¹Centro de Investigacion en Alimentacion y Desarrollo, Hermosillo, Mexico

²Phoenix Epidemiology and Clinical Research Branch, NIH/NIDDK, Phoenix, AZ, USA

³University of Wisconsin-Milwaukee, Milwaukee, WI, USA

Correspondence to: E Ravussin, Director, Obesity Research, Lilly Research Laboratories, Lilly Corporate Center, Drop Code 0545, Indianapolis, IN 46285, USA. Eric_Ravussin@Lilly.com.

^aEqual contribution.

BACKGROUND: Obesity is caused by an imbalance between energy intake and energy expenditure. However, it is unknown whether increased physical activity protects susceptible populations against the development of obesity and type 2 diabetes.

OBJECTIVE: To investigate the potential protective role of environment and physical activity against obesity by measuring total energy expenditure in Mexican and USA Pima Indians.

METHODS: We compared the physical activity level of 40 (17 female and 23 male; 37±11 y, 66±13 kg) Mexican Pima Indians from a remote, mountainous area of Northwest Mexico, with 40 age-and-sex matched (17 female and 23 male; 37±12 y, 93±22 kg) Pima Indians from the Gila River Indian Community in Arizona, USA. We measured total energy expenditure (TEE) by doubly labeled water and calculated physical activity by different methods: physical activity level (PAL) as the ratio of TEE on resting metabolic rate (RMR), TEE adjusted for RMR by linear regression, activity energy expenditure adjusted for body weight (AEE), and activity questionnaire.

RESULTS: Physical activity was higher in Mexican Pima Indians when compared with USA Pima Indians as assessed by PAL (1.97±0.34 vs 1.57±0.16, P<0.0001), TEE adjusted for RMR (3289±454 vs 2671±454 kcal/day, P<0.0001) and AEE adjusted for body weight (1243±415 vs 711±415 kcal/day, P<0.0001). Questionnaires revealed more time spent on occupational activities among Mexican Pima compared with USA Pima (23.9±13.3 vs 12.6±13.9 h/week, P<0.001).

CONCLUSION: These data support a significant role for physical activity in the prevention of obesity in genetically susceptible populations.

International Journal of Obesity (2000)24, 55-59

Pima Indians; doubly labeled water; total energy expenditure; resting metabolic rate; physical activity level

Introduction

Obesity is caused by an imbalance between energy intake and energy expenditure. It is inversely associated with physical activity,^1,2,3,4 yet it is unknown whether a decrease in physical activity precedes obesity. Comparisons of the level of physical activity in obese and lean individuals have provided conflicting results.^5,6,7,8,9 However, data from the UK population indicate that decreased physical activity preceded the increase in the prevalence of obesity in this population.¹⁰

The USA Pima Indians have a high prevalence of obesity¹¹ and type 2 diabetes¹² resulting from an interaction between a genetic susceptibility and an 'obesigenic' environment. Although Pima Indians have lower muscle sympathetic nervous activity (MSNA) than age-matched Caucasians,¹³ little evidence exists for ethnic or racial differences in energy expenditure.^14,15 Recent data also show that Pima Indians living in Mexico do not have lower resting metabolic rates than non-Pima Mexicans living in the same environment.¹⁶ To better understand the etiology of obesity among Pima Indians, we investigated the impact of environmental factors on energy expenditure in two groups of Pima Indians living in drastically different environments. Measurements were obtained from Mexican Pima Indians still living a traditional lifestyle in the Sierra Madre Mountains and USA Pima Indians living a typical North American lifestyle. In the restrictive environment in which they live, Mexican Pima Indians are still very lean when compared with their American counterparts.¹⁷ We hypothesized that the energy expenditure (total energy expenditure and physical activity level) would be higher in Mexican Pima Indians. Our results emphasize the importance of physical activity in the prevention of obesity in a genetically susceptible population.

Methods

Pima Indians in Mexico

A group of people calling themselves 'Pimas' lives in Maycoba, Mexico. Maycoba is located in the mountains of northwest Mexico, in the eastern region of the state of Sonora, 340 km southeast of Hermosillo. According to a 1990 census from the Mexican National Indigenistic Institute, 601 Pima Indians reside in this area.¹⁷ As previously described,¹⁶ a population survey was begun in 1991 to determine the prevalence of type 2 diabetes and obesity in Pima Indians and a selected group of non-Pima Mexicans living in Maycoba and surrounding areas. From this study sample, 40 healthy, full-blooded Mexican Pima Indians were recruited to participate in detailed measurements of energy metabolism.

Pima Indians in USA

The Pima Indians of Arizona are examined every ~2 y as part of a continuing longitudinal epidemiological study of NIDDM.¹⁸ Briefly, these examinations include a medical history and tests relating to diabetes and other major health problems. Forty healthy, full-blooded USA Pima Indians who attended a biennial exam between June 1994 and September 1996 were recruited to match the sex and age (±2 y) of the 40 Pimas studied in Mexico.

Experimental protocol

All volunteers were seen on two occasions, one week apart, after a 10 h fast, for dosing with the doubly labeled water, urine collections and assessment of resting metabolic rate. All were healthy, non-diabetic, and not taking any medications known to influence energy metabolism. Anthropometric measurements, body composition (bioelectrical resistance, model BIA-103, RJL Systems, Detroit, MI, using the prediction equation developed for the USA Pima Indians,¹⁹) and resting metabolic rate (RMR) measurements were performed during both clinic admissions;¹⁶ results represent the means of the two measurements.

USA Pima Indians were studied at the research ward of the Clinical Diabetes and Nutrition Section of the NIDDK in Phoenix, AZ, or at the NIH Field Clinic located in the Gila River Indian Community in Sacaton, Arizona, 40 miles southeast of Phoenix. Mexican Pima Indians and non-Pima Mexicans were studied at the Centro de Investigación en Alimentación y Desarrollo, A.C. Field Clinic in Maycoba, Mexico. The experimental protocol was approved by the Institutional Review Boards of the NIDDK, the Tribal Council of the Gila River Indian Community, and the Centro de Investigación en Alimentación y Desarrollo, A.C. in Hermosillo, México.

Total energy expenditure (TEE)

TEE was measured by doubly labeled water as previously described.²⁰ The ingested dose was a 1:20 mixture of 99% ²H₂O and 10% H₂¹⁸O (Cambridge Isotope Laboratories Inc., Andover, MA) and was administered as 1.9 g/kg and 2.1 g/kg of total body weight for females and males, respectively. Complete urine collections were made at ~1.5 (discarded), 3.0 and 4.5 h after dosing on day 1, and twice during a 3 h period 7 days later. The disappearance rates of the stable isotopes were determined as previously described,²¹ and energy expenditure was calculated from CO₂ production using a respiratory quotient of 0.866. In a validation study in 12 subjects who spent a week in a respiratory chamber, the doubly labeled water method underestimated energy expenditure by 2.5% with a precision of ±5.8%.²¹ With our new deuterium equilibration method which reduces the error by a factor of 6 compared with the original zinc reduction method, it is likely that the precision has improved.²²

Resting metabolic rate

After resting comfortably on a bed for 10 min, measurement of the resting metabolic rate (RMR) was initiated for each subject, using a Deltatrac metabolic cart (SensorMedics Corp, Yorba Linda, CA) as previously described.¹⁶ The RMR measurement was repeated under fasting conditions at the return visit. The same cart was used for the 80 volunteers at the three locations. Gas exchange flows were corrected to STPD values according to the measured barometric pressure. In addition, 14 alcohol combustion burns were performed in Maycoba, Mexico and eight in Phoenix/Sacaton, Arizona. During the alcohol burns in Mexico, the average Deltatrac barometric pressure was 641±1.9 mm (expected barometric pressure=634 mm Hg).²³ According to gas recoveries (expected CO₂ production and O₂ consumption calculated from the amount of alcohol burned), oxygen and carbon dioxide values were multiplied by 1.041 for the USA Pima and 0.901 for the Mexican Pima. The average measured RQ was 0.672±0.017 in Maycoba, Mexico and 0.675±0.010 in Arizona and were estimated to be acceptable (expected RQ=0.667).

Physical activity

Indices of physical activity were calculated as follows: (1) physical activity level (PAL) as the ratio of TEE to RMR; (2) the residuals of TEE, after adjustment for RMR, using regression analysis; (3) activity energy expenditure (AEE) estimated as AEE=TEE-(RMR+0.1*TEE) where 0.1*TEE represents the thermic effect of food.²⁴ AEE was then adjusted for differences in body weight using regression analysis. Physical activity was also assessed by a questionnaire that evaluated weekly occupational and leisure activities over the past year.^25,26 An estimate of the individual's activity level was expressed as hours per week of occupational and leisure activities over the past year.²⁷

Statistical analyses

Pearson correlation coefficients and multiple linear regression analyses were performed using the programs of the SAS Institute (Cary, NC) and NCSS Statistical System (NCSS 6.0.1, Kaysville, UT). Energy expenditure results were adjusted for their major determinants by multiple linear regression models and are expressed as adjusted values (on the basis of the entire group of subjects).

Results

Table 1 shows the physical and metabolic characteristics of 40 (17 female, 23 male) Mexican Pima Indians and 40 (17 female, 23 male) USA Pima Indians. Mexican Pima subjects were similar in age (by study design) and height to their USA counterparts, but were lighter and leaner.

Absolute resting metabolic rate was higher in USA Pima Indians whereas total energy expenditure was similar in the two groups (3010±722 vs 2940±514 kcal/day, P=0.50). RQ was higher in Mexican Pima Indians (P<0.0001). RMR was correlated with weight, height and fat-free mass in both groups (r=0.66-0.92, P<0.0001). After adjustment for body weight, USA Pima Indians had RMRs similar to those of Mexican Pima Indians (1726±181 vs 1686±181 kcal/day, P=0.41). TEE was correlated with weight, height and fat-free mass in both groups. AEE was correlated negatively to percentage fat and fat mass in both populations (r=-0.45 to -0.33, P<0.0003). PAL was inversely correlated with percentage fat in USA Pima Indians (r=-0.38, P<0.02), but not in Mexican Pima Indians (r=-0.23, P=0.15).

Effect of environment on physical activity

Table 2 presents the results of the measurement of energy expenditure by doubly labeled water. Total energy expenditure was higher in Mexican Pima Indians after adjustment for fat-free mass (3156±415 vs 2805±415 kcal/day, P<0.004). Figure 1 illustrates the relationship between TEE and fat-free mass in Mexican Pima subjects compared with USA Pima subjects. Physical activity was higher in Mexican Pima Indians compared with USA Pima Indians by all calculation methods (Table 2). Total occupational activity was also higher in Mexican Pima Indians (23.9±13.3 vs 12.6±13.9 h/week, P<0.001). Total occupational activity (includes moderate and hard activities) in h/week was correlated with PAL (r=0.34, P<0.002).

Discussion

We found that physical activity was higher in Mexican Pima Indians when compared with USA Pima Indians. These results indicate a significant role for increased activity in the prevention of obesity in populations that are genetically susceptible.

Effect of environment on physical activity

Although it has been shown that obesity is inversely associated with physical activity,^1,2,3,4 equal or higher levels of physical activity have been demonstrated in obese when compared with lean subjects.^5,6,7,8,9 Low levels of physical activity seem to predispose men, but not women, to obesity.²⁸ Increased physical activity may be a necessary component for the maintenance of energy balance in an environment that provides unlimited opportunities for the consumption of excessive food.²⁹ Diverging trends of decreasing energy intake and increasing body weight suggest that reduced physical activity may be the most important factor explaining the rising prevalence of obesity.^5,30,31 Longitudinal studies in children have shown that a low energy expenditure, particularly energy expended in physical activity, is associated with weight/fat gain.³² Furthermore, a recent study suggests that an increase in spontaneous physical activity may be important in counteracting weight gain during overfeeding.³³

Pima Indians have a high prevalence of obesity¹¹ and type 2 diabetes¹² when exposed to a Westernized or modern environment, such as that in Arizona. However, when living a traditional lifestyle, such as in the Sierra Madre Mountains of Northwest Mexico, Pima Indians remain lean and non-diabetic.³⁴ The Mexican Pima Indians represent an ideal population in which to test the effect of the environment on physical activity patterns and obesity. The degree to which the Mexican Pima and the USA Pima Indians are related is uncertain. Archaeological evidence suggests that the Mexican Pima population was part of a back-migration from Central Mexico 2000 y ago, and anthropologic evidence dates the separation of the two Pima populations at 700-1000 y ago. Additional information, using linguistic patterns, estimates the separation at 700 y ago.³⁵ Thus, it is likely that the two populations are closely related, and efforts using genetic markers are currently underway to quantify their degree of relatedness.

Physical activity was significantly higher in Mexican Pima Indians when compared with USA Pima Indians, regardless of the method used to assess the level of physical activity. The use of TEE/RMR has been criticized because it assumes a non-significant intercept.³⁶ However, our results were confirmed by the use of linear regression analyses to normalize TEE for RMR, and AEE for body weight. The latter expression of physical activity has been criticized because it assumes that all activities have the same degree of weight-bearing.³⁷ There is a substantial difference between the two populations in the type of occupational activities and the time spent performing them. The main activities for the Mexican Pima Indians include wood milling, non-mechanized farming, livestock breeding, security guarding, construction, mining and homemaking. For the USA Pima Indians, farming is mechanized and the rest of the activities are of lower intensity, averaging fewer h per week. As shown in Table 2, the difference in physical activity corresponds to approximately 500-600 kcal/day, which seems reasonable according to the number of hours spent in moderate and hard activity by the two groups.³⁸

Because this is a cross-sectional study, we cannot infer whether decreased physical activity causes obesity, or whether obesity leads to decreased physical activity. Most of the studies that have reported an inverse association between physical activity and obesity are cross-sectional,^2,3,4 and one of the few prospective studies, in infants, measured total energy expenditure but not the actual physical activity level.¹ Thus, it is still debatable whether decreased physical activity causes obesity, or whether obesity leads to decreased physical activity.

Effect of environmental factors on respiratory quotient

Mexican Pima Indians had a significantly higher RQ than USA Pima Indians. In conditions of energy balance, macronutrient intake is the major determinant of RQ.³⁹ The diet of Mexican Pima Indians has recently been reported,⁴⁰ and preliminary results indicate that their diet contains 62% carbohydrate, as compared with 49% in USA Pima Indians.⁴¹ Additionally, cross-sectional data demonstrate an inverse association between fat mass and RQ.⁴² As the Mexican Pima population is significantly leaner than the USA Pima population, the higher observed RQ is probably due to differences in both diet composition and body fat mass.

In summary, we found that Mexican Pima Indians expend significantly more energy in physical activity, a factor which, in combination with a diet lower in fat and higher in fiber content, may protect this group of people against the development of obesity and type 2 diabetes.

Acknowledgements

We wish to thank the members of the Gila River Indian Community and of the Maycoba community for their participation in these studies. Our gratitude also goes to Hortensia Montesinos, Bertha Isabel Pacheco and Ana Cristina Gallegos for data collection in Mexico, and the staff of the PECRB for data collection in Sacaton, Arizona. This study was in part supported by grant NIH-DK45957.

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Figure 1 Relationship between total energy expenditure and fat-free mass in Pima Indians in Mexico and the USA. Statistical analysis showed that the two lines are actually parallel and the linear regression equation is: total energy expenditure (kcal/day)=300+44´fat-free mass (kg)+500 for Mexican Pimas.

Table 1 Physical and metabolic characteristics of Mexican Pima Indians and USA Pima Indians; mean±s.d.

Table 2 Physical activity parameters in Mexican Pima Indians and USA Pima Indians; mean±s.d.