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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 11 4054-4058
Copyright © 1998 by The Endocrine Society

Original Studies

In Situ Lipolytic Responses to Isoproterenol and Physiological Stressors Are Similar in Obese Pima Indians and Caucasians

SØren Snitker, Johan Hellmér, Jr., Michael Boschmann, Olalekan E. Odeleye, Mary Beth Monroe, James B. Young and Eric Ravussin

Clinical Diabetes and Nutrition Section (S.S., O.E.O., M.B.M.,. E.R.), National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Phoenix, Arizona 85016; the Laboratory of Human Behavior and Metabolism, Rockefeller University (J.H., M.B.), New York, New York 10021; and Northwestern University Medical School (J.B.Y.), Chicago, Illinois 60611

Address all correspondence to: Søren Snitker, M.D., Ph.D., Clinical Diabetes and Nutrition Section, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, 4212 North 16th Street, Room 5–41, Phoenix, Arizona 85016. E-mail: ssnitker{at}phx.niddk.nih.gov


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Evidence suggests that impaired lipolysis may contribute to fat accumulation. To test whether the lipolytic response to adrenergic stimulation is lower in Pima Indians, a population prone to obesity and type 2 diabetes mellitus, than in Caucasians, 48 healthy, nondiabetic subjects were studied: 27 Pima Indians (12 males and 15 females, 30 ± 7 yr, 85 ± 18 kg, 36 ± 10% body fat; mean ± SD) and 21 Caucasians (11 males and 10 females, 34 ± 7 yr, 105 ± 26 kg, 39 ± 11% body fat). Lipolysis in the abdominal sc adipose tissue was assessed in situ by glycerol concentration in microdialysis samples at baseline and during local infusion of the nonselective ß-adrenergic agonist isoproterenol (10-6 mol/L), mental stress, and submaximal exercise. The baseline dialysate glycerol concentrations were similar in Pima Indians and Caucasians. Lipolytic response (relative increment in dialysate glycerol concentration, percentage above the baseline) was similar in Pima Indians and Caucasians in response to local isoproterenol infusion (77 ± 36% and 76 ± 40%) and exercise (38 ± 38% and 41 ± 41%). During mental stress, the dialysate concentration did not change significantly from baseline in either group. Changes in local blood flow, determined by ethanol dilution, did not differ between the two groups. In conclusion, the high propensity for obesity in Pima Indians does not seem to be due to an impaired lipolytic response to stimuli.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE PIMA Indians of Arizona have the world’s highest prevalence of type 2 diabetes mellitus (1) and one of the highest prevalences of obesity (2). The metabolic traits responsible for the high prevalence of obesity in Pima Indians are largely unknown. Intracellular lipolysis, the hydrolysis of triacylglycerols into nonesterified fatty acids and glycerol, is a necessary step for fat stored in the adipocyte to be available for oxidation and is stimulated by the catecholamines norepinephrine and epinephrine via an effect on ß-adrenoceptors (3). A putative impairment in lipolysis might predispose the Pima Indians to obesity, as several lines of evidence suggest that impairments in lipolysis may contribute to regional or generalized fat accumulation. First, lipolytic sensitivity to norepinephrine in isolated abdominal fat cells of subjects with upper body obesity is decreased compared to that in subjects with lower body obesity in both sexes (4, 5). Second, measurements of lipolysis in isolated adipocytes predict weight gain (6). Third, decreased lipolytic effects of iv doses of ß-adrenergic agonists have been demonstrated in obese subjects (7, 8, 9, 10). The persistence of this decrease after weight loss (11) supports the idea that a low lipolytic response is causal, not consequential. Fourth, low whole body fat oxidation is an established risk factor for weight gain (12, 13), and whole body fat oxidation is positively correlated with the plasma nonesterified fatty acid concentration (14, 15).

The purpose of the present study was to test in situ whether Pima Indians have lower lipolytic responses than Caucasians to the nonselective ß-adrenergic agonist isoproterenol and to physiological stimulation with mental stress and exercise.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Twenty-seven Pima Indians and 21 Caucasians were studied (Table 1Go). All subjects were healthy, as determined by medical history, physical examination, and routine blood and urine tests, and none took medications or smoked. None was diabetic or had impaired glucose tolerance according to a 75-g oral glucose tolerance test (16). The study was approved by the institutional review board of the NIDDK and the Tribal Council of the Gila River Indian Community, and the subjects gave written informed consent. The subjects were residing in our metabolic research unit and were fed a weight maintenance diet (20% protein, 30% fat, and 50% carbohydrate) for at least 3 days before the microdialysis procedure. Body composition was determined by total body dual energy x-ray absorptiometry (DPX-1, Lunar Corp., Madison, WI) (17). At least 1 day before the day of microdialysis, maximum oxygen capacity (O2max) was determined indirectly on a bicycle ergometer, using the linear relationship between heart rate and oxygen uptake (18).


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  		Table 1. Characteristics of the subjects

 
Microdialysis

The microdialysis procedure has previously been described in detail (19) and was essentially performed as previously reported (20). At 0600 h after an overnight fast, while the subject was in the supine position, an indwelling catheter was inserted for blood sampling in a forearm vein and was kept open with isotonic saline. At 0700 h, the microdialysis probes (CMA/20, CMA/Microdialysis, Solna, Sweden) were inserted into the sc adipose tissue of the abdomen close to the umbilicus, and perfusion was begun with Ringer’s solution at a rate of 5 µL/min. In separate experiments, in situ recovery of glycerol at 5 µL/min, determined by dialysate glycerol concentrations at various flow rates (21), was similar in five lean and five obese subjects (11.1 ± 2.0% and 10.3 ± 4.4%, respectively). For the determination of blood flow, ethanol was added to the Ringer’s solution for a final concentration of 50 mmol/L (22). The dialysate collected during the first 30 min after the insertion of the probes was discarded. For the remainder of the study, dialysate was collected in 10-min fractions. The dialysate samples were aliquoted into two portions; one was stored at -70 C until analysis of glycerol, and the other was stored at 5 C until analysis of ethanol within 24 h. The probes were used as shown in Fig. 1Go.



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  		Figure 1. Experimental protocol. For details, see text.

 
Probe 1, response to local isoproterenol infusion. After a 30-min baseline collection, isoproterenol (isoproterenol HCl, 2 mg/dL; Abbott, North Chicago, IL) was added to the perfusate for a final concentration of 10-6 mol/L, and samples were collected for another 40 min.

Probe 2, response to mental stress and exercise. After the isoproterenol studies, the subject moved to the chair of the recumbent exercise bicycle. After a 15-min equilibration, samples were collected during a 30-min baseline and during a 30-min modified computerized version of the Stroop color-word conflict test (23) supplemented with distracting auditory color-word stimuli. Heart rate and finger arterial blood pressure were measured continuously during the baseline and the test. To avoid bias from differences in previous computer exposure and faulty comprehension of the task, subjects were given a brief introductory session on the night before the test. After the mental stress test, following a 30-min rest, samples were collected during a 30-min baseline and for 30 min while the subject pedaled at approximately 40% O2max. During mental stress and exercise, plasma samples for catecholamine and glycerol concentrations were collected during the baseline period (-15 min) and after 25 min of testing.

Analyses

Plasma insulin concentrations were determined by RIA (Concept 4, ICN, Horsham, PA). Dialysate glycerol concentrations were determined by a luminometric assay (24, 25). The baseline dialysate glycerol concentration was calculated as the mean value of the three 10-min fractions. The isoproterenol-stimulated dialysate glycerol concentration was calculated as the mean value of the three 10-min fractions from 10–40 min because a steady state concentration was not reached until after 10 min (data not shown). Dialysate ethanol concentrations were determined using a standard enzymatic assay (26). Ethanol outflow/inflow ratios were calculated as [ethanoldialysate]/[ethanolperfusate] (27). Plasma catecholamine concentrations were assayed by liquid chromatography with electrochemical detection (Plasma Catecholamine Kit, Bioanalytical Systems, Inc., West Lafayette, IN) (28, 29). Plasma glycerol concentrations were determined by an enzymatic end-point assay (30).

Statistical analyses

SAS 6.08 statistical software was used (SAS Institute, Inc., Cary, NC). Group comparisons were performed by two-tailed t tests, by multiple linear regression analyses, and by repeated measures ANOVA. Relationships between variables were determined by Pearson’s correlation analysis or, when adjusting for covariates, by multiple linear regression. Adjusted values were calculated by adding residuals from multiple linear regression analyses to group means. Plasma concentrations of insulin, norepinephrine, epinephrine, and glycerol were log10 transformed to approximate normal distributions. Throughout, P < 0.05 was considered significant. Values are given as the mean ± SD or, when indicated, as the mean with the range in parentheses. Statistical power was calculated by the formula n = (2{alpha} + 2ß)2 {varsigma}D2/{delta}2, solved for {delta} (31).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Age, percent body fat, waist/thigh ratio, and fasting plasma insulin concentration were similar in the two racial groups (Table 1Go). Because the sex ratio was similar in the two races and because sex was not a significant determinant of lipolysis at baseline or during any of the stimuli, results are generally reported only by race.

Neither baseline dialysate glycerol concentrations (see below) nor baseline ethanol outflow/inflow ratios (Table 2Go) differed between the two races or by sex and were not correlated with percent body fat, waist/thigh ratio, or fasting plasma insulin concentration.


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  		Table 2. Local blood flow estimated by ethanol dilution, expressed as ethanol outflow/inflow ratio

 
Response to isoproterenol

Both baseline dialysate glycerol concentrations before isoproterenol stimulation (31 ± 13 and 27 ± 12 µmol/L, respectively) and the relative increment in the dialysate glycerol concentration (77 ± 36% and 76 ± 40%, respectively; Fig. 2Go) were similar in Pima Indians and Caucasians. Repeated measures ANOVA demonstrated a significant effect of time (P = 0.001) and time x percent body fat interaction (P = 0.01), but no independent effect of race or sex on the response. The relative increment in dialysate glycerol was negatively correlated with the percentage of body fat in Caucasians (r = -0.67; P = 0.001), in females (r = -0.47; P = 0.02), and in all subjects (r = -0.44; P = 0.002; Fig. 3Go, upper panel). Multiple linear regression analyses in all subjects and in each sex and race revealed no significant independent effect of race, sex, waist/thigh ratio, or fasting plasma insulin concentration. The ethanol outflow/inflow ratio decreased in both races (Table 2Go), suggestive of an increase in blood flow, but this decrease did not reach statistical significance. The magnitude of the isoproterenol-induced change in blood flow was not a significant determinant of the lipolytic response and was not related to the percentage of body fat. The statistical power calculation indicated that a true difference in lipolytic response of 17% or greater would be detected with a probability of 0.80.



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  		Figure 2. Relative change in dialysate glycerol concentration as a percentage of baseline in response to isoproterenol and exercise in Pima Indians and Caucasians.

 


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  		Figure 3. Relative change in dialysate glycerol concentration as a percentage of baseline in response to isoproterenol (upper panel) and mental stress (lower panel) as a function of percent body fat. {blacksquare}, Pima Indian males; •, Pima Indian females; {square}, Caucasian males; {circ}, Caucasian females. The regression lines are for all subjects. By multiple linear regression, race and sex were not significant determinants of these relationships.

 
Response to mental stress

Baseline dialysate glycerol concentrations before mental stress were similar in Pima Indians and Caucasians (27 ± 11 and 26 ± 12 µmol/L, respectively). The color-word test evoked significant increases in systolic/diastolic blood pressure and heart rate from baseline similarly in both races (13 ± 16/11 ± 7 mm Hg and 7.7 ± 5.4 beats/min, respectively; P = 0.0001). The mean dialysate glycerol concentration (Fig. 3Go, lower panel) and the mean ethanol outflow/inflow ratio (Table 2Go) did not differ significantly from baseline in either group, but the individual relative changes in the dialysate glycerol concentration correlated inversely with the percentage of body fat in Caucasians (r = -0.48; P = 0.03) and in all subjects (r = -0.35; P = 0.02). Plasma catecholamine and glycerol concentrations did not differ significantly between the two groups (Table 3Go).


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  		Table 3. Plasma concentrations of norepinephrine, epinephrine, and glycerol

 
Response to exercise

Baseline dialysate glycerol concentrations before exercise were similar in Pima Indians and Caucasians (25 ± 7 and 25 ± 11 µmol/L, respectively). As 50 watts was the lowest workload available, the mean relative workload as percentage of O2max differed slightly between Pima Indians and Caucasians (39 ± 11% and 43 ± 14% of O2max, respectively), but this difference was not statistically significant. The mean relative increments in dialysate glycerol concentration were similar in Pima Indians and Caucasians (38 ± 38% and 41 ± 41%, respectively; Fig. 2Go). After adjustment for relative workload by multiple linear regression, there was no relationship between the increment in dialysate glycerol concentration in response to exercise and the percentage of body fat. Plasma catecholamine and glycerol concentrations were similar in the two groups (Table 3Go). The relative increment in the dialysate glycerol concentration was correlated with the increment in plasma norepinephrine (r = 0.38; P = 0.02), and as revealed by multiple linear regression, this relationship was independent of race. Ethanol outflow/inflow ratios did not differ significantly between the groups (Table 2Go).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Based on evidence suggesting that impaired lipolysis may contribute to fat accumulation, the present study was designed to test the hypothesis that the lipolytic response to ß-adrenergic stimulation and physiological stressors is blunted in Pima Indians. In situ lipolytic responses were similar in Pima Indians and Caucasians of similar sex distribution and body composition.

The similar regulation of lipolysis in Pima Indians and Caucasians in the present study, performed in the is natural hormonal and substrate milieu of the adipocyte, in agreement with the findings of a previous study in isolated adipocytes (32).

Isoproterenol was infused for 40 min at a relatively high concentration (10-6 mol/L), which has been shown to cause maximal or near-maximal rates of lipolysis (21). The lipolytic response to isoproterenol did not differ between the races, but was negatively associated with percent body fat in all subjects combined, with no independent effect of race or sex. It cannot be excluded that racial differences would be present at lower concentrations of isoproterenol. The lack of sex differences is consistent with in vitro data in both lean (33) and obese (34) subjects showing similar maximal isoproterenol-stimulated lipolysis in abdominal adipocytes in the two sexes. As the local microcirculation transports glycerol away from the interstitial fluid, it competes with the microdialysis probe for available glycerol, more so the higher the blood flow. Local isoproterenol infusion stimulates adipose tissue blood flow (21), suggesting that the increase in lipolysis in response to isoproterenol is greater than what is apparent from measurement of interstitial glycerol. In the present study, the increase in local blood flow was not significant, possibly due to low sensitivity of the ethanol dilution method at the perfusion rate of 5 µL/min (27), which was chosen to secure an adequate sample volume. It is possible that undetected racial differences in the regulation of vascular tone could have had effects on the dialysate glycerol concentration that exactly canceled out racial differences in lipolysis to produce the almost identical results in the two races, but it should be kept in mind that the lack of racial differences was a consistent finding in response to all three diverse stimuli (isoproterenol, mental stress, and exercise).

The mental stressor caused significant overall increments in arterial pressure and heart rate. The individual changes in lipolytic rates were widely variable (positive or negative), but overall for each group, there was no change from baseline. The overall increase in lipolysis observed by other investigators during a similar color-word test (35) could be due to differences in the way the test was performed or the subject populations, as suggested by the greater increments in heart rate, blood pressure, and plasma catecholamines in the previous study. Although dialysate glycerol concentration did not change, on the average, for the whole group in response to mental stress, the individual changes from baseline, positive or negative, were negatively associated with the percentage of body fat in Caucasians and in all subjects combined with no independent effect of race, similar to what was seen during local isoproterenol stimulation. The inverse relationship in response to the color-word test could possibly be caused by differences associated with the degree of obesity in the balance between lipolysis-activating ß-adrenoceptors and antilipolysis-activating {alpha}2-adrenoceptors, as previously demonstrated in vitro and proposed as an explanation for site- and sex-related differences in tendency for fat accumulation (34, 36).

The exercise also produced similar increments in dialysate glycerol concentration in Pima Indians and Caucasians, but the increments were not related to percent body fat.

Microdialysis with the membrane size and perfusion rate used in the present study does not result in complete equilibrium for glycerol between the extracellular fluid and the dialysate. Recovery, i.e. the relationship between glycerol concentration in the dialysate and that in the extracellular fluid, may therefore have varied from one subject to another. Because of time constraints, recovery was not determined for each subject. However, methodological experiments (reported in Subjects and Methods) only demonstrated small individual differences in recovery and no difference between groups of lean and obese subjects.

Adipocyte size is of interest when assessing lipolysis, as in isolated adipocytes, both basal and adrenergically stimulated lipolysis increase with increasing adipocyte size (37). In a previous study (32), adipocyte size was similar in Pima Indians and Caucasians of similar body composition. As only the abdominal sc fat depot was studied, it is impossible to exclude that racial differences exist in the possibly more pathophysiologically important visceral fat depot. However, lipolytic responses in cells from the two depots are closely associated (38).

In conclusion, this in situ study, performed in the natural substrate and hormonal milieu of the adipocyte, did not demonstrate any differences in the lipolytic responses to isoproterenol and physiological stressors in abdominal sc adipose tissue in Pima Indians compared to those in Caucasians of similar body composition.


   Acknowledgments
 
The authors thank the individuals who volunteered for this study, Dr. J. R. Jennings of the University of Pittsburgh for providing the color-word test, and Ms. Joy Truesdale for practical assistance.

Received April 30, 1998.

Revised July 7, 1998.

Accepted July 14, 1998.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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