Original Article
Changes in Lipid and Lipoprotein Levels and Body Weight in Tarahumara Indians after Consumption of an Affluent Diet
N Engl J Med 1991; 325:1704-1708December 12, 1991
- Abstract
- Abstract
Background.
Major new public health problems occur in developing countries as they become more affluent and change their traditional dietary patterns. To study this phenomenon in microcosm, we substituted an "affluent" diet for the traditional diet of a group of Tarahumara Indians, a Mexican people known to consume a low-fat, high-fiber diet and to have a very low incidence of risk factors for coronary heart disease.
Methods.
Thirteen Tarahumara Indians (five women and eight men [including one adolescent]) consumed their traditional diet (2700 kcal per day) for one week, and were then fed a diet typical of affluent societies, which contained excessive calories (4100 kcal per day), total fat, saturated fat, and cholesterol, for five weeks.
Results.
After five weeks of consuming the affluent diet, the subjects' mean (±SE) plasma cholesterol level increased by 31 percent, from 121±5 to 159±6 mg per deciliter (3.13±0.13 to 4.11±0.16 mmol per liter, P<0.001). The increase in the plasma cholesterol level was primarily in the low-density lipoprotein (LDL) fraction, which rose 39 percent, from 72±3 to 100±4 mg per deciliter (1.86±0.08 to 2.59±0.10 mmol per liter, P<0.001). High-density lipoprotein (HDL) cholesterol, usually low in this population, increased by 31 percent, from 32±2 to 42±3 mg per deciliter (0.83±0.05 to 1.09±0.08 mmol per liter). Consequently, the ratio of LDL to HDL levels changed little (2.25 with the base-line diet and 2.38 with the affluent diet). Plasma triglyceride levels increased by 18 percent, from 91±8 to 108±11 mg per deciliter (1.03±0.09 to 1.22±0.12 mmol per liter, P<0.05), with a significant increase in the very-low-density lipoprotein triglyceride fraction. All the subjects gained weight, with a mean increase of 3.8 kg (7 percent).
Conclusions.
When Tarahumara Indians from a population with virtually no coronary risk factors consumed for a short time a hypercaloric diet typical of a more affluent society, they had dramatic increases in plasma lipid and lipoprotein levels and body weight. If sustained, such changes might increase their risk of coronary heart disease. (N Engl J Med 1991;325:1704–8.)
Media in This Article
Figure 1
Mean (±SE) Plasma Total and Lipoprotein Cholesterol Concentrations in 10 Tarahumara Indians.Figure 2
Changes in Individual Plasma Lipid and Lipoprotein Values and Body Weight in the Study Subjects in Response to the Affluent Diet.Article Activity
- Article
WHAT happens when there is a profound change in the traditional diet of a culture, from a customary low-fat diet of largely unprocessed plant foods to an "affluent" diet containing the high-fat and low-fiber foods produced by modern food technology? This pattern of nutritional changes is occurring throughout the developing world.1 The World Health Organization has reported that coronary heart disease is moving from relative rarity in the developing world toward becoming the public health epidemic that it already is in more affluent countries.2 Trowell and Burkitt have described many developing countries in which coronary heart disease has become or is threatening to become a major health problem.3
This affluence has not yet had much effect on the Tarahumara Indians of Mexico, who live on the high plateaus of the Sierra Madre Mountains in the state of Chihuahua. The chief foods of the Tarahumara are corn and beans, other vegetables and fruits, and small quantities of game, fish, and eggs.4 , 5 If sufficient calories are provided, their diet, which has been the traditional fare of Mesoamerica for several thousand years, is nutritionally adequate.5 As might be expected, the Tarahumara diet is extremely low in fat and cholesterol,4 and coronary heart disease is rare.6 The Tarahumara (the name means "fleet of foot") value running. They are slender4 and in excellent cardiovascular condition.4 , 6 Hypertension is not found among them, and their plasma total and low-density lipoprotein (LDL) cholesterol levels are low.4 We judged them to be an ideal people in which to measure the short-term effect of a hypercaloric, affluent diet common in the industrialized countries of the world.
Accordingly, with the valued assistance of the Mexican government and the Jesuit Mission of the Tarahumara, we recruited Tarahumara men and women to consume a diet more typical of the United States than of their own culture. We chose a diet that was high in fat, cholesterol, sugar, and calories and low in complex carbohydrates and fiber. In short, we gave them the same rich intake of nutrients that is available to many Americans every day and that is often consumed in excessive amounts during vacations and holiday seasons.
Methods
Study Subjects
This study was carried out in the small village of Sisoguichi, Chihuahua, in the Sierra Madre Mountains of northern Mexico —the native land of the Tarahumara. The Tarahumara community was notified verbally of our intention to recruit subjects for the study, and people came to Sisoguichi to volunteer. Three of the men we recruited had participated in our previous cholesterol feeding study,7 and they brought neighbors and family members with them. The group of volunteers was more varied than in the previous study, because it included women and had a wider range of ages. The study group consisted of 12 adults (ages, 18 to 35 years) and 1 boy (age, 12 years). The adults (five women and seven men) included four married couples. Three of the five women were lactating. All the subjects were traditional Tarahumara Indians in appearance, language, dress, and customs. The men (not including the boy) and women had a similar body-mass index (defined as the weight in kilograms divided by the square of the height in meters), which was normal in all the subjects except one woman, whose index was 32.4 (as compared with the mean [±SE] of 21.3±1.0 for the four other women and 21.8±1.5 for the men).
The research project was explained to the subjects in the Tarahumara language by an interpreter. Each adult signed a consent form previously approved by our investigational review committee, the Mexican government, and the Sisoguichi Jesuit Mission, which owned the facilities used in the study. These bodies had also approved our experimental protocol. In the case of the adolescent boy, he and the relative with whom he lived provided consent.
A metabolic unit was established in an unused mission-school building near the small community hospital. The study food was weighed and prepared in the kitchen, and the subjects were served in the adjacent dining room. The routine included supervised meals at regular times, daily weighing, and venipuncture twice a week. All the subjects were healthy and cooperative during the study. Their level of physical activity was constant throughout the study.
Dietary Plan
The experimental design consisted of two sequential dietary periods (Table 1Table 1
Composition of Diets during Each Study Period.*). The traditional Tarahumara diet was served during week 1. This was the diet that all the subjects had been consuming; it was low in cholesterol and fat and high in complex carbohydrates and fiber. It was the base-line diet we used in our first metabolic study among the Tarahumara.7 This diet was followed by five weeks of the affluent diet, which reflected the high fat, cholesterol, sugar, and energy content of the typical U.S. diet.8 The cholesterol—saturated fat index,9 which indicates the hypercholesterolemic and atherogenic potential of foods, increased markedly, from 20 in the Tarahumara diet to 149 in the affluent diet.The energy content of the base-line Tarahumara diet was 2700 kcal per day for the men and the one overweight woman and 2200 kcal per day for the boy and the four leaner women. These caloric intakes approximated the estimated eucaloric needs of the subjects.10 The affluent diet was higher in calories: 3400 kcal per day for the first week and 4100 kcal per day for the remaining four weeks for all the subjects. This represented an energy intake of 151 to 186 percent of their estimated eucaloric needs. During the period when the affluent diet was served, the same diet was fed to each subject. Using the same diet for each subject simplified the preparation and serving of meals to these family groups in this rather primitive environment. The Tarahumara readily accepted the affluent diet, probably because food shortages are not uncommon for them and abundant food is considered a luxury to be consumed when available.
Both diets were composed of foods that could be purchased locally. The Tarahumara diet consisted primarily of pinto beans and corn, which was made into tortillas and pinole (ground roasted corn mixed with cold water and consumed as a drink). Servings of fruit, vegetables, chili peppers, coffee, and small amounts of sugar and egg whites were included in the daily meal plan.
In the affluent diet, cheese, butter, lard, egg yolks, and white flour replaced all of the corn tortillas and pinole and some of the beans. Soft drinks, table sugar, and jelly were added to the diet. These foods were used in a daily meal plan consisting of three meals. Refined flour was used to make flour tortillas (made with butter), and cake (made with lard, egg yolk, egg white, and sugar). One third of the day's egg yolk was served at each meal. The egg yolk was scrambled with egg white for breakfast. For lunch and dinner the egg yolk was mixed with vegetable soup and refried beans, respectively. The pinto beans were refried with part of the lard. The cheese was served plain, in individually weighed slices.
Although the affluent diet was planned to be served for five weeks, the period was shortened to four weeks for three of the subjects, for personal reasons.
Regular anthropometric measurements included height, body weight, and triceps skin-fold thickness.
Laboratory Studies
Blood samples were obtained twice weekly throughout the study. Plasma specimens were obtained from venous blood by centrifugation and were immediately frozen. At the end of the study period the frozen samples were transported by air to our laboratory in the United States for immediate analysis. We and others have shown the stability of the lipid and lipoprotein values in plasma frozen for less than one month. Cholesterol and triglyceride levels were measured in all samples with the AutoAnalyzer II (Technicon Instruments, Tarrytown, N.Y.).11 Lipoprotein analyses were performed on one sample from each week according to established Lipid Research Clinics techniques of ultracentrifugation and precipitation.11
Differences within subjects were compared by paired t-test, and differences between groups of subjects by Student's t-test.12 Two-sided P values of 0.05 or less were considered to indicate statistical significance.
Results
Mean Changes in Plasma Lipid and Lipoprotein Levels
The mean (±SE) plasma cholesterol concentration of all the subjects increased from 121±5 mg per deciliter (3.13±0.13 mmol per liter) during the week of the Tarahumara diet to 159±6 mg per deciliter (4.11±0.16 mmol per liter, P<0.001) during the last week of the affluent diet (Fig. 1Figure 1
Mean (±SE) Plasma Total and Lipoprotein Cholesterol Concentrations in 10 Tarahumara Indians.). The increase in the mean plasma cholesterol level was thus 38±3 mg per deciliter (0.98±0.08 mmol per liter), or 31 percent. These changes in plasma cholesterol occurred rapidly; the levels increased from 118±5 to 146±7 mg per deciliter (3.05±0.13 to 3.78±0.18 mmol per liter, P<0.001) after only four days of the affluent diet (Fig. 1). The mean cholesterol level further increased to 158±6 mg per deciliter (4.09±0.16 mmol per liter, P<0.005) after seven days of the affluent diet and ranged from 151 to 162 mg per deciliter (3.90 to 4.19 mmol per liter) during the final four weeks of the study.The level of LDL cholesterol rose significantly from 72±3 mg per deciliter (1.86±0.08 mmol per liter) during the period of the Tarahumara diet to 100±4 mg per deciliter (2.59±0.10 mmol per liter) by the end of the affluent diet — a 39 percent increase (P<0.001) (Fig. 1). The mean concentration of LDL cholesterol increased dramatically during the first week of the affluent diet and was stable thereafter. The high-density lipoprotein (HDL) concentration increased 31 percent, from 32±2 to 42±3 mg per deciliter (0.83±0.05 to 1.09±0.08 mmol per liter, P<0.001). Consequently, the ratio of LDL to HDL levels changed little (2.25 at base line, as compared with 2.38 during consumption of the affluent diet).
The plasma triglyceride level increased from 91±8 to 108±11 mg per deciliter (1.03±0.09 to 1.22±0.12 mmol per liter, P<0.05) during the period of the affluent diet. The very-low-density lipoprotein (VLDL) triglyceride level increased from 58±9 to 81±12 mg per deciliter (0.65±0.10 to 0.91±0.14 mmol per liter, P<0.05). The plasma VLDL cholesterol concentration did not change significantly.
Individual Responses in Plasma Lipid and Lipoprotein Levels
Each subject responded similarly to the affluent diet, with increases in plasma levels of total and LDL cholesterol (Fig. 2Figure 2
Changes in Individual Plasma Lipid and Lipoprotein Values and Body Weight in the Study Subjects in Response to the Affluent Diet.). The increases in plasma cholesterol by the final week of the affluent diet ranged from 16 to 52 percent. The women had a mean increase in plasma cholesterol of 41±3 mg per deciliter (1.06±0.08 mmol per liter, 41±5 percent), not significantly different from the increase in the men (35±5 mg per deciliter [0.91±0.13 mmol per liter], 28±4 percent). The three lactating women had mean increases in plasma cholesterol similar to those in the two nonlactating women. The adolescent boy had the highest plasma level of total cholesterol at both the initial and final measurements. However, his increase in plasma cholesterol of 33 percent was not different from the responses in the adults.The changes in lipoprotein cholesterol in the women and men were also similar (Fig. 2). Concentrations of LDL cholesterol increased in all the subjects while they were consuming the affluent diet, and HDL cholesterol increased in all the subjects except two men. The HDL cholesterol level increased more in the women (from 36±2 to 47±3 mg per deciliter [0.93±0.05 to 1.22±0.08 mmol per liter], P<0.01) than in the men (29±2 to 35±3 mg per deciliter [0.75±0.05 to 0.91±0.08 mmol per liter], P<0.04). The increases in LDL cholesterol were similar in both sexes. The changes in the obese woman were similar to those in the lean subjects.
Changes in Anthropometric Measurements
Body weight rose as expected during the period of the affluent diet (Fig. 2), with an average (±SE) increase of 0.8±0.1 kg per week. All the subjects gained weight. The men gained a mean of 3.6±0.4 kg, and the women 3.7±0.4 kg. The boy gained 5.7 kg. The weight gain was associated with a significant increase in the triceps skin-fold thickness, from 8±2 to 11±2 mm (P<0.0001). The mean body-mass index increased from 22.2±0.9 (desirable body weight in the United States) to 24.1±0.9 (about 10 percent above the desirable weight).8
Discussion
The World Health Organization is now focusing on new dangers to international health as people in developing countries meet the challenges of poverty and infectious disease and move on to encounter a new spectrum of chronic diseases.2 Technological development can markedly change traditional dietary patterns. Consumption shifts from low-fat plant foods to more highly processed foods, such as flour, sugar, fats and oils, and animal products. These changes promote a higher intake of energy, cholesterol, and saturated fat and a lower intake of complex carbohydrates and fiber, as in our experimental affluent diet. When excessive calories are readily available, as has been the case in the United States, people become increasingly overweight with age.13
Early interest in the Tarahumara Indians centered around their remarkable physical endurance and high rates of exercise in a rugged environment far removed from the stresses of life in industrialized societies.14 Our series of studies among the Tarahumara have shown, however, that the marked differences in coronary risk factors between them and people in industrialized societies may be substantially explained by nutritional factors. The Tarahumara habitually consume a diet very low in cholesterol (less than 100 mg per day) and fat (9 to 12 percent of calories) that is associated with a virtual absence of coronary risk factors and especially low plasma total and LDL cholesterol concentrations.4 Large amounts of exogenous cholesterol stimulate changes in Tarahumara Indians similar to those seen in people in the United States —increased absorption of cholesterol by the gut, decreased endogenous synthesis, and an increase in plasma lipid concentrations, particularly LDL.7 , 15
The goal of this study was to mimic for a short time the nutritional changes that occur when a traditional low-fat diet is replaced by a high-fat, hypercaloric diet. In the Tarahumara the result was a rapid increase in several risk factors for coronary heart disease. The increases in plasma cholesterol and LDL cholesterol produced by the affluent diet were more rapid (occurring in just one week) and more sizable than those produced by large amounts of dietary cholesterol alone. In particular, levels of LDL cholesterol rose dramatically, but there were also increases in total plasma cholesterol, HDL cholesterol, triglyceride, and VLDL triglyceride. The subjects also gained an average of 3.8 kg over the five-week period. Gains of about 4 kg (8 to 10 lb) are common in the United States during holiday seasons, vacations, or other events associated with an abundance of rich foods. The results of this experiment could reflect a trend that in the United States occurs over many decades, producing overt hyperlipidemia (the rate of increase in plasma cholesterol in the United States is about 2 mg per deciliter [0.05 mmol per liter] per year16), overweight, and coronary heart disease in a large percentage of the population.
The affluent diet increased the usually low plasma HDL cholesterol concentrations in the Tarahumara at the same time that plasma triglyceride levels and weight rose. HDL cholesterol levels generally increased in parallel with those of LDL cholesterol. This is in contrast to the previous study, in which an increase in dietary cholesterol alone had no effect on the HDL concentrations.7 An increase in plasma HDL cholesterol may be the normal response to a high-fat diet.17 , 18 When low HDL cholesterol levels are associated with low plasma LDL cholesterol concentrations in populations whose habitual diet is also low in fat, there is a low risk of coronary disease.17 , 18
The deleterious effects of the Western diet on the health of Indians in the United States have been seen repeatedly.19 Before the arrival of the Spanish in 1687, the Pima Indians of Arizona consumed a diet of corn and beans that was roughly similar to the current Tarahumara diet.20 The Pima now consume a diet similar in composition to the affluent diet.20 , 21 Their plasma cholesterol concentrations are lower than those of U.S. whites but higher than those of Tarahumara Indians who consume their traditional diet.21 During the period of the affluent diet, plasma cholesterol concentrations in our Tarahumara subjects were similar to levels recently reported in Pima Indians (mean plasma cholesterol, 183 mg per deciliter [4.73 mmol per liter] in men and 165 mg per deciliter [4.27 mmol per liter] in women 25 to 29 years old).21 The body-mass index of the Tarahumara subjects in our study rose to 24.1, similar to the mean body-mass index of men and women in the United States,16 but much lower than the mean levels in the Pima (35 for men and 33 for women 25 to 29 years old21). The Pima have high rates of obesity, Type II diabetes, and gallstones.20 21 22
All our study subjects gained weight during the five weeks of excessive caloric intake, with the mean gain 3.8 kg. The caloric excesses of 700 to 1900 kcal per day (approximately 42,000 kcal more than the estimated need over the five-week period) were similar to those in other overfeeding studies.23 24 25 There was little variation in weight gain among the Tarahumara. The consistency of the increase in body weight may reflect the genetic homogeneity of this group and may be similar to the uniform response to overfeeding found in Pima Indians26 and in male monozygotic twins.25
Although this study does not provide criteria for recommending specific dietary changes, it is timely to consider the health risks in rapidly developing societies that adopt Western dietary habits associated with a high incidence of coronary heart disease and cancer. Many investigators have pointed out that health can deteriorate when traditional societies adopt a Western lifestyle.1 The control of infectious disease, improved sanitation, and more constant food supplies, on the other hand, can improve the health of the developing world. People in the United States are gradually moving away from affluent diets. The consumption of lower-fat foods and more natural, less processed foods such as grains, fruits, vegetables, and legumes is a goal advocated by the Surgeon General, the National Academy of Sciences, and many other governmental and voluntary health organizations.27 28 29 Developing countries, which contain more than three fourths of the world's population, might promote optimal health by retaining traditional foods as much as possible as they become more industrialized.
Supported by research grants from the National Heart, Lung, and Blood Institute (HL37940), the Clinical Nutrition Research Unit (DK40566), and the Clinical Research Center (RR00334), all from the National Institutes of Health.
We are indebted to the Tarahumara Indians for their participation and goodwill, to the Sisoguichi Mission and Bishop Llaguno and his staff for sharing their facilities and assisting us with the study, and to the Mexican government for permission to carry out our research.
Source Information
From the Section of Clinical Nutrition and Lipid Metabolism, Department of Medicine, L465, Oregon Health Sciences University, Portland, OR 97201–3098, where reprint requests should be addressed to Dr. Connor.
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Lucia Pavan, Edoardo Casiglia, Laura M. Carvalho Braga, Mikolaj Winnicki, Massimo Puato, Paolo Pauletto, Achille C. Pessina. (1999) Effects of a traditional lifestyle on the cardiovascular risk profile. Journal of Hypertension 17:6, 749-756
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Michael Miller. (1999) The epidemiology of triglyceride as a coronary artery disease risk factor. Clinical Cardiology 22:S2, II-1-II-6
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Carol A Derby, PhD, Henry A Feldman, PhD, Linda L Bausserman, PhD, Donna R Parker, ScD, Kim M Gans, PhD, Richard A Carleton, MD. (1998) HDL Cholesterol: Trends in Two Southeastern New England Communities, 1981–1993. Annals of Epidemiology 8:2, 84-91
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I. U. Haq, W. W. Yeo, P. R. Jackson, L. E. Ramsay. (1995) The effects of dietary change on serum cholesterol. Proceedings of the Nutrition Society 54:03, 601-616
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PATTI BAZEL GEIL, JAMES W ANDERSON, NANCY J GUSTAFSON. (1995) Women and Men with Hypercholesterolemia Respond Similarly to an American Heart Association Step 1 Diet. Journal of the American Dietetic Association 95:4, 436-441
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(1992) Lipid Levels and Affluent Diets. New England Journal of Medicine 327:1, 52-54
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