Metabolic correlates of eating behavior in severe obesity

Abstract

BACKGROUND: The benefit of spreading energy intake over many small meals (‘nibbling’) rather than few large ones (‘gorging’) for control of blood glucose, serum lipids and body fat accretion has been known for 60 y, but the mechanisms are poorly understood. Men exhibit more of a gorging eating pattern than women and are also more prone to the metabolic complications of obesity, as are women with a ‘male’, central distribution of adipose tissue. We have shown correlations between central fat distribution, and other components of the metabolic ‘Syndrome X’ and fatty infiltration of the liver. Here we study relationships between eating rate and fat distribution and test the hypothesis that gorging might be associated with fatty liver.

SUBJECTS AND METHODS: In 30 non-alcoholic, non-diabetic, severely obese women (body mass index, BMI=47±1 kg/m2; mean±s.e.m.) with a mean age of 36±1 y and 16 men (BMI: 52±3) age 38±2 y, who were candidates for anti-obesity surgery, we measured eating rate using an eating monitor, and fat distribution by the waist–hip circumference ratio (WHR). In addition in the 17 women and 11 men who had surgery, serum lipids were analyzed and routine liver biopsies were evaluated for steatosis by a pathologist blinded to the conditions of the study.

RESULTS: Men ate significantly faster than women (188±28 vs 123±9 g/min; P<0.01), and had more liver fat (score: 2.7±03 vs 1.5±0.3; P<0.01), with no statistically significant sex differences in s-cholesterol or s-triglycerides. Eating rate correlated with WHR (r=0.46; P<0.01, n=46), liver fat (r=0.55; P<0.01), and s-triglycerides (r=0.42; P<0.05) adjusting for sex. Liver fat correlated with WHR (r=0.50; P<0.05), s-triglycerides (r=0.70; P<0.01) and s-cholesterol (r=0.50; P<0.05), while there were no significant correlations with BMI or body weight. In multivariate analysis eating rate (32%), meal size (8%) and WHR (6%) contributed 46% of the variance in liver fat.

CONCLUSION: We showed increased eating rates in severely obese men and women with central fat distribution. Furthermore, increased eating rates were associated with fatty liver and elevated serum lipids. Eating rate in severely obese women and men may be a determinant of the metabolic syndrome.

Introduction

Associations between body habitus and disease have been known since antiquity and were extended by Vague's observations of relationships between a ‘male’ or central fat distribution and metabolic complications of obesity more than 50 y ago.1 Subsequently, central fat distribution, particularly intra-abdominal, visceral, fat was correlated with a constellation of diseases seen in the obese, referred to as Syndrome X or the metabolic syndrome of obesity.2,3,4 This central fat distribution has also been associated with fatty infiltration of the liver,5,6 often seen in the obese, and liver fat has been implicated in the development of insulin resistance with hyperinsulinemia and increased lipid synthesis.7,8,9

Since the early 1930s, associations between feeding frequency and metabolic abnormalities and disease have been found in laboratory animals and in people.10,11,12 Fabry and Tepperman concluded: ‘an infrequent meal pattern is associated with a tendency toward obesity, hypercholesterolemia, impaired glucose tolerance and also toward ischemic heart disease’,10 thus describing metabolic abnormalities associated with obesity before the notion of a ‘metabolic syndrome of obesity’ was presented.

More recent studies of the metabolic consequences of larger meals demonstrate striking similarities with elements of the metabolic syndrome of obesity, including elevated peaks in serum glucose, insulin, free fatty acids (FFAs) and lipids, enhanced lipogenesis, and decreased glucose tolerance.13,14,15,16 These physiologic effects of ‘gorging’ are remarkably consistent despite the variety of patient groups studied (type II diabetics, dyslipidemics, obese men and women and healthy non-obese men).

In spite of the seemingly obvious cultural stereotypes of gorging, pot-bellied men and nibbling, pear-shaped women, and the knowledge that force-feeding geese produces fatty liver for foie gras,17 no one has formally addressed the possible relationship between eating behavior, fat distribution, liver fat and metabolic abnormalities in obese people. In fact, none of the studies of meal frequency have analyzed the intra-meal rate of ingestion. Indeed, the dictionary definition of ‘gorging’ involves both speed (‘swallow with greediness’) and amount or volume (‘in large quantities’), though scientific papers using the term refer to both the number of meals10,11,14 and the rate of ingestion.12,15

Although eating rate differs between sexes, and between the lean and obese,18 it has not been investigated in relation to body fat distribution or metabolic abnormalities associated with fat distribution. Therefore, we studied eating rate, fat distribution,19 serum lipids and liver fat in severely obese subjects undergoing anti-obesity surgery and, in so doing, demonstrate relationships between eating behavior and metabolism which may contribute to the understanding of the metabolic syndrome of obesity.

Methods

Subjects

Thirty severely obese premenopausal women (body mass index, BMI: 47±1.3 kg/m2; mean±s.e.m.) aged 19–52, and 16 severely obese men (BMI: 52±3) aged 18–53 were studied during evaluation for surgical treatment of severe obesity. The patients were weight stable within 3 kg of their maximum weight on regular diets for at least 3 months. Patients with medical histories of alcoholism, liver disease, hepatotoxic medications or exposures, or diabetes mellitus were excluded from the study. None of the women were taking oral contraceptives. At the time of this study the diagnostic criteria for binge-eating disorder (BED; Spitzer et al20) had not been defined; however, none of the patients described a current history of bulimia nervosa.

Because 18 (13 women and five men) among these 46 studied candidates did not proceed to have an operation, we have liver biopsies in a subset of 17 women and 11 men. Among these latter 28 subjects, serum lipids were only available in 23. Furthermore, among the 30 women undergoing eating tests with a liquid meal, 14 also had tests with a solid meal.

Blood chemistry

Standard overnight fasting laboratory tests of serum electrolytes, protein and albumin and liver function tests were obtained in all patients. Serum triglycerides and cholesterol were analyzed in a random subset of 13 women and 10 men.

Anthropometry

Waist and hip circumference ratio (WHR) was calculated after measurement during mid-expiration, with the patient standing. Waist girth was taken at the inferior costal margin and hip girth at the superior iliac spine.

Eating test

Eating ratios were determined covertly in the laboratory using the universal eating monitor (UEM).21 The UEM consists of a false tabletop suspended on an electronic scale for recording the reduction of weight of a liquid or solid test meal over time, allowing determination of exactly when eating has stopped and calculation of the eating rate.

Prior to the actual test meal, patients underwent pretests for palatability of the test food. The screening procedure was performed to reduce the contribution to eating rate attributable to variation in liking of the test food. Patients were excluded if they rated the test meal less than 5 on a nine-point category scale (1=dislike extremely, 9=like extremely).

Meals.

After an overnight fast, a standard breakfast of muffin and juice was given. Four hours later, using a spoon, the patient consumed a liquid test meal consisting of a flavoured casein shake (50% CHO, 35% fat, 15% protein by energy; caloric density 1 cal/g). A random subset of 14 of the 30 women was also tested in a similar fashion, ie with a standard breakfast followed 4 h later by a solid meal consisting of macaroni and beef (Stouffer's®).

Procedure.

Patients were instructed to eat as much of a test meal as they wanted, for as long as they wanted. The total amount (grams) of test meal consumed from the time the meal was initiated until the subject stopped eating was measured. The eating rate, expressed as g/min, was defined as this amount divided by the number of minutes the meal lasted. Patients eating less than 150 g, as an indication of dissatisfaction with the meal, were excluded. Retest reproducibility of test meals in our laboratory is approximately ±15%.22

Liver biopsy

The subset of 17 women and 11 men who subsequently underwent surgical treatment had routine liver biopsies at the time of surgery. Wedge and/or needle biopsies were performed immediately upon entering the abdomen and specimens were placed in formalin and processed with conventional H&E stains. The hepatologist (FS), blinded to patient data, examined the liver tissue and graded the amount of fat present within hepatocytes on a semi-quantitative scale of 0–4+.5 Furthermore, he made a full hepatopathological assessment of each biopsy, evaluating portal and parenchymal inflammation and fibrosis, as well as cirrhosis and the presence of Mallory bodies, glycogen nuclei, granuloma and ductular cell proliferation.

Informed written consent was obtained from all patients. The protocol was approved by the Institutional Review Board of the institution where the patients were treated.

Statistics

Descriptive statistics, Pearson and Spearman rank correlations and multiple stepwise regression analyses controlled for shared variance were performed using SPSS-X and Statview II. Between-group comparisons were performed using t-tests, accepting a significance level of P<0.05. All values are given as mean±standard error.

Results

Clinical characteristics of the patients are presented in Table 1. The statistically significant difference in absolute weight between sexes did not reflect true differences when using the more appropriate body mass index (BMI) to correct for height. Men had significantly greater WHR and faster eating rates, while there were no statistically significant differences between the sexes in the size of the meal. The 14 women who had solid meals consumed a mean 590±110 g with durations ranging between 36 and 722 s.

Table 1 Characteristics of 30 women and 16 men including eating rate, meal size and WHRa determinations (mean±s.e.m.)

Blood chemistry studies revealed normal levels of electrolytes, protein, albumin and bilirubin in all patients. Slightly increased liver enzyme activities were found in some patients, consistent with severe obesity. Serum triglycerides and cholesterol were in the high normal range.

In the subset of 17 women and 11 men, average age, weight, BMI, WHR and eating rate did not differ significantly from the larger group (data not shown). While no significant differences in mean serum triglycerides and cholesterol were seen between men and women, men had a greater degree of hepatic steatosis (Table 2).

Table 2 Liver fat in 17 women and 11 men undergoing anti-obesity surgery and serum lipids in 13 of the women and 11 of the men (mean±s.e.m.)

Liver histology

Sixteen of the women and 11 of the men had portal inflammation. This inflammation was mild in 11 of the 16 women (69%) and 10 of the 11 men (91%). Mild parenchymal inflammation was just as prevalent in the men (nine of nine), but less so in women with any parenchymal inflammation (seven of nine). Mild portal fibrosis was present in all patients, while none of them exhibited any parenchymal fibrosis. One of the women and one of the men had severe portal inflammation (3+), while none had severe parenchymal inflammation or fibrosis.

Correlations

The correlation between eating rate and WHR in the total population (n=46) was r=0.46 (P<0.01; Figure 1), but no statistically significant correlations between eating rate and BMI or body weight were found. Meal size was positively correlated with eating rate in the 46 subjects (r=0.44; P<0.005) as well as in the subgroup with liver biopsies (r=0.47; P=0.01) with a trend toward a correlation with waist:hip ratio in the larger group (r=0.24; P=0.11). Meal size contributed 8% and WHR 6% of the variance in liver fat after accounting for eating rate (R2=0.32; P=0.002), with no contribution from BMI. Correlations between eating rate and WHR and serum lipids and liver fat are shown in Table 3 and Figures 2 and 3. Among the 14 women who had both liquid and solid meals, the correlation in eating rate was statistically significant (r=0.69; P=0.02).

Figure 1
figure1

Correlation between eating rate and WHR in 30 women and 16 men (r=0.46; P<0.01).

Table 3 Correlation coefficient (r) between eating rate and WHR and liver fat in 17 severely obese women and 11 men and similar correlations with serum triglycerides and cholesterol in 13 women and 10 of the men
Figure 2
figure2

Correlation between eating and liver fat in 17 women and 11 men (r=0.55; P<0.01).

Figure 3
figure3

Correlation between eating rate and serum triglycerides in 13 women and 10 men (r=0.42; P<0.05).

There were no statistically significant associations between hepatic inflammation or fibrosis and eating rate, fat distribution, BMI or body weight.

In multivariate analysis eating rate contributed 32% of the variance in liver fat (R2=0.32; P=0.002), with additional contributions of 8% from meal size (NS) and 6% from WHR (NS) and no contribution from BMI. Thus 46% of the variance in liver fat was predicted from eating rate, meal size and fat distribution. Regression analysis of WHR as the dependent variable in the total population of 46 subjects demonstrated that eating rate (R2=0.25; P<0.000) made the largest contribution to the explained variance, including meal size (2%; NS) and BMI (3%; NS) in the analysis.

Discussion

This study demonstrated relationships between eating rate and components of the metabolic syndrome as well as fatty infiltration of the liver. Numerous studies, some as early as 1934, have shown effects of meal frequency on various metabolic parameters10,11,12,13,14,15,16,23,24 subsequently grouped together in the metabolic Syndrome X,4 but none of them investigated the rate of food consumption under laboratory or natural conditions.

Our finding of increased hepatic steatosis with increased rates of eating is not surprising against the background of increased hepatic lipogenesis during gorging described in rat experiments from 1942 by Tepperman et al25 and the testimonial evidence of farmers in Strasbourg, who have long recognized the importance of the rate of force-feeding geese to obtain foie gras. Though the size of the meal was related to eating rate, meal size only made a minor contribution to the variance in liver fat. Unfortunately, we are unable to conclusively determine whether meal frequency and rate of ingestion are independent of each other. We do not have information on the daily eating patterns of the subjects and are unaware of any published data relating rate of eating to frequency in free-living humans.

More surprising is the finding that a ‘male’ habitus, even in women, is associated with a ‘male’, rapid eating rate which, however, was independent of the degree of obesity (BMI). This agrees with our earlier reports of relationships between fat distribution and fatty liver8,26 independent of body fat or body mass5 and extends those findings to include relationships with serum lipids.

Eating rate has been studied in obese and lean subjects of both sexes with varying results. Thus an ‘obese eating style’ proposed in 196127 has been refuted28 and replicated by others29 and by us18 with no obvious consensus. Methodological differences with regard to measurements and meal choices as well as population differences may explain the controversy. The statistically significant correlation between eating rate of liquids and of solids among the 14 women tested with both meals (r=0.69; P=0.02) implies that the results from liquid meals are truly relevant. Although it may be argued that laboratory eating conditions might not reflect habitual eating habits, we feel that the concordance between these two very different meals supports the notion that our eating test measures an inherent eating style. Further support for this has been presented by Kissileff.30

Recently the binge-eating disorder (BED) has been recognized as a prevalent finding among the obese.31 Unfortunately we cannot conclusively rule out the occurrence of binge-eating disorder in some of the patients, although our history-taking did not disclose any current such practice. As mentioned, no patient described a current history of bulimia.

The mechanism(s) underlying the relationship between eating rate and fatty liver are not known and were not the object of this study. Circumstantial evidence implicates insulin and glycemic responses, known to be elevated in similar severely obese patients7 commonly exhibiting impaired glucose tolerance with hyperinsulinemia progressing to non-insulin dependent diabetes mellitus (NidDM). In one study of geese prone to fatty liver large meals evoked greater glucose and insulin responses than small meals consumed in the same amount of time.32

Based on the present findings and experimental33 and clinical evidence,11,13,15 we propose that enhanced and rapid glucose absorption, mediated by a brisk insulin response via cephalic phase release,34 an incretin effect35,36 and rapid intestinal handling,37,38 causes fatty infiltration of the liver via glucose toxicity.39,40,41 Patients with ‘early NidDM’ have increased rates of gastric emptying according to one study,42 while others have demonstrated correlations between gastric emptying and serum glucose and insulin in normal subjects and patients with NidDM.43 Alone or in conjunction with rapid absorption of lipid,38,44 glucose and insulin increases may lead to insulin resistance9,45 and the metabolic syndrome with central/visceral fat distribution and dyslipidemia. Indeed, in a recent study normalizing glycemia in type II diabetics, plasma glucose was shown to be a prime determinant of hepatic insulin action in the presence of a decrease in serum FFA.41 In order to verify and extend our observations to attempt to determine mechanisms, it will be necessary to study subjects instructed to ‘nibble’ or ‘gorge’ isoenergetic solid meals while measuring gastrointestinal peptide release.

Despite the obvious multi-factorial etiology of the metabolic syndrome, we believe that eating behavior, particularly the rate of eating, should be considered for inclusion as a component of the syndrome. Indeed, modification of eating rate pharmacologically,46 by diet47 or by gastric restrictive surgery may be a feasible treatment of the metabolic syndrome by reducing the rate of glucose absorption and glucose-stimulated insulin release.

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Kral, J., Buckley, M., Kissileff, H. et al. Metabolic correlates of eating behavior in severe obesity. Int J Obes 25, 258–264 (2001). https://doi.org/10.1038/sj.ijo.0801469

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Keywords

  • fatty liver
  • Syndrome X
  • dyslipidemia
  • fat distribution

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