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Journal of Pediatric Gastroenterology & Nutrition:
doi: 10.1097/MPG.0b013e31803815d9
Original Articles: Hepatology & Nutrition

Metabolic and Nutritional Profile of Obese Adolescents With Nonalcoholic Fatty Liver Disease

de Piano, Aline; Prado, Wagner L; Caranti, Danielle A; Siqueira, Kãli O; Stella, Sérgio G; Lofrano, Mara; Tock, Lian; Cristofalo, Dejaldo MJ; Lederman, Henrique; Tufik, Sérgio; de Mello, Marco Túlio; Dâmaso, Ana R

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Author Information

Federal University of São Paulo, Escola Paulista de Medicina UNIFESP-EPM, São Paulo, Brazil

Received 15 May, 2006

Accepted 17 January, 2007

Address correspondence and reprint requests to Nadja Ana R. Dâmaso, Rua Marselhesa no. 535-Vila Clementino, São Paulo/SP 04020-060, Brazil (e-mail: ana.damaso@unifesp.br).

Financial support was received from AFIP, CNPq, CAPES, FAPESP 2006/00684-3, CENESP, FADA, FAPESP (CEPID/Sleep #9814303-3 S.T), UNIFESP, and the CEPE Multidisciplinary Obesity Intervention Program.

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Abstract

Background: The incidence of nonalcoholic fatty liver disease (NAFLD) is increasing due to its prevalence in obesity, diabetes, and insulin-resistance syndrome. The best treatment protocol for NAFLD has not been determined. However, there is evidence that exercise and nutritional intervention can improve and prevent it. The aim of the present study was to evaluate the dietary and metabolic profiles of obese adolescents with NAFLD who participated in a multidisciplinary program.

Patients and Methods: We studied 43 adolescents ages 15 to 19 years (17.18 ± 1.66 years) with a body mass index (BMI) ≥30, consisting of 30 patients without NAFLD (BMI = 35.80 ± 3.44 kg/m2) and 13 with NAFLD (BMI = 33.47 ± 2.34 kg/m2). The NAFLD diagnosis was determined by ultrasonography. Blood samples were collected to analyze glycemia, hepatic aminotransferase levels, and lipid profiles. Insulin resistance was measured by homeostasis model assessment insulin-resistance index (HOMA-IR). The analyses of baseline and postintervention food intake were made by a 3-day inquiry.

Results: At baseline conditions, the patients with NAFLD showed significant differences in body mass, BMI, and visceral and subcutaneous fat. Glucose and visceral and subcutaneous fat presented a significant reduction after treatment in patients with NAFLD. Analyzing the food intake, at baseline we observed a positive correlation between the visceral obesity and lipid consumption only in patients with NAFLD. We also observed significant decrease in energy and cholesterol consumption in patients with NAFLD after the multidisciplinary therapy.

Conclusions: The intervention promoted a decrease in the prevalence of NAFLD, a significant decrease in visceral obesity, and improved HOMA-IR, glycemia, and serum lipid levels that are risk factors for NAFLD. In summary, the multidisciplinary program is essential in the treatment and prevention of NAFLD.

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INTRODUCTION

Obesity is increasing worldwide, especially in adolescents, affecting more than 15% of Brazilian children and adolescents (1–3). Studies have shown the relationship between obesity and several diseases in adult life, such as arterial hypertension, type 2 diabetes mellitus, cancer, and cardiovascular mortality (4–8). Body fat excess, mainly in the form of central obesity, is closely correlated with dyslipidemia, high blood pressure, hyperinsulinemia, and high fasting glucose levels (7,9,10).

The visceral obesity increases plasma free fatty acid (FFA) levels because these adipocytes have higher lipolytic activity. Consequently, the visceral obesity increases the FFA levels in the portal circulation, and insulin resistance can also be responsible for this increase (7,11). A large amount of FFA increases triglycerides serum levels, and may exceed the very low–density lipoprotein (VLDL) synthetic capacity, promoting storage in the liver, known as fatty liver (12).

Nonalcoholic fatty liver disease (NAFLD) is an emerging clinical problem among patients of all ages. NAFLD includes a broad spectrum of liver tissue alterations, ranging from pure steatosis to cirrhosis (13,14) to nonalcoholic steatohepatitis (NASH). NASH is defined by the presence of lobular necroinflammatory activity with or without the presence or perisinusoidal fibrosis that can evolve to cirrhosis and can be detected on liver biopsy (15). Differentiating between the 2 is important because as many as 28% of patients with steatohepatitis, in contrast to those with simple steatosis, may progress to cirrhosis, but the only reliable method of differentiating them is by biopsy, which is costly and carries risks to patients (16). Therefore, ultrasonography (US), a noninvasive method to diagnose NAFLD in an ambulatory care setting, is common (17–21).

Considering the grading for steatosis, a variation from grades I to III was observed (grade I, <33%; grade II, 33%–66%, and grade III, >66% of hepatocytes are affected) (20). NAFLD affects 10% to 39% of the world population, 50% of diabetic patients, 57% to 74% of obese people, and as many as 90% of morbidly obese people (13,14). The prevalence in obese adolescents is between 22.5% and 52.8% (20,22–24).

The treatment of NAFLD is based on the associated factors of the disease and consists of gradual body mass reduction, glycemia, and lipid control (ie, cholesterol and triglycerides). The main goal is not only to treat the fatty liver disease but also obesity, diabetes, and hyperlipidemia (25–28). Although there is no accepted treatment that can reverse fatty liver disease, all patients should be given a low-fat diet and triglyceride-lowering agents. They should also be encouraged to exercise regularly (6).

Because of the scarcity of studies related to the influence of diet on NAFLD, the purpose of this study was to assess the short-term (12 weeks) effect of a multidisciplinary program on the dietary and metabolic profiles of obese adolescents with NAFLD.

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PATIENTS AND METHODS

Population

A total of 43 postpuberes obese adolescents (19 boys and 24 girls) were recruited. Their ages ranged from 15 to 19 years, and their BMI was 34.22 ± 2.93 kg/m2. The inclusion criteria were pubertal stage as assessed by means described by Tanner et al (29) and severe primary obesity (body mass index [BMI] >30), and agreement by the adolescents and their families to participate in a 12-week multidisciplinary weight loss program. The exclusion criteria were identified as genetic, metabolic, or endocrine disease; chronic alcohol consumption; previous drug use; and other causes of liver steatosis. The subjects volunteered in response to statements on radio and television and in local newspapers.

This study was carried out in accordance with the principles of the Declaration of Helsinki and was formally approved by the ethical committee of the Federal University of São Paulo Paulista Medicine School (#0135/04). Informed consent was obtained from all subjects and/or their parents. All subjects underwent electrocardiography.

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Study Protocol

During the first visit, subjects were medically screened, had their pubertal stage assessed, and had their anthropometrics profile measured (height, weight, BMI, and body composition). During the second visit a blood sample was collected and analyzed for various variables. At the third visit US was performed. The patients were divided into 2 groups: NAFLD (n = 13) and non-NAFLD (n = 30). For each subject, the procedures were scheduled for the same time of day and at least 15 hours after the last training session to remove any influence of diurnal variations. Thereafter, obese adolescents started the multidisciplinary weight loss program, as described in the subsequent sections.

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Anthropometric Measurements and Body Composition

Subjects were weighed wearing light clothing and no shoes on a Filizola scale to the nearest 0.1 kg. Height was measured to the nearest 0.5 cm by using a wall-mounted stadiometer (Sanny, model ES 2030). BMI was calculated as body weight divided by height squared. Body composition was estimated by plethysmography in the BOD POD body composition system (version 1.69; Life Measurement Instruments, Concord, CA) (30).

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Serum Analysis

Blood samples were collected in the outpatient clinic at approximately 8:00 AM after an overnight fast. Insulin resistance was assessed by homeostasis model assessment insulin-resistance index (HOMA-IR). HOMA-IR was calculated by the fasting blood glucose (FBG) and the immunoreactive insulin (I): [FBG (mg/dL) × I (mU/L)]/405. Total cholesterol, high-density lipoprotein (HDL), triacylglycerol, and hepatic alanine aminotransferase were analyzed using a commercial kit (CELM, Barueri, Brazil). The HOMA-IR, lipid serum level, and aminotransferase data were analyzed according to reference values described by Schwimmer et al (31).

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Hepatic Steatosis and Visceral and Subcutaneous Adiposity Measurements

All abdominal US procedures and measurements of visceral and subcutaneous fat tissue and fatty liver before and after intervention were performed in a double-blinded fashion by the same physician specializing in image diagnostic using a 3.5-MHz multifrequency transducer (broadband). This procedure permits a reduction of risk margin for misclassification. The intraexamination coefficient of variation for US was 0.8%.

The US measurements of intraabdominal (ie, visceral) and subcutaneous fat were taken. US-determined subcutaneous fat was defined as the distance between the skin and external face of the rectus abdominis muscle, and visceral fat was defined as the distance between the internal face of the same muscle and the anterior wall of the aorta. Cutoff points to define visceral obesity by US parameters were based on previous methodological descriptions by Ribeiro-Filho et al (32).

The US definition of fatty liver was based on previously reported diagnostic criteria and detected liver steatosis was classified as grade I (liver attenuation slightly less than spleen), grade II (more pronounced difference between liver and spleen and intrahepatic vessels not seen or slightly higher attenuation than liver), or grade III (markedly reduced liver attenuation with sharp contrast between liver and intrahepatic vessels) (19,22). In the present study the group with NAFLD presented with some liver steatosis diagnosed by US, and all of the patients presented with normal alanine aminotransferase levels, which was diagnosed as simple steatosis.

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Medical Program

To accomplish their health and clinical parameters, the patients visited the endocrinologist once per month.

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Dietary Program

Energy intake was set at the levels recommended by the dietary reference intake for subjects with low levels of physical activity of the same age and sex (33). However, no fixed level of energy intake was prescribed; they were encouraged only to reduce their food intake and follow a balanced diet. No drugs and antioxidants were recommended.

Once each week, adolescents attended dietetics classes that included information on the food pyramid, recording energy units intake, weight loss, dieting, diet versus “light,” fat and cholesterol, and nutrition facts.

At the beginning and end of the 12-week program, a 3-day dietary record was made by all of the adolescents with the help of their parents because most obese people underreport their food consumption (34). The degree of underreporting may be substantial; however, this is a valid method of evaluating nutrition consumption (35). Portions were measured in terms of familiar volume and size and by reference to an atlas of local food portions. The dietitian taught the parents and adolescents how to record food consumption. These dietary data were transferred to a computer by the same dietitian, and nutrient composition was analyzed by a software program developed at the Federal University of São Paulo Paulista Medicine School (Nutwin software for Windows, version 1.5, 2002) based on Western and local food tables. In addition, the parents were encouraged by a dietitian to call if they needed extra information.

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Exercise Program

During the 12-week multidisciplinary intervention period, adolescents followed a personalized aerobic training program including 60-minute sessions 3 times per week (180 minutes/week) under the supervision of a sports therapist. Each program was developed according to the results of an initial oxygen uptake test for aerobic exercises (cycle ergometer and treadmill). The intensity was set at a workload corresponding to ventilatory threshold 1 (50%–70% of oxygen uptake test). At the end of 6 weeks, aerobic tests were performed to assess physical capacities and to adjust physical training intensity individually (data not shown). During the aerobic sessions, adolescents underwent heart rate monitoring. The exercise program was based on the American College of Sports Medicine position statement of 2001 (36). Information about lifestyle changes related to activity was also provided and spontaneous physical activity (eg, walking, stair climbing) was encouraged but not measured.

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Psychological Intervention

A diagnosis was established by validated questionnaires considering some psychological problems caused by obesity that have been described in the literature, such as depression, disturbances of body image, anxiety, and decrease of self-esteem. During the multidisciplinary intervention, the adolescents attended weekly psychological orientation group sessions in which they discussed body image and alimentary disorders such as bulimia and anorexia nervosa; binge eating; their signals, symptoms, and consequences for health; relation between feelings and food; familiar problems such as alcoholism; and other topics. An individual psychological therapy was recommended when we found nutritional and behavioral problems.

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Statistical Analysis

All data were analyzed by means of Statistica version 6 for Windows with significance set at P < 0.05. All of the data are expressed as mean ± SD unless otherwise stated.

Comparisons between measures at baseline and after the weight loss program were made using paired t tests, between groups by independent t tests, and Pearson correlation.

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RESULTS

The present study comprised 43 obese adolescents divided into 30 patients without NAFLD and 13 with NAFLD. The prevalence of NAFLD was 30.23% in this population, but only 18.6% at the end of the multidisciplinary program (Fig. 1).

Fig. 1
Fig. 1
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Complete data after the intervention were available for 34 subjects (24 without NAFLD and 10 with NAFLD) because 9 patients dropped out of the program. Indeed, the dietary data were available for only 23 subjects (18 without NAFLD and 5 with NAFLD) because 11 of them did not fill out the 3-day inquiry.

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Anthropometrics, Body Fat, Glucose, Insulin, HOMA-IR, Lipid Serum Levels, and Waist

Comparing the 2 groups at baseline conditions, the patients with NAFLD had higher values in all categories. However, only body mass, BMI, and visceral and subcutaneous fat showed significant differences. Glucose and visceral and subcutaneous fat presented a significant reduction after treatment in patients with NAFLD. In the same way, body mass, BMI, glucose, subcutaneous fat, HOMA-IR, cholesterol, and triglycerides decreased significantly in patients without NAFLD (Table 1).

Table 1
Table 1
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Food Intake

At baseline conditions, no significant differences in all nutrient values were observed between the groups with and without NAFLD. However, carbohydrate, protein, and cholesterol consumption were higher in patients with NAFLD. We observed a significant decrease in energy and cholesterol consumption in patients with NAFLD after the multidisciplinary therapy (Table 2).

Table 2
Table 2
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No significant difference was observed in lipid consumption between the 2 groups at baseline conditions, but we did observe a positive correlation only between visceral obesity and lipid consumption of patients with NAFLD (Fig. 2).

Fig. 2
Fig. 2
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DISCUSSION

Obesity is strictly related to the development of NAFLD. Several recent reviews showed that the reduction of weight and changes in lifestyle could promote an improvement in fatty liver, and data from the present study corroborated the results of these studies. We also analyzed a possible relationship between dietary composition and the development of this disease. Hence, the multidisciplinary program to treat obese adolescents is highly important (25–27). These studies did not show a correlation between visceral obesity and lipid ingestion, however.

In the present study 30.23% of obese adolescents had a diagnosis NAFLD, which is similar to values observed by other authors. After the 12-week intervention, there was a 18.6% reduction in the prevalence of NAFLD (Fig. 1). A limitation of the present study was the lack of histological data, which would better describe the actual effect of the intervention on the prevalence and grade of NAFLD. However, there is increasing interest in US-diagnosed NAFLD in the ambulatory care setting (17–21).

NAFLD is strongly associated with features of metabolic syndrome, including insulin resistance, impaired glucose tolerance, and dyslipidemia (37–42). It has also been proposed that visceral obesity may be a major contributor to fatty liver in the insulin-resistant state. As such, evaluation of these metabolic parameters is essential in obese adolescents. When we compared the 2 groups at baseline conditions, we observed a significant difference in body fat composition. The patients with NAFLD showed higher values for body mass, BMI, and visceral and subcutaneous fat; however, our study was effective in promoting a significant reduction in visceral and subcutaneous fat in patients with NAFLD. The reduction in visceral obesity in patients with NAFLD is important because several studies suggest that the adipose tissue may be a major source of massive free fatty acid flow to the liver. Indeed, visceral obesity is more influential than body mass in predicting fatty liver (20,39,43). Subjects with more pronounced visceral obesity appear to be at greater risk for fatty liver because of their ability to transport free fatty acids directly into the portal vein for conversion to triglycerides within the liver (19,44–46).

Insulin resistance causes alterations in the uptake, degradation, and/or secretion of lipid molecules, which leads to the accumulation of lipids in the hepatocytes. Studies have observed that patients with NAFLD had insulin resistance (14,28,46–48). Glycemia presented a significant reduction in both groups after the intervention, but the values were normal at the beginning of the present study. We observed altered values of insulin in 38.46% in the group with NAFLD and 26.6% in the group without NAFLD. Analyzing the insulin resistance by HOMA-IR, we noticed a higher prevalence in the NAFLD group (92.3%) compared with the group without NAFLD (76.7%). It is also generally believed that NAFLD is a metabolic disorder and that insulin resistance plays a key role in its genesis. Insulin resistance, along with other potential biochemical abnormalities, results in fatty liver and the generation of excessive free radicals in the liver, which produce liver injury (49).

Cholesterol and triglycerides showed a significant decrease after the intervention in patients without NAFLD. Indeed, we observed decreases in total cholesterol (13.9%), LDL (9.58%), HOMA-IR (11.7%), and waist circumference (2.24%), as well as increased HDL (1.2%) in patients with NAFLD. Conversely, at the beginning of treatment, the serum lipid level measurements presented normal values in both groups except the total cholesterol of patients with NAFLD.

There is evidence that the diet composition can influence the development and improvement of NAFLD. Studies suggest that a hypocaloric diet that promotes a reduction of 5% to 10% of body mass decreases lipid intake, and increased antioxidants can contribute to the treatment of NAFLD (37,50–54).

In Table 1, patients with NAFLD were heavier at baseline (102.76 kg) than patients without NAFLD (92.32 kg). Conversely, the group with NAFLD consumed fewer energy units (1620.74 kcal/d) than the group without NAFLD (1866.6 kcal/d). A possible explanation is that elevated levels of leptin are found in the majority of patients with NAFLD (55). It may contribute to leptin resistance and low ghrelin concentrations, suggesting a decrease in energy expenditure and food intake. In fact, previous research by our group reinforces this hypothesis (56).

Although no significant differences in food intake were observed between the 2 groups, in patients with NAFLD there was a reduction in lipid consumption from 23.55% to 20.67% and a significant reduction in total energy intake (from 1620.74 kcal ± 399.12 to 1328.38 kcal ± 422.44) and cholesterol (from 253.54 ± 86.07 to 195.12 ± 94.13). This result can be partially explained because the adolescents decreased portion sizes mainly in foods that are sources of lipids. Consequently, the nutritional intervention contributed to improve lipid ingestion in patients with NAFLD, which plays an important role in the development of this disease. However, other investigations pointed out that the subjectivity of food-recording techniques may be a source of error. A number of investigators think that underrecording of self-reported food intake often occurs, and that participation in a weight management study leads to subconscious underestimation and/or underreporting of total daily energy intake (57).

One of the most important findings of our study is that despite the lipid consumption at baseline conditions, there was no significant difference between the patients with and without NAFLD, and a positive correlation (0.61) between lipid consumption and visceral obesity was observed only in patients with NAFLD (Fig. 2). Although the r value was not extremely strong, it represents an important positive correlation that has not been discussed in the literature to our knowledge and requires further investigation with better patient samples.

The key observation in this clinical study is that the patients with NAFLD accumulated more visceral fat and presented more altered insulinemia and higher HOMA-IR values than patients without NAFLD (Table 1). Under these conditions there is a disproportionately greater flow of free fatty acids from visceral adipose stores, which are transported to the liver by portal blood and affect hepatic lipid and glucose metabolism and insulin sensitivity, causing insulin resistance (9,10,25,58,59). These mechanisms contribute to the development of NAFLD. It provides a unifying mechanism that links the coordinated regulation of glucose and lipid metabolism in the liver by hormonal regulation of lipolysis in visceral adipose stores (49). This way, reduction in the HOMA-IR, visceral obesity, and lipid ingestion is essential to prevent and treat fatty liver disease.

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CONCLUSIONS

The multidisciplinary intervention promoted a decrease in the prevalence of NAFLD, a significant decrease in the visceral obesity, and improved HOMA-IR, glycemia, and lipid serum levels that are risk factors for NAFLD. The patients with NAFLD presented higher anthropometrics, visceral and subcutaneous fat, HOMA-IR, total cholesterol, LDL and waist values at baseline conditions. After the intervention all of the values, except HOMA-IR, were normalized in both groups. No significant differences were observed in the food intake between the 2 groups, however the lipid consumption of patients with NAFLD was correlated with visceral obesity. In summary, the multidisciplinary program, including the nutritional intervention, is essential in the treatment and prevention of NAFLD.

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Acknowledgment

The authors thank the patients and their parents for their participation in this study.

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Are saturated fatty acids and insulin resistance associated with fatty liver in obese children?
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Back to Top | Article Outline
Keywords:

Food intake; Nutrition; Visceral adipose tissue

© 2007 Lippincott Williams & Wilkins, Inc.

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