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American Journal of Clinical Nutrition, Vol. 84, No. 5, 1009-1013, November 2006
© 2006 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

Serum cholesteryl fatty acid composition and plasma glucose concentrations in Amerindian women1,2,3

Folke Lindgärde, Bengt Vessby and Bo Ahrén

1 From the Department of Vascular Medicine, Malmö University Hospital (FL) and the Department of Medicine (BA), Lund University, Lund, Sweden, and the Unit for Clinical Nutritional Research, Department of Public Health and Caring Sciences, University of Uppsala, Uppsala, Sweden (BV)

2 Supported by grants from the Swedish Research Council (no. 6834), the Swedish Diabetes Association, the Albert Påhlsson Foundation, Stiftelsen för forskning inom diabetes och kärlsjukdom, Skåne County Health Authority, and the Faculty of Medicine, Lund University.

3 Address correspondence to B Ahrén, Department of Medicine, B11 BMC, SE-221 84 Lund, Sweden. E-mail: bo.ahren{at}med.lu.se.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Diabetes mellitus has reached epidemic proportions in women of Amerindian origin. The risk of developing diabetes has been found to be related to the serum fatty acid composition in whites.

Objective: We prospectively investigated the relation between the serum cholesteryl fatty acid composition and changes in fasting plasma glucose concentrations in Peruvian Indian women who are characterized by hyperinsulinemia in comparison to white women.

Design: A 5-y follow-up study of 73 women with normal fasting plasma glucose values was undertaken by performing a survey in 1999 and a follow-up survey in 2004. The studied variables included anthropometric measurements, plasma insulin and leptin, dietary food consumption from 24-h recall, blood pressure, and serum fatty acid composition.

Results: The participants developed significantly higher fasting plasma glucose concentrations in 2004 compared with 1999 (P < 0.0001) with unaltered plasma insulin values. Palmitoleic acid (16:1n–7) in 1999 was the only fatty acid that was significantly correlated to glucose concentration at follow-up. In a multiple regression analysis that included waist circumference, percentage of body fat, systolic blood pressure, and circulating triacylglycerol, insulin, leptin, and 16:1n–7 as independent determinants, 16:1n–7 and systolic blood pressure were the only significant determinants of plasma glucose concentration 5 y later.

Conclusions: A high proportion of 16:1n–7 in serum is an independent predictor of high plasma glucose concentrations in Amerindian women. The reason for this association remains to be elucidated.

Key Words: Palmitoleic acid • Amerindian women • fasting plasma glucose concentration • insulin sensitivity • leptin • dietary food consumption


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Diabetes mellitus has reached epidemic proportions, with the greatest increases in the developing countries of Africa, Asia, and South America (1). In Amerindian populations, one explanation may be the rapid transition from hunter-gatherer societies to an agricultural lifestyle (2) and the transition to urbanization (3). This development is associated with an increase in cardiovascular risk factors, including insulin resistance (4). Insulin resistance is a principal risk factor for type 2 diabetes mellitus (5). The hallmark of the condition is, however, an inadequate increase in insulin secretion. This is illustrated by findings in the prediabetic phase, which is characterized by insulin resistance: when the ß cells hypersecrete sufficient insulin, normal blood glucose concentrations are maintained, whereas when insulin secretion becomes insufficient to compensate for the ambient insulin resistance, glycemia increases (6–8).

Impairment of insulin sensitivity with accompanied reduction in glucose utilization is related to elevated concentrations of free fatty acids in the plasma (9), increased lipid content in skeletal muscle (10), and a specific fatty acid pattern in body tissues (11–14). Also, the ß cell dysfunction underlying type 2 diabetes may be associated with lipotoxicity (15). Changes in the fatty acid composition in plasma, including an increased proportion of palmitoleic acid (16:1n–7), predict the development of diabetes mellitus (16, 17). An important product of endogenous lipogenesis is 16:1n–7, which is formed through desaturation of palmitic acid (16:0) by {Delta}–9 desaturase (stearoyl desaturase). An increased proportion of 16:1n–7 in plasma is related either to a high intake of 16:0 in the diet (18) or to increased endogenous lipid synthesis with a carbon flux from carbohydrates to fatty acids (19). Note that the studies on which the hypotheses have been based regarding the role of fatty acids in causing glucose intolerance were performed on whites. This is an important limitation, considering the ethnic variability in the occurrence and risk of developing type 2 diabetes (20).

In Peru, a health survey found diabetes in 17% of women, with the highest incidence in the poorest areas (21). We have shown that women from the capital, Lima, comprise a population that is characterized by substantial hyperinsulinemia and increased body fat mass (22). However, plasma leptin concentrations and systolic blood pressure were lower than in a matched white population. Because these women simultaneously exhibited low glucose concentrations, the Amerindian population seems to have the ability to compensate for the insulin resistance in obesity by a sufficient islet response, leading to hyperinsulinemia and avoidance of hyperglycemia. The purpose of the present study was to prospectively evaluate the 5-y relation among serum cholesteryl ester fatty acid composition and insulin sensitivity and fasting plasma glucose concentrations in Amerindian women from Lima, Peru.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study participants
The study population consisted of 182 Peruvian Amerindian women living in a northern urban area of Lima who took part in the study in 1999 (22). A migration antecedent from indigenous Andean communities in Peru was identified in all participants. The age range was 20–59 y, with a mean age of 41 y. Fatty acid composition in serum was measured in 141 subjects. This subgroup was invited to take part in the follow-up examination in 2004. A total of 83 women (59%) participated in the second examination; 99 women had moved or were lost to follow-up. Plasma glucose concentrations were available from 73 subjects in both investigations. These 73 women did not differ significantly from the remaining 109 in baseline characteristics of glucose, insulin, leptin, triacylglycerols, body weight, body fat, or dietary factors. None of the participants was taking cholesterol-lowering medication, was consuming a special diet, or had ongoing cardiovascular disease. The study was undertaken in accord with the Helsinki Declaration of 1975, as revised in 1983.

Methods
The examination procedures were the same in 1999 and 2004, and the examination took place in the morning after an overnight fast at Alternativa, a center for social research and popular education in the district of San Martin, Lima. Body mass index (BMI; in kg/m2) was calculated according to the standard formula. Body fat mass and the percentage fat mass in relation to body mass were determined by measuring the resistance of the body to a low-level electrical current (Biodynamic Model 310e; Biodynamic Research Inc, Seattle, WA). Measurements were performed with subjects lying on a couch for 5 min, and the electrodes were placed on the dorsal surfaces of the right hand and foot. Blood pressure was measured after placing a cuff over the upper right arm after a 5-min rest.

Measurement of plasma insulin, glucose, and leptin concentrations
Serum or plasma was separated from venous blood and stored within 1 h at –20 °C and then brought to Sweden for analysis. Insulin was measured with double-antibody radioimmunoassay techniques with the use of guinea pig anti-human insulin antibodies and human insulin as the standard (Linco Research, St Charles, MO). Plasma glucose was measured by using the glucose oxidase procedure. For the indirect determination of insulin sensitivity, the homeostasis model assessment of insulin resistance (HOMA-IR) was calculated as follows (23):

Formula 1(1)
Note that we used pmol/L as the unit for insulin. Leptin was measured with a radioimmunoassay specific to human leptin (Linco Research).

Lipid extraction and serum fatty acid measurements
The fatty acid composition of serum cholesteryl esters was measured as previously described (24). Serum was extracted with a hexane-isopropanol solution, and cholesteryl esters (only lipid esters that were measured at baseline) were separated from the extract by thin-layer chromatography before interesterification with acidic methanol was performed. Free cholesterol that had been liberated in the reaction was removed by aluminum oxide to avoid contamination of the column. The composition of methylated fatty acids was determined by gas chromatography (25-m NB-351 silica capillary column) with a flame ionization detector and helium as carrier gas. Every 25th sample was a serum control pool. The CV between successive gas chromatography runs was 0.2–5%. The relative amount of fatty acid was expressed as a percentage of the total amount of fatty acids reported.

Enzyme activity index
Stearoyl-CoA desaturase (SCD) is the rate-limiting enzyme that catalyzes the synthesis of 16:1n–7 from 16:0. The enzyme activity was estimated from the ratio of the amount of 16:1n–7 to 16:0 in serum cholesteryl ester.

Dietary intake
Twenty-four–hour recall was used to evaluate the composition of the diet, including saturated and unsaturated fat consumption. Food intake records were obtained within a month of the examination in 1999 and analyzed with the use of the Peruvian tables of food composition, from the Ministry of Health (7th edition), Lima, Peru, 1996.

Statistical analysis
All data are expressed as means ± SDs. Changes in values between 1999 and 2004 were compared by using two-sided t tests and two-sided statistical significance at P value < 0.05. The correlation coefficients between 2 variables were determined by Spearman rank analysis. A multiple regression analysis was undertaken to examine which variables predicted the plasma glucose values for 2004. All statistical analyses were conducted by using the statistical package STATVIEW (version 5.0.1, for Macintosh; SAS Institute Inc, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Comparison of variables obtained in 1999 and 2004
Body composition
As can be seen in Table 1Go, body weight, waist circumference, fat mass, and fat as a percentage of body weight increased significantly during the 5-y period.


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  		TABLE 1. Anthropomorphologic data from the survey in 1999 and the results 5 y later, in 73 Peruvian Amerindian women living in a northern urban area of Lima, Peru1

 
Glucose and insulin
The mean value of plasma glucose increased from 4.1 ± 0.5 to 5.0 ± 1.2 mmol/L (P < 0.0001). In contrast, plasma insulin concentrations did not change significantly during the 5 y. Consequently, when calculating insulin resistance according the HOMA-IR value, it increased, because the plasma glucose concentrations were higher in 2004 (P = 0.0152).

Fatty acid composition of serum cholesteryl esters in 1999 and the prediction of plasma glucose concentrations in 2004
The fatty acid composition of serum cholesteryl esters in samples taken in 1999 is given in Table 2Go. The Spearman rank correlation test was used to analyze the associations between fatty acids and plasma glucose values in 1999 and 2004. Two fatty acids, 16:1n–7 (r = 0.38, P = 0.002) and oleic acid (18:1n–9) (r = 0.27, P = 0.023), and SCD activity (16:1n–7/16:0) (r = 0.42, P = 0.0003) were significantly correlated to glucose concentrations in 2004. None of these variables was correlated significantly to plasma glucose concentrations in 1999. They all, however, correlated also to the change in glucose between 1999 and 2004 (16:1n–7: r = 0.26, P = 0.018; 18:1n–9: r = 0.19, P = 0.041; SCD activity: r = 0.30, P = 0.017). In a partial correlation analysis taking into account 16:1n–7, 18:1n–9, and the ratio of 16:1n–7 to 16:0, only the significance for 16:1n–7 remained.


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  		TABLE 2. Average proportion of fatty acids in serum cholesteryl esters and estimated desaturase activity from the survey in 1999 in 73 Peruvian Amerindian women living in a northern urban area of Lima, Peru1

 
Relation among SCD activity, insulin, leptin, HOMA-IR, and percentage body fat in 1999
SCD activity was positively and significantly correlated to insulin (r = 0.301, P = 0.0071), leptin (r = 0.332, P = 0.003), HOMA-IR (r = 0.285, P = 0.0107), and percentage body fat (r = 0.488, P = 0.0006). In a multiple regression analysis that included percentage body fat, waist circumference, and HOMA-IR as independent predictors, percentage body fat was the only predictor of SCD activity.

Relation between 16:1n–7 content in serum and risk factors for glucose intolerance and cardiovascular disease
In 1999, 16:1n–7 was closely related to a cluster of risk factors associated with the metabolic syndrome and an increased risk of glucose intolerance and cardiovascular diseases (Table 3Go).


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  		TABLE 3. Correlation coefficients (r) between palmitoleic acid content in serum and metabolic variables in 73 Peruvian Amerindian women living in a northern urban area of Lima, Peru in the survey in 19991

 
Predictors of plasma glucose values in 2004
Multiple regression analysis was performed with plasma glucose values in 2004 as the dependent variable and variables from 1999 as the independent variables to examine which variables independently predicted glucose concentrations. It can be seen from Table 4Go that serum 16:1n–7 and systolic blood pressure were significant variables.


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  		TABLE 4. Multiple regression analysis in 73 women with the indicated variables obtained in the survey in 1999 as independent variables and plasma glucose concentration in 2004 as the dependent variable1

 
Dietary intake determined by 24-h recall
Information on mean values and SDs about dietary composition is given in Table 5Go. The food consumption pattern is characterized by a high percentage of calories from carbohydrates (69%) and a low percentage of calories from fat (19%), in comparison with reports from industrialized countries. According to the Spearman rank correlation tests, none of the variables, including the total energy intake and the ratio of saturated to unsaturated fat intake, was able to predict plasma glucose values in 2004.


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  		TABLE 5. Dietary intakes for Amerindian women, determined by 24-h recall in 19991

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Several important and novel findings have been made in this prospective study of Peruvian Amerindian women that warrant discussion. First, 5 y after the baseline examination, in 1999, plasma glucose values were higher, and this was seen in association with unaltered plasma insulin concentrations. Recall that plasma insulin values were increased in comparison to whites at the first examination (22). This suggests that insulin resistance with adequate islet compensation existed at the time of the first examination, whereas after the 5-y period, insulin secretion from ß cells was insufficient to cope with a further deterioration of peripheral insulin sensitivity. The observed increase in glucose concentration may be the consequence of the continuous impairment of insulin sensitivity, as suggested by the increased body weight, body fat mass, and HOMA-IR, possibly concomitant with progressive islet dysfunction. Second, the proportion of 16:1n–7 in serum was a strong, independent predictor of plasma glucose concentrations at the follow-up examination in 2004. This indicates that the increase in plasma glucose values was related to fatty acid metabolism.

Insulin resistance and related disorders are characterized by a specific fatty acid pattern in the serum lipid esters (25, 26). In our study, as in others [reviewed in Vessby et al (27)], an increased content of serum 16:1n–7 and a high ratio between the fatty acids 16:1n–7 and 16:0 were correlated to insulin insensitivity. We also found that serum 16:1n–7 was significantly related to body adiposity, serum concentrations of triacylglycerol, plasma concentrations of leptin and insulin, and systolic blood pressure at the baseline examination. The mechanism behind the relation between 16:1n–7 content and these risk factors, associated with glucose intolerance, is not clear. However, some studies have shown that 16:1n–7 content reflects the hepatic lipid pool, and the elevated concentrations of 16:1n–7 in serum represent a shift of carbon from carbohydrates to fatty acids that may underlie the aggregation of risk factors (19). Endogenous lipid synthesis is probably restricted when the dietary fat intake is high, as in Western industrialized societies, but may be increased in our study population, which is characterized by a low proportion of energy derived from fat (28). Also, when the proportion of saturated fat, including 16:0, increases in the diet, on a shift from a diet rich in unsaturated fat to a diet with a high proportion of saturated fat, the proportion of 16:1n–7 in serum increases (27). A hypothesis gaining credibility is that elevated concentrations of circulating free fatty acids contribute to the complications of obesity, particularly insulin resistance, by promoting excessive deposition of fat in tissues not suited for fat storage, such as skeletal muscle (29). Not only the amount but also the type of fatty acids are of importance. A high content of 16:0 in the diet and in the blood may contribute to impaired insulin sensitivity through several different mechanisms. The precise identity of the lipid factor responsible for lipotoxicity is, however, not known.

Leptin is an important regulator of SCD activity, which appears to be involved in fat storage when its activity is high and in oxidation when the activity is low (30). In contrast to animal studies in which leptin inhibits SCD function, an important component of the antiobesity effect of leptin (31), we found a positive correlation between leptin and SCD activity. In a multiple regression analysis that included percentage body fat, waist circumference, leptin, and HOMA-IR as independent predictors, percentage body fat was the only predictor of SCD activity. Thus, this difference between animal studies and our findings may be due to leptin resistance or lower plasma leptin concentrations in our group.

The present study population is characterized by higher BMI values and lower plasma leptin values adjusted for BMI in comparison to a white population (mean values 0.63 compared with 0.95, respectively) (22). The mean serum value of 16:1n–7 in the present population was 4.98 mmol/L, which is higher than the mean value of 3.5 mmol/L observed in Swedish women of the same age (32). Hence, a relative plasma leptin deficiency may in part explain the increased body adiposity and glucose intolerance observed in women of Peruvian Indian origin.

Only a few studies have explored the relation among serum cholesteryl ester fatty acid composition, insulin resistance, and glucose intolerance in Amerindians. Dietary fat has been considered to be a risk factor in the development of insulin resistance and type 2 diabetes in both Pima Indians and whites (33, 34). Observed differences in insulin sensitivity between nondiabetic Mexican Americans and non-Hispanic whites disappeared when dietary intakes of 16:0 and 16:1n–7 were accounted for, suggesting the possibility that these factors may contribute to the lower insulin sensitivity seen in Mexican Americans (35). Differences in dietary composition, ie, a low fat intake in Lima women (19%) in contrast to a normal dietary fat content (32.7%) of the total calorie intake for the Mexican Indian population, may in part explain why we were unable to observe lower insulin sensitivity coupled with higher total dietary intake among our group of nondiabetic women. Furthermore, no significant relations were found between serum 16:1n–7 and any of the dietary variables.

It was also suggested that reverse causation could explain why plasma fatty acids are associated with type 2 diabetes; that is, disturbed glucose metabolism increases the plasma concentrations of fatty acids (36). Although a limitation of the present study is the small number of subjects in the cohort, the prospective design of the study and the exclusion of women with a history of diabetes and increased fasting plasma glucose concentrations reduced the risk of reverse causation. Nevertheless, we cannot rule out the possibility that subjects with normal fasting glucose concentrations but elevated 120-min values, established by an oral-glucose-tolerance test, were included in the study group. In any case, we conclude that a high proportion of 16:1n–7 in serum is an independent predictor of higher plasma glucose concentrations in Amerindian women. The reason for this association remains to be elucidated.


   ACKNOWLEDGMENTS
 
We thank Miyaray Benavente Ercilla and Laura Retamozo for collecting data and for providing information to the study participants at the Center for Social Research and Popular Education in Lima, Peru. We also thank Lillian Bengtsson and Siv Tengblad for technical assistance.

FL and BA were responsible for the study design; FL was responsible for data collection; BA and BV were responsible for data analysis; and FL, BV, and BA were responsible for writing the manuscript. None of the authors had any financial or personal conflicts of interest.


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 RESULTS
 DISCUSSION
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Received for publication January 28, 2006. Accepted for publication July 5, 2006.




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