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Low-Fat Diets

N Engl J Med 1998; 338:127-129January 8, 1998

Article

To the Editor:

We need to move beyond simplistic concepts such as the idea that low-density lipoprotein (LDL) cholesterol is “bad” and high-density lipoprotein (HDL) cholesterol is “good.” A low HDL level in a person consuming a diet that is low in fat, cholesterol, and animal protein may have prognostic implications that differ from those of a low HDL level in a person consuming a typical American diet.1

In the Lifestyle Heart Trial, we found additional support for the statement by Connor and Connor (Aug. 21 issue),2 “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.” Patients in the Lifestyle Heart Trial were asked to consume a vegetarian diet that was low in fat (providing approximately 10 percent of calories from fat), high in complex carbohydrates, and low in simple carbohydrates. All oils were excluded from the diet.

Patients in the treatment group had significant reductions in both LDL and HDL cholesterol levels. However, these patients had a 91 percent reduction in angina after one year and a 72 percent reduction after four years. Quantitative coronary arteriography showed a significant reduction in stenosis after one year and an even greater improvement after four years in the treatment group, whereas patients in the control group had an overall progression of coronary atherosclerosis after one year, which was even worse after four years.3,4 Cardiac positron-emission tomography showed significant improvement in myocardial perfusion in the treatment group but worsening in the control group.5 Also, we found that the number of cardiac events was more than twice as high in the control group as in the treatment group.6 Clearly, lowering HDL cholesterol levels by changing the diet did not harm these patients.

Katan et al. (Aug. 21 issue)7 underscore the importance of obesity as a risk factor. Olive oil contains 14 g of total fat and 2.25 g of saturated fat per tablespoon. From the standpoint of obesity, adding three tablespoons of olive oil to one's pasta or salad is equivalent to adding three scoops of ice cream; few persons would do this and expect to lose weight. From the standpoint of cardiac disease, the more olive oil one consumes, the greater the amount of saturated fat. Olive oil is a better choice than butter or lard, but an even better choice is to eliminate it altogether. A few grams a day of flaxseed oil or fish oil will provide the cardioprotective n - 3 fatty acids that are virtually absent in olive oil. In the Lifestyle Heart Trial, there was an average weight loss of 23.9 lb after one year and 13 lb after four years.

Editor's note: Dr. Ornish consults with ConAgra to develop low-fat, low-cholesterol foods.

Dean Ornish, M.D.
University of California, San Francisco, San Francisco, CA 94143

7 References
  1. 1

    Ornish D, Denke M. Dietary treatment of hyperlipidemia. J Cardiovasc Risk 1994;1:283-286
    CrossRef | Medline

  2. 2

    Connor WE, Connor SL. Should a low-fat, high-carbohydrate diet be recommended for everyone? The case for a low-fat, high-carbohydrate diet. N Engl J Med 1997;337:562-3, 566
    Full Text | Web of Science | Medline

  3. 3

    Ornish DM, Brown SE, Scherwitz LW, et al. Can lifestyle changes reverse coronary heart disease? Lancet 1990;336:129-133
    CrossRef | Web of Science | Medline

  4. 4

    Gould KL, Ornish D, Kirkeeide R, et al. Improved stenosis geometry by quantitative coronary arteriography after vigorous risk factor modification. Am J Cardiol 1992;69:845-853
    CrossRef | Web of Science | Medline

  5. 5

    Gould KL, Ornish D, Scherwitz L, et al. Changes in myocardial perfusion abnormalities by positron emission tomography after long-term, intense risk factor modification. JAMA 1995;274:894-901
    CrossRef | Web of Science | Medline

  6. 6

    Ornish DM, Brown SE, Billings JH, et al. Can lifestyle changes reverse coronary atherosclerosis? Four-year results of the Lifestyle Heart Trial. Presented at the American Heart Association 66th Scientific Sessions, Atlanta, November 1993.

  7. 7

    Katan MB, Grundy SM, Willett WC. Should a low-fat, high-carbohydrate diet be recommended for everyone? Beyond low-fat diets. N Engl J Med 1997;337:563-6, 567
    Web of Science | Medline

To the Editor:

The argument is whether low-fat diets offer better protection against heart disease than diets in which the fat is modified to make up a similar percentage of calories but enriched in monounsaturated fat. The HDL cholesterol level is higher when fat remains in the diet; therefore, the monounsaturated-fat substitution may be better, since HDL cholesterol is protective against coronary heart disease.

This argument is based entirely on risk-factor associations, and no direct data on atherosclerosis in the coronary arteries are discussed. In fact, a recent study of coronary-artery atherosclerosis in African green monkeys found that monounsaturated fat isocalorically substituted for saturated fat failed to provide protection against the development of atherosclerosis, whereas polyunsaturated fat from vegetable oil was protective.1 The data in this model were especially interesting because the study was modeled on an earlier study performed in humans,2 with similar outcomes for lipoprotein risk factors — namely, LDL cholesterol levels were lower in animals fed monounsaturated and polyunsaturated fat than in animals fed saturated fat, and HDL cholesterol levels were lower in animals fed polyunsaturated fat than in those fed monounsaturated and saturated fat. Therefore, the best risk-factor profile in the monkeys fed monounsaturated fat (the lowest ratio of LDL cholesterol to HDL cholesterol) did not translate into a lower likelihood of atherosclerosis.

Nonhuman-primate models of atherosclerosis have had a good track record in predicting the outcome in humans, as discussed by Connor and Connor. Measurement of LDL and HDL cholesterol concentrations also generally predicts atherosclerosis in these models.3 We speculate that the enrichment in the proportion of plasma cholesteryl esters in the form of cholesteryl oleate may be the factor that overcame the improved LDL:HDL ratio, but more work is needed to clarify this point.

The recommendation to increase the monounsaturated-fat content of our diet, as made by Katan et al., seems dangerously premature. No health benefit can be directly ascribed to an increase in monounsaturated fat. The use of the Mediterranean diet as an example is not valid, since it is completely different from the U.S. diet (a mostly vegetarian diet with a lower animal-fat content and more fish). The Mediterranean diet may be good in spite of the olive oil.

Lawrence L. Rudel, Ph.D.
Bowman Gray School of Medicine, Winston-Salem, NC 27157-1040

3 References
  1. 1

    Rudel LL, Parks JS, Sawyer JK. Compared with dietary monounsaturated and saturated fat, polyunsaturated fat protects African green monkeys from coronary artery atherosclerosis. Arterioscler Thromb Vasc Biol 1995;15:2101-2110
    CrossRef | Web of Science | Medline

  2. 2

    Mattson FH, Grundy SM. Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. J Lipid Res 1985;26:194-202
    Web of Science | Medline

  3. 3

    Rudel LL, Bond MG, Bullock BC. LDL heterogeneity and atherosclerosis in nonhuman primates. Ann N Y Acad Sci 1985;454:248-253
    CrossRef | Web of Science | Medline

To the Editor:

The Journal presents important patient-care issues about which the “experts” disagree. Connor and Connor refer to the wealth of data that support the consumption of a low-fat, high-carbohydrate diet to reduce the risk of atherosclerosis, coronary artery disease, and certain forms of cancer. Katan et al. agree with the basic tenets that saturated fat should be reduced and that the consumption of fruits, vegetables, and whole grains should be increased. The controversy focuses on the use of monounsaturated fat as a replacement for saturated fat. However, let me highlight an important phrase that Katan et al. use to qualify their recommendations: “in people who are close to their ideal body weight.” This is not the weight status of 30 percent of the American population or those at greatest risk for the development of the diseases that are the target of the proposed dietary interventions. The layperson may be confused if weight status is not stressed, and he or she may pour olive oil onto food in the belief that this is a healthful thing to do. A similar problem arises if pasta, potatoes, rice, and bread are substituted in isocaloric proportion to the reduction in fat: no weight loss results.

The diseases we are trying to prevent in the majority of people are related to weight. How can caloric restriction or increased energy expenditure, or both, be effectively implemented? Increased physical activity is encouraged, but for elderly persons and those with decreased mobility, this recommendation is problematic. It takes an enormous amount of effort to burn off any substantial number of calories, and oils are concentrated calories — hence, the low-fat recommendation. Fat-free products may add flexibility to the diet, but they must be calorie-reduced foods, not sugar-laden goodies with similar or higher energy concentrations. The recommendation to reduce total calories while maintaining volume and increasing soluble fiber provides a strategy for eating well and decreasing the risk of disease.

Gladys W. Strain, Ph.D., R.D.
Mount Sinai Medical Center, New York, NY 10029

Author/Editor Response

The authors reply:

To the Editor: We appreciate the comments of Drs. Ornish, Rudel, and Strain about the multiple values of low-fat diets. Even the recent Dietary Approaches to Stop Hypertension (DASH) study indicated that a low-fat diet rich in fruits and vegetables lowered blood pressure in both normal subjects and patients with mild hypertension.1 Most of all, we agree that obesity is an ever-increasing problem in this country. The metabolic consequences of the availability of tasty foods in a physically confining environment — in other words, a situation mimicking the U.S. lifestyle — were recently reported. When healthy young men were confined in order to restrict their physical activity and given a high-fat or low-fat diet, the energy balance and cumulative-fat balance were both significantly lower in the men consuming the low-fat diet.2 Furthermore, adiposity in children has been shown to be directly related to the amount of fat consumed in the diet.3 Rolls et al. have also stressed the implications of high-fat diets for obesity.4

The studies by both Ornish et al. and Rudel et al. offer important evidence about the effects of diet on atherosclerosis in humans and monkeys, with vessel lesions being the gold standard for dietary effects. Ornish et al. observed some reversibility of coronary lesions with a very-low-fat diet in humans. Rudel et al. showed that monounsaturated fat failed to protect against atherosclerosis in monkeys, whereas polyunsaturated fat did offer some protection. In humans, an “olive oil formula diet” supplemented with dietary cholesterol did not prevent serum cholesterol levels from increasing by more than 20 percent.5

The recent data plus the long historical tradition about the antiatherogenic properties of a low-fat, low-cholesterol diet composed of natural foods and small amounts of olive oil and other vegetable oils continue to be compelling. Dr. Rudel is correct that most people's concept of the Mediterranean diet is not a “mostly vegetarian diet with a lower animal-fat content and more fish.” Our experience is that many people think of the Mediterranean diet as meat, cheese, ice cream, and chocolate — covered with olive oil. Recommending additional olive oil or other monounsaturated fat would only dilute the fruits, vegetables, grains, and beans and provide a source of calories without other benefits. The scientific evidence currently suggests that a low-fat diet high in complex carbohydrates and increased physical activity are essential for optimal health throughout life.

William E. Connor, M.D.
Sonja L. Connor, M.S., R.D.
Oregon Health Sciences University, Portland, OR 97201-3098

5 References
  1. 1

    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;336:1117-1124
    Full Text | Web of Science | Medline

  2. 2

    Proserpi C, Sparti A, Schutz Y, Di Vetta V, Milon H, Jequier E. Ad libitum intake of a high-carbohydrate or high-fat diet in young men: effects on nutrient balances. Am J Clin Nutr 1997;66:539-545
    Web of Science | Medline

  3. 3

    Tucker LA, Seljaas GT, Hager RL. Body fat percentage of children varies according to their diet composition. J Am Diet Assoc 1997;97:981-986
    CrossRef | Web of Science | Medline

  4. 4

    Rolls BJ, Kim-Harris S, Fischman MW, Foltin RW, Moran TH, Stoner SA. Satiety after preloads with different amounts of fat and carbohydrate: implications for obesity. Am J Clin Nutr 1994;60:476-487
    Web of Science | Medline

  5. 5

    Steiner A, Howard EJ, Akgun S. Importance of dietary cholesterol in man. JAMA 1962;181:186-190
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Author/Editor Response

Dr. Ornish and his colleagues deserve acclaim for their demonstration that lifestyle changes can cause a regression of coronary atherosclerosis.1 However, the patients in their trial1 ate a diet that was not only low in fat but also high in fruits, vegetables, and high-fiber grains and low in sugars. The patients also increased their physical activity, and they lost 10 kg of body wight. The increased activity and weight loss may explain why HDL levels remained constant over a one-year period despite a drastic increase in carbohydrate intake and why the ratio of total cholesterol to HDL cholesterol fell by 20 percent. In contrast, low-fat diets alone hardly affect body weight,2 and they lower total and HDL cholesterol levels proportionally.3 Such diet-induced lowering of HDL cholesterol levels should not be considered safe until its safety has been proved in randomized controlled trials.

Dr. Strain rightfully stresses how serious a problem obesity has become. However, it is a fallacy to think that only calories from fat lead to overweight and that diets high in carbohydrates reduce weight. The evidence shows that they do not. It is time to admit that the present dietary recommendations are ineffective in combating obesity and to start investigating other avenues.

Dr. Rudel's letter affords us the opportunity to correct a misconception. We do not favor adding large amounts of olive oil to an existing diet. What we recommend is reducing the intake of saturated and trans fats and making up the deficit with a balanced mixture of monounsaturated fat, n-6 polyunsaturated fat, and n - 3 fat. The optimal mix of the various unsaturated fats remains an important research topic. Controlled trials 2 and prospective studies 4 confirm the benefit of replacing saturated (and trans) fat with polyunsaturated fat and the lack of a major benefit of replacing saturated fat with carbohydrates. However, the long-term data in humans on the very high intakes of polyunsaturated fat used in the study by Rudel et al. are limited. Therefore, it may be prudent to limit polyunsaturated-fat intake to no more than 10 percent of energy, which is the maximal amount consumed by human populations.5 Our main concern is that foods high in sugar and refined carbohydrates may be considered healthful merely because they can be labeled low fat. In fact, the available evidence indicates that the displacement of unsaturated fats by such foods can be harmful.

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

5 References
  1. 1

    Ornish DM, Brown SE, Scherwitz LW, et al. Can lifestyle changes reverse coronary heart disease? Lancet 1990;336:129-133
    CrossRef | Web of Science | Medline

  2. 2

    Katan MB, Grundy SM, Willett WC. Should a low-fat, high-carbohydrate diet be recommended for everyone? Beyond low-fat diets. N Engl J Med 1997;337:563-6, 567
    Web of Science | Medline

  3. 3

    Knopp RH, Walden CE, Retzlaff BM, et al. Long-term cholesterol-lowering effects of 4 fat-restricted diets in hypercholesterolemic and combined hyperlipidemic men -- the Dietary Alternatives Study. JAMA 1997;278:1509-1515
    CrossRef | Web of Science | Medline

  4. 4

    Hu FB, Stampfer MJ, Manson JE, et al. Dietary fat intake and the risk of coronary heart disease in women. N Engl J Med 1997;337:491-499
    Full Text | Web of Science | Medline

  5. 5

    Seidell JC, Cigolini M, Deslypere JP, Charzewska J, Ellsinger BM. Polyunsaturated fatty acids in adipose tissue in European men aged 38 years in relation to serum lipids, smoking habits, and fat distribution. Am J Epidemiol 1991;134:583-589
    Web of Science | Medline

Citing Articles (7)

Citing Articles

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    Erick Prado de Oliveira, Rodrigo Minoru Manda, Gabriel Augusto Torezan, José Eduardo Corrente, Roberto Carlos Burini. (2011) Dietary, Anthropometric, and Biochemical Determinants of Plasma High-Density Lipoprotein-Cholesterol in Free-Living Adults. Cholesterol 2011, 1-7
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  2. 2

    Sung-Hee Park, Kwang-Soo Lee, Hyun-Young Park. (2010) Dietary carbohydrate intake is associated with cardiovascular disease risk in Korean: Analysis of the third Korea National Health and Nutrition Examination Survey (KNHANES III). International Journal of Cardiology 139:3, 234-240
    CrossRef

  3. 3

    Elizabeth J. Parks. (2002) Changes in fat synthesis influenced by dietary macronutrient content. Proceedings of the Nutrition Society 61:02, 281-286
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  4. 4

    Elizabeth J. Parks, John C. Rutledge, Paul A. Davis, Dianne A. Hyson, Barbara O. Schneeman, C. Tissa Kappagoda. (2001) Predictors of Plasma Triglyceride Elevation in Patients Participating in a Coronary Atherosclerosis Treatment Program. Journal of Cardiopulmonary Rehabilitation 21:2, 73-79
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  5. 5

    Lisa C. Hudgins. (2000) Effect of High-Carbohydrate Feeding on Triglyceride and Saturated Fatty Acid Synthesis. Proceedings of the Society for Experimental Biology and Medicine 225:3, 178-183
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  6. 6

    Elizabeth J. Parks, Ronald M. Krauss, Mark P. Christiansen, Richard A. Neese, Marc K. Hellerstein. (1999) Effects of a low-fat, high-carbohydrate diet on VLDL-triglyceride assembly, production, and clearance. Journal of Clinical Investigation 104:8, 1087-1096
    CrossRef

  7. 7

    (1998) More on Low-Fat Diets. New England Journal of Medicine 338:22, 1623-1624
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