) as a risk factor for coronary heart disease. Curr Opin Lipidology 1996;7:209-16.
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9.Willett WC. Is dietary fat a major determinant of body fat? Am J Clin Nutr (in press).
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10.National Diet-Heart Study Research Group. Body weight changes. Circulation 1968;37:Suppl I:I-170-I-180.
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11.Jeffery RW, Hellerstedt WL, French SA, Baxter JE. A randomized trial of counseling for fat restriction versus calorie restriction in the treatment of obesity. Int J Obes Relat Metab Disord 1995;19:132-7.
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12.Black HS, Herd JA, Goldberg LH, et al. Effect of a low-fat diet on the incidence of actinic keratosis. N Engl J Med 1994;330:1272-5.
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13.Sheppard L, Kristal AR, Kushi LH. Weight loss in women participating in a randomized trial of low-fat diets. Am J Clin Nutr 1991;54:821-8.
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14.Kasim SE, Martino S, Kim PN, et al. Dietary and anthropometric determinants of plasma lipoproteins during a long-term low-fat diet in healthy women. Am J Clin Nutr 1993;57:146-53.
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15.Willett WC. Diet and health: what should we eat? Science 1994;264:532-7.
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16.Willett WC. Cancer prevention: diet and risk reduction: FAT. In: DeVita V, Hellman S, Rosenberg S, eds. Cancer: principles and practice of oncology. 5th ed. New York: Lippincott-Raven, 1997:559-66.
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Although there is refreshing agreement about increasing the consumption of plant-derived foods, we suggest that a greater amount be consumed, to provide optimal intake of fiber, antioxidants, and other protective factors. In the study cited by Katan et al., (1) subjects were fed a high-fat diet (41 percent of total energy), most of this from olive oil, which would dilute the effect of grains, beans, vegetables, and fruits. We emphasize that Americans have already cut fat intake to 33 percent of total energy consumption, but the fat has been replaced largely with sugar, not complex carbohydrates and fiber. Fat intake should be reduced further. A low-fat diet (27 percent of energy intake from fat) is even advantageous for blood-pressure reduction. (2)
There are no data showing that the physiologic reduction of HDL cholesterol levels with a low-fat diet is detrimental. Diet-induced lowering of HDL cholesterol does not confer the same risk of atherosclerosis as do low HDL cholesterol levels in Americans consuming a high-fat diet. (3) Lowering HDL cholesterol levels by the consumption of a low-fat diet results in more rapid clearance of HDL and decreased transport of HDL apoproteins. (3) Populations eating a low-fat diet that have low HDL cholesterol levels do not have an increased incidence of coronary disease. (4,5) Neither do patients with some forms of inherited low plasma HDL cholesterol levels, including Tangier disease, in which HDL is virtually absent. (6)
Finally, the recommendations of Katan et al. invite the American public to increase fat intake when all health agencies are advocating the consumption of less fat and more complex carbohydrates and fiber. Such conflicting recommendations only compound public confusion about health and nutrition. Ninety years of research should permit the scientific community to speak with a consistent voice about diet and the prevention of coronary disease. The public deserves the opportunity to implement fully the current, scientifically sound recommendations.
References
1.Mensink RP, Katan MB. Effect of monounsaturated fatty acids versus complex carbohydrates on high-density lipoproteins in healthy men and women. Lancet 1987;1:122-5.
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2.Appel LJ, Moore TJ, Obarzanek E, et al. A clinical trial of the effects of dietary patterns on blood pressure. N Engl J Med 1997;336:1117-24.
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3.Brinton EA, Eisenberg S, Breslow JL. A low-fat diet decreases high density lipoprotein (HDL) cholesterol levels by decreasing HDL apolipoprotein transport rates. J Clin Invest 1990;85:144-51.
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4.Connor WE, Cerqueira MT, Connor RW, Wallace RB, Malinow MR, Casdorph HR. The plasma lipids, lipoproteins, and diet of the Tarahumara Indians of Mexico. Am J Clin Nutr 1978;31:1131-42.
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5.Knuiman JT, West CE, Burema J. Serum total and high density lipoprotein cholesterol concentrations and body mass index in adult men from 13 countries. Am J Epidemiol 1982;116:631-42.
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6.Rader DJ, Ikewaki K, Duverger N, et al. Very low high-density lipoproteins without coronary atherosclerosis. Lancet 1993;342:1455-8.
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We agree that the intake of fruits, vegetables, and high-fiber foods should be increased and that the high amounts of saturated and trans fatty acids consumed by Americans in the 1950s were unhealthful. However, one cannot generalize from those fats to all fats, because unsaturated fats, which make up the majority of fats in the current U.S. diet, lower LDL cholesterol levels. (1) Reductions in saturated fat and cholesterol in the diet cannot by themselves account for the decline in mortality due to coronary heart disease since the 1950s; increases in the consumption of unsaturated vegetable oils may have been important as well. (2)
Connor and Connor object to substituting unsaturated fats for unhealthful fats because fats produce postprandial lipemia. However, long-term substitution of carbohydrate, instead, does not reduce postprandial lipemia, (3,4) probably because high carbohydrate intake increases the levels of endogenous triglycerides that delay postprandial clearance of lipoproteins. HDL cholesterol levels are also reduced. In the study cited by Connor and Connor, a low-fat, high-fiber diet reduced weight after 12 weeks, but this effect was transient in longer studies (see our Figure 2). There is no good evidence that reducing total dietary fat will prevent cancer or hypertension. (5)
Like Connor and Connor, we lament the plethora of fat-free products high in sugar and the avoidance of foods such as nuts and oil-based salad dressing that provide n-3 fatty acids. However, the failure to distinguish among types of fat and the emphasis on total fat reduction are the very causes of these problems.
Lower consumption of saturated and trans fats is desirable, but nonspecific recommendations to reduce total fat consumption have no strong scientific basis and could be harmful if unsaturated fats are avoided.
References
1.Mensink RP, Katan MB. Effect of dietary fatty acids on serum lipids and lipoproteins: a meta-analysis of 27 trials. Arterioscler Thromb 1992;12:911-9.
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2.Hetzel BS, Charnock JS, Dwyer T, McLennan PL. Fall in coronary heart disease mortality in U.S.A. and Australia due to sudden death: evidence for the role of polyunsaturated fat. J Clin Epidemiol 1989;42:885-93.
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3.Blades B, Garg A. Mechanisms of increase in plasma triacylglycerol concentrations as a result of high carbohydrate intakes in patients with non-insulin-dependent diabetes mellitus. Am J Clin Nutr 1995;62:996-1002.
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4.Chen YD, Coulston AM, Zhou MY, Hollenbeck CB, Reaven GM. Why do low-fat high-carbohydrate diets accentuate postprandial lipemia in patients with NIDDM? Diabetes Care 1995;18:10-6.
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5.Morris MC. Dietary fats and blood pressure. J Cardiovasc Risk 1994;1:21-30.
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Copyright © 1997 by the Massachusetts Medical Society. All rights reserved.
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