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The Journal of Clinical Endocrinology & Metabolism Vol. 88, No. 3 1157-1161
Copyright © 2003 by The Endocrine Society

Relationship between Serum Leptin Concentration and Low-Density Muscle in Postmenopausal Women

Julian Muñoz and Barbara A. Gower

University of Alabama at Birmingham (UAB), Department of Nutrition Sciences, Division of Physiology and Metabolism, and UAB Clinical Nutrition Research Center, Birmingham, Alabama 35294-3360

Address all correspondence and requests for reprints to: Barbara A. Gower, University of Alabama at Birmingham, Department of Nutrition Sciences, 427 Webb Building, 1675 University Boulevard, Birmingham, Alabama 35294-3360. E-mail: bgower{at}uab.edu.


   Abstract
Top
 Abstract
Introduction
 Subject and Methods
 Results
 Discussion
 References
 
The accretion of fat within skeletal muscle has been associated with metabolic abnormalities. Leptin increases muscle fatty acid oxidation and triglyceride hydrolysis. Therefore, leptin concentrations may affect muscle fat content. The objective of this study was to determine if serum leptin concentrations were associated with im lipid content, as reflected in the mid-thigh low-density skeletal muscle area (LDMA). In addition, we evaluated whether hormone replacement therapy (HRT) or ethnicity affected this relationship. Our study population consisted of 80 postmenopausal women aged 45–55 yr, (72 Caucasian and 8 African-American). Both HRT users (n = 50) and nonusers (n = 30) were recruited. Total fat mass was estimated using total body dual-energy x-ray absorptiometry. Fat and muscle areas at the mid-thigh were measured using computed tomography scanning. Results showed that, after adjusting for total fat mass, higher-density muscle area, and ethnicity, higher serum leptin concentration was associated with lower LDMA (P < 0.05). African-American women had greater LDMA than Caucasian women, after controlling for leptin concentration (P < 0.05). Use of HRT did not significantly influence LDMA. These results support the hypothesis that leptin decreases skeletal muscle lipid content, promoting lipid oxidation.


   Introduction
Top
 Abstract
 Introduction
Subject and Methods
 Results
 Discussion
 References
 
THE LOCALIZATION AND composition of fat within skeletal muscle have been identified as major determinants of insulin resistance (1). In particular, intramyocellular lipid (IML), as opposed to adipose tissue accumulation within the muscle sheath, is associated with insulin resistance. One factor affecting the accumulation of skeletal muscle IML is the adipocyte-derived hormone leptin. Leptin has been shown to increase skeletal muscle fatty acid oxidation and triglyceride (TG) hydrolysis in rodent studies, while decreasing fatty acid esterification (2, 3). The improvement of insulin sensitivity in leptin-replaced lipodystrophic subjects reinforced the idea that leptin provides a regulatory signal for insulin sensitivity independent of its effect on calorie restriction, perhaps through depletion of intramyocellular TG (4). Recent research indicates that leptin’s actions on fat oxidation involve activation of AMP-activated protein kinase (AMPK), which inhibits acetyl coenzyme A carboxylase (5). Acetyl coenzyme A carboxylase is a key enzyme involved in substrate partitioning in muscle, and it inhibits lipid oxidation by facilitating pathways involved in lipogenesis (6).

Among women, the postmenopausal condition is associated with increased risk for obesity and insulin resistance (7). Estradiol stimulates skeletal muscle lipid oxidation and adipocyte leptin secretion (8, 9). Thus, the decline in estrogen that occurs with menopause may lead to adipose tissue deposition, as well as to both increased intramyocellular lipogenesis and decreased lipid oxidation, processes that would facilitate intramyocellular lipid accumulation and associated insulin resistance. Whether estrogen replacement therapy (HRT) minimizes deposition of IML, thereby affecting insulin action, has not been determined. However, we have shown that, among women using estrogen-progestin HRT, insulin sensitivity is positively related to lean body mass (primarily skeletal muscle); this relationship was not observed among those not using HRT (10). Taken together, these observations suggest that HRT may affect insulin sensitivity by facilitating the increase in skeletal muscle lipid oxidation induced by leptin.

Ethnic or racial differences have been described in insulin sensitivity (11). African-American individuals, relative to Caucasian individuals, are more insulin resistant, independent of body composition and body fat distribution, but the bases for this difference are not clearly known. Published studies have shown no differences in serum leptin concentrations between African-Americans and Caucasians (12, 13). However, ethnic/racial differences in IML, as well as in the effect of leptin on IML depletion, have not been examined.

Much of the existing data on the association between IML and disease risk factors have been acquired using biopsy material to assess skeletal muscle IML; few studies have used noninvasive, in vivo methods (14, 15). The use of skeletal muscle attenuation for a measure of IML has been validated in a group of 45 men and women (including 10 patients with type 2 diabetes) against muscle fiber lipid content determined histologically with oil red O staining. Reduced attenuation was associated with increased fiber lipid (correlation coefficient of -0.43, P < 0.01) (14). Muscle attenuation, as measured by computed tomography (CT) scanning, is reported to be reduced in obese women and to be inversely related to insulin sensitivity (16, 17). Thus, the use of CT-derived skeletal muscle attenuation may offer a rapid, noninvasive method for assessing relationships between IML and disease risk factors.

Insights into physiological mechanisms that promote skeletal muscle lipid oxidation have implications for the prevention of major obesity-related diseases. Neither the relationship between serum leptin concentration and IML, nor that between estrogen status and IML, has been examined in postmenopausal women. The present study was undertaken to determine if greater serum leptin concentration, use of HRT, or ethnicity/race were associated with lower IML, as reflected in CT-derived attenuation values, in a group of postmenopausal women.


   Subject and Methods
Top
 Abstract
 Introduction
 Subject and Methods
Results
 Discussion
 References
 
Experimental subjects

Subjects were 80 postmenopausal women aged 45–55 yr, 72 Caucasians and 8 African-Americans. Volunteers were recruited via newspaper advertisements and targeted mailings; no effort was made to ensure that the sample was random; however, recruitment efforts were designed to recruit a subject population that was of a similar ethnic make-up as Jefferson County, Alabama (30% African-American for women aged 45–54 yr). Due to eligibility issues and to a lower response rate than anticipated among African-Americans, 12% of the subjects in the parent study were African-American (several individuals were not included in the present analyses due to missing data). Ethnicity was self-reported as was postmenopausal status, which was defined as the spontaneous cessation of menses for at least 6 months before study enrollment. In those with amenorrhea shorter than 1 yr, menopause status was confirmed by an FSH level greater than 30 mIU/ml. Both women using HRT and women not using HRT were recruited. Treatment regimen and duration were also self-reported by the subjects. Among the recruited subjects, 75 women had experienced natural menopause and 5 had had surgical menopause. Fifty women were receiving HRT (six were receiving exclusively conjugated equine estrogens, 40 combined conjugated equine estrogens and medroxyprogesterone acetate, three conjugated equine estrogens and medroxyprogesterone acetate plus testosterone, and one subject was receiving alternative estrogen-progestin therapy). Only women using HRT for between 1 month and 6 yr were included in the study. A nonuser (n = 30) was defined as no current use, and no use within the past 6 months. One nonuser had used HRT greater than 6 months before recruitment. Data were collected over a 27-h period during an in-patient visit to the Department of Nutrition Sciences and the General Clinical Research Center (GCRC) at the University of Alabama at Birmingham (UAB). The protocol was approved by the Institutional Review Board for Human Use at UAB, and all subjects signed an informed consent before testing.

Protocol

Subjects arrived at the Department of Nutrition Sciences at approximately 0900 h in the fasted condition (12-h fast). Body composition was determined by dual-energy x-ray absorptiometry. At approximately 1200 h, subjects were escorted to UAB’s GCRC. Subjects remained at the GCRC for approximately 24 h, departing at noon the following day. At approximately 1900 h, subjects were escorted to Radiology for computed tomography scanning. While at the GCRC, all food was provided. The evening snack was consumed before 1900 h. Subjects then remained fasted until blood collection commenced the following morning (0700 h).

Body composition, fat distribution, and lean tissue density. Total and regional body composition, including total fat mass and lean body mass, were measured using a DPX-L densitometer (Lunar Radiation Corp., Madison, WI) as previously described (18). Intra-abdominal fat, sc abdominal fat, and mid-thigh muscle area were analyzed by computed tomography scanning with a HiLight/Advantage Scanner (General Electric, Milwaukee, WI) set at 120 kVp (peak kilovoltage) and 40 mA, as previously described (19). A scout scan was first performed to locate the L4-L5 intervertebral space. Subsequently, a 5-mm scan of this abdominal site was taken. One 5-mm scan of the right thigh (mid-way between superior border of the patella and the inferior anterior iliac crest) was taken. Scans were later analyzed for cross-sectional area (cm2) of adipose tissue and lean tissue. The analysis was performed on a Macintosh computer using the public domain NIH Image program (developed at NIH and available on the Internet at http://rsb.info.nih.gov/nih-image/). The matrix of pixels was 512 x 512. For adipose tissue, the window measurement was set at -190 to -30 Hounsfield units (HU), and for muscle tissue it was set at 0–100 HU. Mid-thigh low-density muscle area (LDMA) was quantified within the 0–29 HU attenuation window (14, 20). Mid-thigh higher-density muscle area was calculated from the difference between mid-thigh total muscle area and LDMA. The main outcome variable for the study was the proportion of the mid-thigh muscle area that was low density; this was expressed as LDMA statistically adjusted for higher-density muscle area.

Assay of glucose, TGs, insulin, leptin, and estradiol. Serum was obtained after an overnight fast. Glucose and lipids were measured using an Ektachem DT II System (Johnson \|[amp ]\| Johnson Clinical Diagnostics, Rochester, NY) as previously described (21). Serum insulin, estradiol, and leptin were assayed with reagents from Diagnostic Products Corp. (DPC, Los Angeles, CA; insulin and estradiol) and Linco Research Products (St. Charles, MO; leptin) as previously described (18).

Statistics. Values are given as means ± 1 SD. For all analyses, values for body composition variables and serum analytes were log transformed to eliminate skewness. P < 0.05 was considered to indicate statistical significance for all tests. Unpaired, two-tailed t tests were used to compare means between HRT users and nonusers. Simple Pearson correlation analyses were used to examine associations between LDMA and body composition variables. General Linear Model procedures were used to examine associations between LDMA and leptin, after statistically adjusting for total fat mass and higher-density muscle area. Additional models were constructed with ethnicity and HRT use as independent variables. All data were analyzed with SAS software version 8.0 (SAS Institute Inc., Cary, NC; 1998).


   Results
Top
 Abstract
 Introduction
 Subject and Methods
 Results
Discussion
 References
 
Tables 1Go and 2Go display the characteristics of the subjects by treatment group and ethnicity, respectively. The population exhibited a wide range of adiposity, with body mass indexes from 19.0–40.1 kg/m2. The women were in the early postmenopausal stage, with the mean time since last spontaneous menstruation being 2.5 ± 1.6 yr. HRT users had been receiving replacement therapy for a mean period of 2.4 ± 2.0 yr. HRT users had significantly lower fasting serum glucose and insulin concentrations compared with nonusers, as well as lower intra-abdominal fat areas. African-American women, on average, had greater body mass index, lean body mass, and mid-thigh muscle area, and higher serum concentrations of insulin and leptin, than Caucasian women. Among all subjects, univariate analyses showed that LDMA was positively correlated with lean body mass (0.33, P < 0.05) and mid-thigh muscle area (0.48, P < 0.01). No significant correlation was found with fasting serum insulin, TG, intraabdominal fat, or sc abdominal fat.


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  		Table 1. Characteristics of the subjects by HRT use

 

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  		Table 2. Characteristics of the subjects by ethnicity

 
In multiple linear regression analyses adjusting for total fat mass, higher-density muscle area, and ethnicity, leptin was independently associated with LDMA (P < 0.05, Table 3Go). When HRT was included in the same model with or without ethnicity, HRT use was not associated with LDMA (P = 0.53). In general linear modeling analysis, an interaction was detected between ethnicity and leptin (P < 0.05), indicating that, at any given leptin concentration, LDMA was higher among African-Americans. Figure 1Go shows log LDMA, statistically adjusted for total fat and higher-density muscle area using a linear regression technique (22), plotted against log leptin concentration, by ethnic group.


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  		Table 3. Prediction of log LDMA in eighty postmenopausal women

 


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  		Figure 1. Relationship between log low-density mid-thigh muscle area and log serum leptin (adjusted for total body fat and higher-density muscle area), by ethnic group (open circles {circ} = Caucasians, R2 = 0.08, P = 0.06 for regression; black circles • = African-Americans, R2 = 0.78, P < 0.05 for regression); P < 0.01 for the difference between groups.

 

   Discussion
Top
 Abstract
 Introduction
 Subject and Methods
 Results
 Discussion
References
 
Results of this study indicate that, among postmenopausal women, serum leptin concentration and ethnicity were significant determinants of LDMA. After adjusting for adiposity, women with higher leptin had a lower proportion of LDMA (LDMA adjusted for higher-density muscle area), supporting the hypothesis that leptin promotes skeletal muscle lipid oxidation, or inhibits its accumulation. Furthermore, after adjusting for leptin, adiposity, and mid-thigh higher density muscle area, African-American women had a greater LDMA, implying either that skeletal muscle of African-American women is less responsive to leptin, or that African-Americans may have a greater proportion of LDMA due to another mechanism(s). In this population, use of HRT did not influence LDMA.

In rats, leptin enhances fatty acid oxidation and TG hydrolysis in muscle (3). Reduction of muscle TG is associated with improvement in insulin sensitivity clinically (23). Insulin sensitivity is likewise improved by leptin treatment in human patients with lipodystrophy in the absence of weight loss, but with a reduction in IML (24). Taken together, these observations suggest that leptin improves insulin sensitivity by depleting or minimizing intramyocellular lipid stores. This hypothesis is supported by the present results of an inverse association between leptin and LDMA. However, it is important to emphasize that the present data are based on CT-derived estimates of whole muscle lipid accumulation, rather than more direct measures of IML. We adjusted LDMA for total fat mass to statistically eliminate the contribution of obesity to extramyocellular lipid (20), and thereby maximize the likelihood that the LDMA measure reflected IML. Nonetheless, it will be important to verify the present finding with either muscle histochemistry, or with measurements of IML by magnetic resonance spectroscopy.

In this study, ethnicity emerged as a significant predictor of LDMA. After adjusting for total fat mass, higher-density muscle area, and leptin, African-American women had a greater proportion of LDMA. Thus, it appears either that leptin is less active in promoting lipid oxidation among African-Americans, or that an independent factor yet to be identified is responsible for promoting greater IML stores among African-Americans. African-Americans are reported to have a greater proportion of glycolytic "fast-twitch" muscle fibers than Caucasians (25). Leptin’s ability to stimulate AMPK activity is most apparent in red, oxidative fibers and is absent in white, glycolytic fibers (5). Whether racial differences in muscle fiber type play a role in IML accumulation remains to be determined.

African-Americans also are reported to be less insulin sensitive than Caucasians, independent of body composition and body fat distribution (11, 21). The physiological basis for the independent effect of African-American race on insulin sensitivity is not known. Although the number of African-American women in this study was small (n = 8), the present results suggest that greater intramyocellular fat infiltration may contribute to lower insulin sensitivity. Further study is needed to clarify the cause-and-effect relationships among leptin, intramyocellular lipid, muscle fiber type, and insulin sensitivity in African-Americans.

HRT use did not emerge as a significant predictor of LDMA. It is feasible that our measurement of intramyocellular fat infiltration lacked the required sensitivity to detect small variations in IML induced by HRT in a sample with few very obese women. Our measurement of IML is indirect, and because CT measurements have a limited resolution (pixel size 0.94 mm), they are not capable of completely excluding extramyocellular lipid. This limitation also may explain the relatively low proportion of variance explained by the model (13%). However, previous studies have not reported on the amount of variance in IML explained by adiposity and leptin deficiency (lipodystrophy); it is known only that manipulation of this fraction has a physiologically relevant impact on insulin sensitivity (23, 26).

In summary, our results indicated that women with higher leptin had a lower LDMA, supporting the hypothesis that leptin promotes skeletal muscle lipid oxidation. At any given leptin concentration, African-American women showed a greater LDMA, implying that African-Americans may have greater IML, independent of other factors affecting IML deposition. Hormone replacement therapy did not influence LDMA. Further studies, using more accurate measurements of IML content, are needed to assess the role of leptin in muscle metabolism, and the contribution of IML to ethnic differences in insulin sensitivity.


   Acknowledgments
 
We thank Tena Hilario for her dedication as study coordinator.


   Footnotes
 
This work is supported by Grant K01-AG-00740 from National Institute on Aging, GCRC Grant M01-RR-00032, and Clinical Nutrition Research Unit Grant P30-DK-56336.

Abbreviations: AMPK, AMP-activated protein kinase; CT, computed tomography; HRT, hormone replacement therapy; IML, intramyocellular lipid; LDMA, low-density skeletal muscle area; TG, triglyceride.

Received June 20, 2002.

Accepted November 20, 2002.


   References
Top
 Abstract
 Introduction
 Subject and Methods
 Results
 Discussion
 References
 

  1. Shulman GI 2000 Cellular mechanisms of insulin resistance. J Clin Invest 106:171–176[Medline]
  2. Muoio DM, Dohm GL, Fiedorek Jr FT, Tapscott EB, Coleman RA, Dohn GL 1997 Leptin directly alters lipid partitioning in skeletal muscle. Diabetes 46:1360–1363[Abstract]
  3. Steinberg GR, Bonen A, Dyck DJ 2002 Fatty acid oxidation and triacylglycerol hydrolysis are enhanced after chronic leptin treatment in rats. Am J Physiol Endocrinol Metab 282:E593–E600
  4. Oral EA, Simha V, Ruiz E, Andewelt A, Premkumar A, Snell P, Wagner AJ, DePaoli AM, Reitman ML, Taylor SI, Gorden P, Garg A 2002 Leptin replacement therapy for lipodystrophy. N Engl J Med 346:570–578[Abstract/Free Full Text]
  5. Minokoshi Y, Kim Y-B, Peroni OD, Fryer LGD, Muller C, Carling D, Kahn BB 2002 Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415:339–343[CrossRef][Medline]
  6. Vernon RG, Barber MC, Travers MT 1999 Present and future studies on lipogenesis in animals and human subjects. Proc Nutr Soc 58:541–549[Medline]
  7. Rosano GM, Fini M 2002 Postmenopausal women and cardiovascular risk: impact of hormone replacement therapy. Cardiol Rev 10:51–60[CrossRef][Medline]
  8. Toda K, Takeda K, Akira S, Saibara T, Okada T, Onishi S, Shizuta Y 2001 Alterations in hepatic expression of fatty-acid metabolizing enyzmes in ArKO mice and their reversal by the treatment with 17ß-estradiol or a peroxisome proliferator. J Steroid Biochem Mol Biol 79:11–17[CrossRef][Medline]
  9. Tanaka M, Nakaya S, Kumai T, Watanabe M, Tateishi T, Shimizu H, Kobayashi S 2001 Effects of estrogen on serum leptin levels and leptin mRNA expression in adipose tissue in rats. Horm Res 56:98–104[CrossRef]
  10. Munoz J, Derstine A, Gower BA 2002 Fat distribution and insulin sensitivity in postmenopausal women: influence of hormone replacement. Obes Res 10:424–431[Medline]
  11. Lovejoy JC, de la Bretonne JA, Klemperer M, Tulley R 1996 Abdominal fat distribution and metabolic risk factors: effects of race. Metabolism 45:1119–1124[CrossRef][Medline]
  12. Ellis KJ, Nicolson M 1997 Leptin levels and body fatness in children: effects of gender, ethnicity, and sexual development. Pediatr Res 42:484–488[Medline]
  13. Nagy TR, Gower BA, Trowbridge CA, Dezenberg C, Shewchuk RM, Goran MI 1997 Effects of gender, ethnicity, body composition, and fat distribution on serum leptin concentrations in children. J Clin Endocrinol Metab 82:2148–2152[Abstract/Free Full Text]
  14. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R 2000 Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89:104–110[Abstract/Free Full Text]
  15. Boesch C, Kreis R 2000 Observation of intramyocellular lipids by 1H-magnetic resonance spectroscopy. Ann NY Acad Sci 904:25–31[Abstract/Free Full Text]
  16. Goodpaster BH, Theriault R, Watkins SC, Kelley DE 2000 Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49:467–472[CrossRef][Medline]
  17. Goodpaster BH, Thaete FL, Kelley DE 2000 Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes. Am J Clin Nutr 71:885–892[Abstract/Free Full Text]
  18. Gower BA, Nagy TR, Goran MI, Smith A, Kent E 2000 Leptin in postmenopausal women: influence of hormone therapy, insulin, and fat distribution. J Clin Endocrinol Metab 85:1770–1775[Abstract/Free Full Text]
  19. Kekes-Szabo T, Hunter GR, Nyikos I, Nicholson C, Snyder S, Berland L 1994 Development and validation of computed tomography derived anthropometric regression equations for estimating abdominal adipose tissue distribution. Obes Res 2:450–457[Medline]
  20. Goodpaster BH, Thaete FL, Kelley DE 2000 Composition of skeletal muscle evaluated with computed tomography. Ann NY Acad Sci 904:18–24[Abstract/Free Full Text]
  21. Gower BA, Nagy TR, Goran MI 1999 Visceral fat, insulin sensitivity, and lipids in prepubertal children. Diabetes 48:1515–1521[Abstract]
  22. Toth MJ, Goran MI, Ades PA, Howard DB, Poehlman ET 1993 An examination of data normalization procedures for expressing peak VO2 data. J Appl Physiol 75:2288–2292[Abstract/Free Full Text]
  23. Greco AV, Mingrone G, Giancaterini A, Manco M, Morroni M, Cinti S, Granzotto M, Vettor R, Camastra S, Ferrannini E 2002 Insulin resistance in morbid obesity. Diabetes 51:144–151[Abstract/Free Full Text]
  24. Petersen KF, Oral EA, Dufour S, Befroy D, Ariyan C, Yu C, Cline GW, DePaoli AM, Taylor SI, Gorden P, Shulman GI 2002 Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy. J Clin Invest 109:1345–1350[CrossRef][Medline]
  25. Ama PF, Simoneau JA, Boulay MR, Serresse O, Theriault G, Bouchard C 1986 Skeletal muscle characteristics in sedentary black and Caucasian males. J Appl Physiol 61:1758–1761[Abstract/Free Full Text]
  26. Crawford PB, Obarzanek E, Schreiber GB, Barrier P, Goldman S, Frederick MM, Sabry ZI 1995 The effects of race, household income, and parental education on nutrient intakes of 9- and 10-year-old girls. NHLBI Growth and Health Study. Ann Epidemiol 5:360–368[CrossRef][Medline]



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