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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 12 4382-4385
Copyright © 1998 by The Endocrine Society

Original Studies

Evidence for Leptin Regulation of Food Intake in Humans1

Hillevi Larsson, Sölve Elmståhl, Göran Berglund and Bo Ahrén

Departments of Medicine (H.L., G.B., B.A.) and Community Medicine (S.E.), Lund University, Malmö University Hospital, S-205 02 Malmö, Sweden

Address all correspondence and requests for reprints to: Dr. Hillevi Larsson, Department of Medicine, Lund University, Malmö University Hospital, S-205 02 Malmö, Sweden. E-mail: Hillevi.Larsson{at}medforsk.mas.lu.se


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The adipocyte hormone leptin regulates body weight in mice by decreasing food intake and increasing energy expenditure. Whether leptin is of physiological importance for these processes in humans is, however, not clear. We therefore studied the relation between leptin and habitual food intake in 64 healthy postmenopausal women. Dietary habits were assessed with a modified diet history method. Body fat content was measured using bioelectrical impedance. In the 64 women, aged 58.6 ± 0.4 yr (mean ± SD), serum leptin was 19.3 ± 12.7 ng/mL, body mass index was 25.0 ± 3.5 kg/m2, body fat content was 31.6 ± 4.3%, fasting glucose was 4.6 ± 0.5 mmol/L, and fasting insulin was 56 ± 21 pmol/L. Leptin levels were negatively correlated to total energy intake (r = -0.34; P = 0.006), carbohydrate intake (r = -0.36; P = 0.004), and total (r = -0.27; P = 0.034) as well as saturated fat intake (r = -0.31; P = 0.014). Leptin was correlated to the absolute, but not to the percent, intake of these nutrients. When normalized for body fat content, the correlations remained significant. Our results suggest that plasma leptin is involved in the physiological regulation of food intake in humans, and that leptin is related to the quantity rather than the quality of habitual food intake.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
LEPTIN is produced in adipose tissue and is known to regulate body weight in mice. Thus, leptin administration inhibits food intake (1, 2) through a central effect on leptin receptors in the hypothalamus (3, 4), and increases energy expenditure through activating the sympathetic nervous system (5, 6) and uncoupling protein-2 (7, 8). In addition, the importance of endogenous leptin for the regulation of food intake in rats was recently demonstrated using leptin antibodies (9). The combined effects of leptin on food intake and energy expenditure reduce body weight in rodents. In humans, however, the physiological role of leptin is still unclear. It is known that plasma leptin levels are increased in obese humans (10, 11), suggesting that leptin is released from the adipose tissue in relation to adiposity. Furthermore, evidence for long term regulation of body weight by leptin has been presented in Pima Indians (12). Whether these effects are mediated by changes in food intake and/or energy expenditure is not known. Recently, there have been conflicting reports on the relation between leptin and energy expenditure in humans (13, 14, 15), whereas the physiological effects of leptin on food intake are unknown.

It is known from animal experiments that neuropeptides and hormones can affect the intake of specific nutrients (16, 17). For example, in rats, central administration of neuropeptide Y (NPY) stimulates the intake of carbohydrates (18, 19) as opposed to fat intake, which is increased by galanin (20). As leptin has been demonstrated to inhibit NPY in the rat hypothalamus (4, 21, 22), it is conceivable that leptin, in addition to regulating total energy intake, is related to qualitative aspects of food intake. Our aim was to determine whether leptin levels are associated with habitual intake of energy or specific nutrients in humans. We therefore related plasma leptin levels in healthy women to their dietary habits as assessed by a combined method of a food frequency questionnaire and a 7-day menu book.


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

We studied the relation between plasma leptin levels and dietary habits in 64 postmenopausal women with normal glucose tolerance, as determined by a WHO 75-g oral glucose tolerance test (mean ± SD 2 h glucose, 6.3 ± 0.9 mmol/L). The women constituted a random sample of the population of women born in 1935 living in the city of Malmö, Sweden. As previously described, all women born in 1935 were invited to a health screening at Malmö University Hospital (23); 841 women (67.7%) completed the screening procedure in 1990–1991, which included an oral glucose tolerance test. Six hundred and three (71.7%) of the women had normal glucose tolerance. A computerized random sample of 71 of these women with normal glucose tolerance was invited to take part in the present study. Three women declined to take part in the dietary study, and 4 subjects started the study but did not complete it. The 7 women who did not take part in the study were similar to the study group in body weight and body composition. Thus, the complete data from 64 women are presented in this paper. At the time of the study, the women were 57–59 yr of age (mean ± SD age, 58 yr, 7 months ± 5 months). The subjects were all healthy, and none was taking any medication known to affect carbohydrate metabolism. The ethics committee of Lund University approved of the study, and written informed consent was obtained from all participants before entering the study. The mean body mass index (BMI) in the previously studied population of 841 women born in 1935 was 25.1 ± 4.3 kg/m2, with few subjects being underweight (6.3% had BMI <20) or morbidly obese (2.9% had BMI >35). The 64 presently studied women were well representative of the background population with regard to BMI (see Table 1Go).


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  		Table 1. Anthropometric characteristics and habitual dietary intake in the 64 women

 
Dietary habits

The dietary habits of the subjects were assessed with a modified diet history method, which measures the entire diet, including cooking methods. The method combines quantitative and semiquantitative measurements of dietary intake, using a combination of a food frequency questionnaire, which surveys the regularly consumed foods during the last year, and a 7-day menu book (24). The food frequency questionnaire included 168 items of food, covering breakfast, snacks, and fruits. For each food item, usual intake frequency and portion size were given. Portion sizes were estimated using a booklet with pictures of the different food items with varying portion sizes. All cooked meals and beverages during 7 days were recorded in the menu book, including all ingredients of each meal. At the start of the study, the subjects were instructed in a small group by a dietitian how to fill out the questionnaires. Two to 3 weeks later, the subjects returned to the dietitian individually. The dietitian recorded the usual amount consumed by the subject of each food item in the food frequency questionnaire and the 7-day food record. The food data were coded using the Swedish Food Data Base, which is provided by the National Food Administration and gives information on the contents of 34 different nutrients in approximately 1500 food items, drinks, and recipes (25). Thus, the nutrient intake of each individual was calculated.

Anthropometric measurements

All measurements were performed with the subjects wearing light clothing without shoes. Body weight was measured to the nearest 0.1 kg in the morning before breakfast. Height was measured to the nearest centimeter. BMI was calculated as weight (kilograms) divided by height (meters) squared. Waist and hip circumferences were measured with the subjects standing. The waist circumference was measured at the level of the umbilicus, the hip circumference was measured at the level of the greater trochanters, and the waist to hip ratio was calculated as a measure of central adiposity. Body fat content was determined using a validated and reliable bioelectrical impedance analyzer (BIA-109, JRL Systems, Detroit, MI) (26, 27).

Plasma leptin

Samples for analysis of plasma leptin were taken in the morning after an overnight fast. Samples were collected in prechilled tubes containing 0.084 mL ethylenediamine tetraacetate (0.34 mol/L). The analysis was performed with a double antibody RIA using rabbit antihuman leptin antibodies, 125I-labeled human leptin as tracer, and human leptin as standard (Linco Research, Inc., St. Charles, MO). The leptin samples were analyzed in duplicate, and the results are given as the mean of the two samples. The interassay coefficient of variation of the leptin RIA was 1.9% at low leptin values (<5 ng/mL) and 3.2% at higher leptin values (10–15 ng/mL).

Statistics

Data are presented as the mean ± SD. Statistical analyses were performed with the SPSS for Windows system (SPSS Inc., Chicago, IL) (28). Normality of distribution was tested with the Kolmogorov-Smirnov goodness of fit test. Differences between groups were tested with Student’s t test for unrelated samples and ANOVA. Two-sided tests were used, and P < 0.05 was considered statistically significant. Pearson’s product-moment correlation coefficients were obtained to estimate linear correlation between variables.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The mean plasma leptin level in the 64 women was 19.3 ± 12.7 ng/mL. In this population, plasma leptin was normally distributed. Anthropometric characteristics and habitual dietary intake of the women are shown in Table 1Go.

Correlation analyses were performed to assess the relation between plasma leptin levels and dietary intake. We found that leptin correlated negatively with total energy intake (r = -0.34; P = 0.006; Fig. 1Go). Leptin also correlated negatively with the absolute amount of carbohydrate intake and total and saturated fat intake (Table 2Go). The correlation with monounsaturated fat intake was close to significance, whereas leptin was not directly related to the intake of polyunsaturated fat or protein. Leptin did not correlate with the intake of these nutrients, expressed as a percentage of the total energy intake (data not shown), with the exception of protein. There was a significant positive correlation between plasma leptin and percentage of energy eaten as protein (r = 0.26; P = 0.036).



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  		Figure 1. Scatterplot of the correlation between energy intake and plasma leptin in 64 healthy postmenopausal women.

 

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  		Table 2. Correlations between plasma leptin and dietary variables in the 64 women

 
The correlations between leptin and diet might be influenced by the close relation between leptin and body fat content; the correlation between plasma leptin and body fat content in this population was high (r = 0.76; P < 0.001). To assess whether there also is an independent relation between leptin and dietary intake, we normalized both leptin and the dietary variables for body fat content, expressed as body fat mass (Table 2Go). All of the correlations remained significant; in fact, the correlation coefficients were slightly increased. Interestingly, when normalized for fat mass, the relations between plasma leptin and mono- and polyunsaturated fat as well as protein were highly significant.

To further study the relation between plasma leptin and habitual dietary intake, we divided the women into quartiles of plasma leptin. ANOVA showed that energy intake (P = 0.028), carbohydrate (P = 0.029), and saturated fat (P = 0.020) differed among the leptin quartiles, whereas the differences in total fat (P = 0.065) or protein (P = 0.28) were not significant. To examine specifically the impact of high vs. low leptin levels, we compared the quartiles with the highest (>25.9 ng/mL; n = 16) and lowest (<8.8 ng/mL; n = 16) plasma leptin levels. As expected, the group with the highest leptin levels was more obese than the low leptin group (Table 3Go). The high leptin group had a lower energy intake than the low leptin group. Furthermore, the high leptin group had a lower intake of carbohydrate and saturated fat, whereas the intakes of total, monounsaturated, or polyunsaturated fat or protein did not differ between the two groups. There was no difference between high and low leptin groups in the intake of these nutrients expressed as percentage of total energy intake (data not shown).


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  		Table 3. Anthropometric characteristics and habitual dietary intake of the women in the lowest (<8.8 ng/mL; n = 16) and the highest (>25.9 ng/mL; n = 16) quartiles of serum leptin

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Leptin is known to be involved in the regulation of food intake in animals. This study suggests that this is true also for humans, as we found that plasma leptin was correlated negatively to total energy intake in a group of healthy women. Furthermore, leptin was negatively associated with the intake of carbohydrate, fat, and protein. These findings were corroborated when the women were divided into quartiles of leptin levels. Therefore, the higher the leptin level, the lower the intake of energy and nutrients. This suggests that leptin is involved in the regulation of energy balance by inhibiting dietary intake in healthy humans. Our findings could imply that when body weight is increased, the simultaneously increased leptin levels would influence the subject to decrease energy intake and thus reduce body weight. Such a scenario is supported by recent studies in Pima Indians where low leptin levels predicted weight gain in healthy subjects (12). However, prospective studies are required to evaluate the cause and the effect in the observed relationship between leptin and food intake. A strength in the present study was that the women constituted a representative sample of the population, which would allow a more generalized interpretation of the results.

The correlations presented here between nutrients and plasma leptin were independent of body fat content. Thus, it seems that leptin is directly related to food intake at any level of body fat. This strengthens the hypothesis that leptin might regulate energy intake and body weight in humans. In contrast to our finding, a recent study demonstrated a negative correlation between plasma leptin and fat intake, which was not significant after controling for body fat mass (13).

The correlations between leptin and the different nutrients were of similar magnitude, suggesting that leptin is not related specifically to one of these nutrients but, rather, to the total intake. Other evidence for this is that leptin was not related to the intake of these nutrients when expressed as a percentage of total energy intake, but only to the absolute amounts. This implies that leptin is associated with the quantity rather than the quality of carbohydrate and fat intake. This is corroborated by the recent finding that a short term energy-balanced high fat diet did not alter plasma leptin levels in humans (29). Findings in animal studies have implied that leptin regulates the expression of NPY in the hypothalamus (4, 21, 22). As hypothalamic NPY is known to influence the preferences for carbohydrates and fat in the diet by increasing carbohydrate intake (17, 18, 19), a plausible hypothesis is that leptin could also regulate qualitative aspects of energy intake. In the present study there was no evidence for leptin specificity for carbohydrate or fat. There was, however, a significant positive relation between plasma leptin and the energy percentage of protein intake. This correlation was also significant after normalization for body fat mass, but was not reproduced in the study of the high and low leptin quartiles. The reason for this discrepancy is unclear, but could be a result of reduced energy intake leading to increased protein intake as a percentage of total energy intake; there was a significant negative correlation between energy intake and percent protein intake (r = -0.45; P < 0.001). Thus, the finding that leptin was also correlated to the protein intake as a percentage of the total energy supports our hypothesis that leptin regulates total food intake rather than the intake of specific nutrients.

The accuracy of the reported findings is highly dependent on the method of studying dietary intake. In the present study, a combination of a food frequency questionnaire and a 7-day food record was used to assess dietary intake. This method has been previously validated against an 18-day weighed food record in a large group of men and women of similar age and body composition as the women in the present study (24). The weighed records were spread over six periods of 3 days repeated every 2 months to minimize random errors due to day to day variation in food intake. Moreover, the design covered any seasonal variation in food intake. In addition to the weighed food record, urinary nitrogen was measured to objectively assess protein intake, demonstrating high accuracy of the weighed record. It was shown that the combined method used in the present study overestimated energy intake compared to the weighed record by about 14% in women and 29% in men. Overall, the results of the present method were comparable to those of other methods that have been validated in the same manner (24). The reproducibility of the method has also been evaluated, showing high concordance between two measurements performed 1 yr apart in a group of 241 men and women, aged 50–69 yr (30). Therefore, the results of these methodological studies justify the use of this combined method as valid and reproducible for the determination of habitual dietary intake.

Apart from the accuracy of the method, another problem when assessing dietary habits is that of underreporting of dietary intake. It is known that both normal weight and obese subjects underestimate their dietary intake. This has been verified, for example, by comparing weighed food records to measurements of energy expenditure by the doubly labeled water technique, as reviewed by Schoeller (31). In a large group of healthy nonobese men and women, energy intake was underestimated by about 10% (32). Further, the underestimation is larger in highly obese subjects, being around 20% or higher (33, 34). In the present study we did not have the opportunity to directly measure whether there was a degree of underreporting of food intake. Therefore, although the women in the study population were not highly obese, it cannot be excluded that underestimation of food intake could partially explain our finding of a negative correlation between leptin and food intake, because leptin levels are higher in obesity. However, this may not reduce the validity of our general conclusion, as we found that plasma leptin also correlated negatively with food intake after adjustment for body fat, i.e. independent of the influence of obesity on circulating leptin and food intake.

In conclusion, this study has shown that circulating levels of leptin correlate negatively with the amount of food intake in humans, without any obvious correlation to a specific nutrient. Thus, the study suggests that leptin is involved in the physiological regulation of the quantity, but not the quality, of food intake in humans.


   Acknowledgments
 
The authors are grateful to Lilian Bengtsson, Ulrika Gustavsson, Eva Holmström, Gertrud Jensen, and Margaretha Persson for expert technical assistance.


   Footnotes
 
1 This work was supported by the Swedish Medical Research Council (Grant 4X-6834); the Ernhold Lundström, Albert Påhlsson, and Novo Nordic Foundations; the Swedish Diabetes Association; Malmö University Hospital, and the Faculty of Medicine, Lund University. Back

Received April 21, 1998.

Revised June 2, 1998.

Revised August 13, 1988.

Accepted September 4, 1998.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals