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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2005-0281
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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 10 5876-5879
Copyright © 2005 by The Endocrine Society

BRIEF REPORT

Association between Circulating Adiponectin and Interleukin-10 Levels in Android Obesity: Effects of Weight Loss

M. R. Manigrasso, P. Ferroni, F. Santilli, T. Taraborelli, M. T. Guagnano, N. Michetti and G. Davì

G. D’Annunzio Foundation, University of Chieti (M.R.M., F.S., T.T., M.T.G., N.M., G.D.), 66013 Chieti, Italy; and Department of Experimental Medicine and Pathology, University of Rome La Sapienza (P.F.), 00161 Rome, Italy

Address all correspondence and requests for reprints to: Dr. Giovanni Davì, G. D’Annunzio Foundation, University of Chieti, Via Colle dell’Ara, 66013 Chieti, Italy. E-mail: gdavi{at}unich.it.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Objective: Adiponectin inhibits vascular inflammation and increases IL-10 mRNA expression in human macrophages. Thus, we investigated the possible relationship between plasma adiponectin and IL-10 levels and the effects of a diet-induced moderate weight loss on both cytokines.

Patients and Study Design: Plasma adiponectin and IL-10 levels were analyzed in 64 android [body mass index (BMI), >28 kg/m2; waist to hip ratio (WHR), ≥0.86] and 20 gynoid [BMI, >28 kg/m2; WHR, <0.86] obese healthy women. Android obese women (49 ± 14 yr) had a mean BMI of 37.1 ± 5.3 kg/m2, similar to that of gynoid obese women (49 ± 11 yr; BMI, 33.4 ± 2.6 kg/m2). Twenty nonobese control women (46 ± 11 yr; BMI, 25.2 ± 2.2 kg/m2) were also studied. In 15 android obese women, measurements were repeated after a 12-wk diet period (1200 kcal/d).

Results: Median adiponectin [5.2 (range, 3.3–7.8) vs. 12.1 (9.7–13.9) vs. 15.0 (12.6–18.2) µg/ml; P < 0.0001] and IL-10 [1.8 (1.2–3.3) vs. 3.5 (2.9–4.3) and vs. 4.1 (3.5–4.8) pg/ml; P < 0.0001] levels were lower in android vs. gynoid vs. nonobese women. Among android obese women, low adiponectin levels were independently related (P < 0.0001) to decreased IL-10 levels, independently of BMI, WHR, or insulin resistance. No significant change in either median adiponectin or IL-10 levels was observed after body weight reduction (8 ± 4 kg; P < 0.01), although percent changes in adiponectin paralleled those in IL-10 (P < 0.05).

Conclusions: Android obesity is associated with a concomitant reduction of IL-10 and adiponectin levels. However, the antiinflammatory status of obesity might require prolonged periods of energy-restricted diets to revert to normal.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
SINCE THE PIONEERING work of Hotamisligil et al. (1), who demonstrated that adipocytes of obese animals constitutively express TNF-{alpha}, increasing evidence is accumulating suggesting that obesity, especially visceral obesity, is associated with a low-grade inflammatory state. More recently, it has been demonstrated that circulating mononuclear cells in the obese are in a proinflammatory state, with an increase in nuclear factor-{kappa}B-binding activity and a concomitant increase in the expression of nuclear factor-{kappa}B-modulated genes, including TNF-{alpha}, IL-6, and matrix metalloprotease-9 (2).

Adiponectin, a recently described adipokine of emerging importance, is distinct from other known adipokines in that it alone among them appears to inhibit vascular inflammation, being capable of lowering C-reactive protein (CRP) and TNF-{alpha} levels in adiponectin knockout mice (3). A reciprocal association of adiponectin and CRP levels in both human plasma and adipose tissue has also been reported (4). More recently, it was shown that adiponectin increases IL-10 mRNA expression in human macrophages (5). Thus, we investigated the relationship between plasma adiponectin and IL-10 levels in obese women who were otherwise healthy. Moreover, because visceral fat is currently acknowledged as a source of adipokines, we performed subgroup analyses of women with android or gynoid obesity to verify whether fat distribution might influence circulating levels of IL-10 and adiponectin. Finally, the effects of successful weight loss on these analytical variables were also investigated.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
A cross-sectional comparison of adiponectin and IL-10 levels was performed in 104 women of reproductive age: 84 obese healthy women and 20 healthy nonobese women. Obesity was defined on the basis of body mass index (BMI) greater than 28 kg/m2, and women were classified into android or visceral type by waist to hip ratio (WHR) according to the indication of the Italian Consensus Conference of Obesity (6). Women with a BMI higher than 28 kg/m2 and a WHR of 0.86 or more were classified as having android obesity (n = 64); women with a BMI higher than 28 and a WHR lower than 0.86 were classified as having gynoid obesity (n = 20). Clinical characteristics of the three groups are reported in Table 1Go. All women were recruited at the eating disorders clinic of the University of Chieti after they had provided written informed consent. The study was approved by the medical ethics committee of the G. D’Annunzio University Medical School.


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  		TABLE 1. Clinical characteristics of study participants

 
All women were sedentary (<1 h/wk of physical activity); none smoked or took any drug. In addition, they had to be in good general health and physical condition and must not fulfill the criteria recognized by the National Cholesterol Education Program’s Adult Treatment Panel III report for the definition of metabolic syndrome (7). All subjects attended the eating disorders clinic of the University of Chieti after an overnight fast. Sleep/wake pattern and meal timing were synchronized in all women. Blood samples were collected, and anthropometrical measurements were taken by a trained staff according to World Health Organization recommendations (8) after the subject had voided her bladder. Weight was measured to the nearest 0.1 kg, height was measured to the nearest 0.5 cm, and BMI (kilograms per meter squared) was computed. WHR was defined as the minimal abdominal circumference between the xiphoid process and the iliac crests (waist) with subjects standing and breathing normally, divided by the hip circumference, measured on the greater trochanters. Exclusion criteria were clinical cardiovascular disease, diabetes mellitus (9), smoking (more than five cigarettes per day), dyslipidemia (7), and arterial hypertension (10). Women were also excluded if they were pregnant or had delivered in the previous 6 months. Treatment with hormonal contraception or replacement therapy, corticosteroids or nonsteroidal antiinflammatory drugs, and vitamin supplements were considered additional exclusion criteria.

Blood glucose was measured by the glucose oxidase method, and plasma insulin was measured by RIA (Coat-A-Count insulin kit, Diagnostic Products Corp., Los Angeles, CA). Insulin resistance was evaluated by the homeostasis model assessment (HOMA) using fasting insulin and glucose concentrations (11). Circulating plasma levels of adiponectin and IL-10 (Adiponectin and IL-10 Quantikine ELISA kits, R&D Systems, Inc., Minneapolis, MN) were assessed by enzyme immunoassays. Measurements were made in a blinded manner. All samples were assayed in duplicate, and those showing values above the standard curve were retested with appropriate dilutions. Intra- and interassay coefficients of variation for both adiponectin and IL-10 immunoassays were less than 5% and 10%, respectively.

Fifteen android obese women (47.2 ± 6.7 yr; BMI, 39.0 ± 7.3 kg/m2; WHR, 0.95 ± 0.05) underwent a 12-wk weight loss program designed to achieve a reduction of approximately 0.6 kg/wk (55–60% carbohydrate, 15–20% protein, and 20–25% fat; 1200 kcal/d). Successful weight loss was defined as a reduction of at least 5 kg. Women were also encouraged to increase their physical activity during this period. IL-10 and adiponectin levels were measured at baseline and at program completion. The study was performed under the appropriate institutional ethics approvals and in accordance with the principles embodied in the Declaration of Helsinki. Informed consent was obtained from each participating subject.

An ANOVA test followed by a Bonferroni test were used for normally distributed variables. A Kruskal-Wallis test followed by a Mann-Whitney U test was used for post hoc comparison, and a Spearman rank correlation test were employed for nonparametric variables. Multivariate linear regression analysis performed by backward stepping was used to assess relationships among the variables. Data are expressed as the mean ± SD or the median and interquartile range (25th percentile to 75th percentile). Only values of P < 0.05 were regarded as statistically significant. All calculations were made using a computer software package (Statistica 6.0; StatSoft, Inc., Tulsa, OK).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Baseline HOMA, BMI, WHR, and related measurements for the three groups of subjects are summarized in Table 1Go. Only one of the obese women (in the android group) had a BMI of 28.1 kg/m2, which is lower than 30 kg/m2, i.e. the commonly recommended cutoff for definition of obesity (12). The exclusion of this subject from the analysis did not significantly affect the results. Baseline median (interquartile range) levels of circulating adiponectin were significantly lower in 64 android vs. 20 gynoid obese and vs. 20 nonobese women [5.2 (3.3–7.8) vs. 12.1 (9.7–13.9) and vs. 15.0 (12.6–18.2) µg/ml; by Kruskal-Wallis test: H = 40.2; P < 0.0001; Fig. 1AGo]. In addition, we observed significantly lower IL-10 levels in android vs. either gynoid or nonobese healthy women [1.8 (1.2–3.3) vs. 3.5 (2.9–4.3) and vs. 4.1 (3.5–4.8) pg/ml; H = 35.1; P < 0.0001], whereas IL-10 levels of gynoid obese did not significantly differ from those observed in nonobese women (Fig. 1BGo).



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  		FIG. 1. Baseline plasma levels of adiponectin (A) and IL-10 (B) in nonobese, gynoid, and android obese women. The solid line represents the median. IL-10 median levels (interquartile range): android, 1.8 pg/ml (1.2–3.3); gynoid, 3.5 pg/ml (2.9–4.3); and nonobese healthy women, 4.1 pg/ml (3.5–4.8; by Kruskal-Wallis test: H = 35.1; P < 0.0001). Adiponectin median levels (interquartile range): android, 5.2 mg/ml (3.3–7.8); gynoid, 12.1 mg/ml (9.7–13.9); and nonobese healthy women, 15.0 mg/ml (12.6–18.2; by Kruskal-Wallis test: H = 40.2; P < 0.0001).

 
No correlation was observed between either adiponectin or IL-10 baseline levels or the anthropometric measures in the nonobese group. Baseline IL-10 levels were significantly related to adiponectin concentrations (Rho = 0.594; P < 0.0001) among android, but not gynoid, obese women. No correlation was found between either adiponectin or IL-10 levels and HOMA index. Univariate regression analysis of IL-10 predictor variables (age, WHR, BMI, HOMA index, and adiponectin levels) in all 84 obese women showed that WHR [ß (±SE), –0.20 (0.09); P = 0.02], HOMA index [ß (±SE), 0.16 (0.08); P = 0.05] and adiponectin levels [ß (±SE), 0.67 (0.09); P < 0.0001] were all independently related to IL-10. Multivariate analysis performed by backward stepping demonstrated that adiponectin [ß (±SE), 0.72 (0.08); P < 0.0001] was the only variable independently associated with IL-10. Similar results were observed in the subgroup of women with android, but not gynoid, obesity (data not shown).

The effects of a short-term weight loss program on circulating adiponectin and IL-10 levels were investigated in 15 android obese women. A median 8% decrease in BMI was observed in all 15 women, but a significant reduction of weight [from 113 ± 15 to 95 ± 10 kg; mean ± SE, 8 ± 4 kg; P < 0.01] was achieved in 12 participants. Adiponectin and IL-10 were analyzed before and after weight loss in all 15 patients according to an intent to treat basis regardless of a successful reduction of body weight. The HOMA index significantly decreased by 17% (P < 0.02), whereas no significant change in either adiponectin (median change, 1%; range, –19% to 40%; P = 0.23) or IL-10 (median change, 7.3%; range, –17% to 32%; P = 0.99) was observed. Multivariate regression analysis of IL-10 predictor variables (age and percent changes in weight, HOMA index, and adiponectin levels) showed that adiponectin changes [ß (±SE), 0.65 (0.24); P = 0.017], but not HOMA index [ß (±SE), 0.48 (0.24); P = 0.071] were independently related to IL-10 changes.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
A transcriptional mechanism leading to decreased adiponectin plasma levels in obese women has been previously demonstrated, and low levels of adiponectin have been associated with high levels of CRP and IL-6 (13). To our knowledge, this is the first study demonstrating that android, but not gynoid, obesity is associated with a down-regulation of circulating IL-10, and that low adiponectin concentrations are independently related to decreased IL-10 levels in women with android obesity independently of insulin resistance. Based on these results, we hypothesize that adiponectin might modulate the antiinflammatory response through IL-10 expression, as recently suggested by in vitro models of human monocyte-derived macrophages (5, 14).

The finding of decreased IL-10 levels in android obese women appears controversial with previously published data that showed higher IL-10 levels in obese women compared with normal weight individuals (15). However, we must consider that one of the exclusion criteria of our study was the presence of metabolic syndrome, and our obese subjects were otherwise healthy, whereas in the cited study, both obese and nonobese groups included women with metabolic syndrome or one or more cardiovascular risk factors (15). Furthermore, Esposito et al. (15) performed no comparative analysis between android and gynoid obesity. In the present study we found no difference in IL-10 levels between gynoid obese and nonobese women, whereas low IL-10 levels were significantly associated with an increased WHR, suggesting that different fat distribution might be responsible for decreased levels of this cytokine. Thus, differences in the populations recruited and the design of the studies may explain an apparent discrepancy between the two studies.

IL-10 exerts multifaceted antiinflammatory properties, and its reduction may favor the progression of atheromatous lesions toward a vulnerable phenotype (16). Adiponectin may also have antiatherogenic and antiinflammatory properties, and high circulating levels of both proteins have been related to a lower risk of coronary heart disease (16). Because these factors may be regulated by adipocytes and/or adipose tissue, it seems reasonable to expect that weight loss programs might have favorable effects. However, our data do not support this and are in agreement with recent reports indicating that moderate weight loss (17) did not result in a change in plasma adiponectin concentrations. In contrast, Esposito et al. (18) reported that a long-term program of body weight reduction was capable of increasing adiponectin concentrations. However, it should be noted that in the latter study a weight reduction of 10% or more maintained for 2 yr was required for inclusion, whereas in others (17) and in our study a reduction of approximately 8 kg was achieved over a 12-wk period. Moreover, in the study by Esposito et al. (18), adiponectin concentrations were significantly increased in obese individuals who had lost a mean of 14 kg, but not in subjects who had lost a mean of 3 kg. These considerations suggest that changes in plasma adiponectin may not become apparent until substantial amounts of weight have been lost.

Our results also indicated that substantial improvements in insulin sensitivity (assessed by HOMA index) after moderate weight loss were not associated with an increase in plasma adiponectin concentration in android obese women. Because there is ample evidence that insulin resistance is attenuated with this degree of weight loss (19), our findings imply that changes in circulating adiponectin may not mediate weight loss-induced improvements in insulin sensitivity. These data differ from those in studies where much greater amounts of weight were lost (18), but are consistent with the findings by Abbasi et al. (17), who showed that moderate weight loss in obese women was not associated with an increase in plasma adiponectin concentration in either insulin-sensitive or insulin-resistant individuals.

Plasma IL-10 levels did not show any significant change after moderate weight loss, which is in agreement with the finding that a lifestyle change program was unable to substantially modify IL-10 levels in obese women with the metabolic syndrome (15). The significant association observed between the percent changes in IL-10 and adiponectin after a change in diet could be biased by the minimal variation observed and the limited number of subjects, and do not allow any conclusion at this time. However, the independent association of adiponectin and IL-10 levels in multivariate analysis is suggestive of their close relationship.

In summary, this study suggests a discordant effect of moderate body weight loss on reducing cardiovascular risk in obese patients, at least during energy restriction. Inflammatory markers such as CRP (20) and IL-6 (18) appear to be the most sensitive for energy restriction, whereas the antiinflammatory adiponectin and IL-10 are not affected by a moderate weight decrease and might require prolonged periods of energy-restricted diets to revert to normal.


   Footnotes
 
This work was supported by grants from the Italian Ministry of Research and Education (40% and Fondo per gli Investimenti Recerca di Base).

First Published Online July 19, 2005

Abbreviations: BMI, Body mass index; CRP, C-reactive protein; HOMA, homeostasis model assessment; WHR, waist to hip ratio.

Received February 8, 2005.

Accepted July 12, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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