Journal List > Clin Nutr Res > v.4(4) > 1059807

An, Jun, and Lee: Development and Application of Low-Carbohydrates and Low-Simple Sugar Nutrition Education Materials for Non-Alcoholic Fatty Liver Disease Patients

Abstract

We developed nutrition education materials for non-alcoholic fatty liver disease (NAFLD) patients focusing on low-carbohydrate and low-simple sugar diet and assessed subjective difficulty and compliance for the developed materials. The materials were developed in 2 types, a booklet for face-to-face education and a handout for phone education. The booklet covered 4 topic areas of fatty liver, low-carbohydrate and low-simple sugar diet, weight control, and meal plan. The handout material included several eating behavior tips. To assess practical usability of nutrition education using the developed materials, subjective compliance and difficulty levels were examined in a sample for NAFLD patients. A total of 106 patients recruited from 5 general hospitals were randomly assigned to a low-carbohydrate and low-simple sugar weight control diet group or a general weight control diet group. Each participant received a 6-week nutrition education program consisting of a face-to-face education session and two sessions of phone education. The developed materials were used for the low-carbohydrate and low-simple sugar weight control diet group and general weight control information materials were used for the control group. Subjective difficulty and compliance levels were evaluated three times during the education period. Subjective difficulty level was significantly higher in the low-carbohydrate and low-simple sugar diet group compared to the control group at the end of the second week, but such a discrepancy disappeared afterward. No significant difference was found for subjective compliance between the groups at each time. In conclusion, the developed nutrition education materials for low-carbohydrate and low-simple sugar diet are reasonably applicable to general Korean NAFLD patients.

Introduction

Non-alcoholic fatty liver disease (NAFLD) is a disease that the fat sticks within the liver, though a patient doesn't excessively drinks alcohol [1]. NAFLD is closely related to abdominal obesity and insulin resistance syndrome [2]. As the prevalence of insulin resistance syndrome and obesity increases, NAFLD tends to increase globally [345]. According to the report of Korea Food and Drug Administration in 2012, prevalence of NAFLD in Korean adults is rapidly increasing with 11.5% in 2004 and 27.3% in 2010.
According to the two hits hypothesis, NAFLD development is explained as the inflammatory response from oxidative stress and lipid peroxidation and the lipid accumulation in the liver due to insulin resistance [67]. It has been reported that people in Asian countries show higher NAFLD prevalence at similar body mass index level compared to people in Western countries, and it is attributable that NAFLD development is related to genetic factors as well as eating habits [8910].
So far weight-loss is most emphasized method among NAFLD treatments. Fat adherence degree in the liver showed favorable results when the patient lost weight [1112]. To decrease fat accumulated in the liver 3-5% of weight loss is required, and over 10% of weight loss and gradual weight loss over 6 months is recommended to attenuate inflammation in the liver [1314]. The fact that ingestion of high-fat diet causes fat accumulation within the liver tissue has been observed [15] and saturated fat intake in NAFLD patients raised insulin resistance and oxidative stress in the serum [16].
One point that should be paid attention with regard to dietary factors of NAFLD is carbohydrate and simple sugar consumption. Intake of food with high carbohydrate content stimulates insulin secretion. Also, increase of insulin influences generation of fatty liver by inducing fat synthesis in the liver [17]. Kang et al. [18] investigated inflammation degree of liver tissue according to macronutrient energy intake rate among patients with both fatty liver disease and insulin resistance syndrome and observed more severe inflammation degree among those with higher energy intake ratio from carbohydrate. In addition significantly positive correlation was reported between abnormal aminotransferase activation and insulin resistance syndrome for those with carbohydrate energy intake rate over 70% while no meaningful relation was found among those with high fat intake [19].
Effect of low-carbohydrate diet has been reported by several previous studies. When NAFLD patients have low-carbohydrate diet, alanine aminotransferase (ALT) and fat accumulation in liver decreased [20]. Haufe et al. [21] who conducted a random clinical trial comparing low-carbohydrate diet and low-fat diet reported that fat amount in liver decreased in both groups. On the contrary, patients with over 54% of energy intake from carbohydrate showed 6.5 times higher incidence of fatty liver inflammation compared to patients with below 35%. Interestingly, those with high fat intake displayed a lower level of inflammation in liver [22]. Furthermore several studies showed that low-carbohydrate diet was more effective than low-fat diet in managing obesity and insulin resistance syndrome [232425].
Simple sugar, particularly fructose, appeares to have close relation with the incidence of NAFLD. Excessive fructose intake may cut off fatty acid oxidation process by rapidly generating citrate in liver and increasing malony-CoA. As a result increased free fatty acid in liver is accumulated as triglyceride [26]. Bergheim et al. [27] reported that fructose caused liver inflammation by increasing the number of intestinal virus and toxin inflow through hepatic portal vein. Along with the increase of beverage consumption including high fructose corn syrup, incidence of NAFLD and liver tissue fibrilization of NAFLD patients also increased [2829].
According to 2011 Korean National Health and Nutrition Examination Surveys, average carbohydrate intake was as high as about 322 g/day [30]. Average energy intake proportions from carbohydrate and fat were 65.8% and 19.6%, respectively. Compared to Americans' diet, Koreans' energy intake from carbohydrate is markedly higher while energy intake from fat is lower [31]. Therefore weight loss approach applying reduction in carbohydrate intake can be effective for NAFLD treatment in Koreans. Clear NAFLD medicine has not been developed so far. Recently genetic factors such as patatin-like phospholipase domain-containing protein 3 (PNPLA3) were reported to have close relation with fat adhesion in liver, but genetic treatment development is insufficient. Accordingly, weight loss by modifying diet is recommended as the best method for managing and treating NAFLD [32]. It is important for NAFLD patients to continuously manage diet by themselves in daily life, because patients are mostly outpatients rather than inpatients. Positive effects of nutrition education on patients' self-efficacy has already been reported through several domestic studies [333435]. While there have been several studies regarding that nutrition education is effective in treatment of certain diseases [363738], research on concrete development of nutrition education material for NAFLD patients has been scarce. Recently Korean Association for the Study of the Liver presented 'clinical practice guidelines for non-alcoholic fatty liver disease'. The guidelines recommended low-carbohydrate and low simple-sugar diet education along with overall energy intake reduction to NAFLD patients [39]. Therefore this research aimed to develop nutrition education materials for NAFLD patients focusing on low-carbohydrate and low-simple sugar diet and examine practical applicability of the developed materials.

Materials and Methods

Development of educational material

The overall purpose of this educational material is 'desirable diet of NAFLD', targeting male and female adults in the age of 20-60 year-old. We aimed at developing materials for low-carbohydrate and low simple-sugar diet that is effective in weight control and can minimize triglyceride adhesion to liver [3940]. This research intended to develop a material optimized for the individual interview education and the telephone education, currently utilized mainly by many hospitals as the educational method for outpatients. Education materials were developed in two forms: a booklet form with relatively much content for individual interview education [41] and a handout form for telephone education to follow-up outpatients who are difficult to frequently visit a hospital. Overall process of educational material development is displayed in Figure 1.
The materials were designed to cover a total of 5 major themes and 3-4 sub-themes for each major theme (Table 1). The major themes included understanding of fatty liver disease, understanding of low-carbohydrates and low-simple sugar diet, importance of weight control, meal plan, and tips for eating behaviors. The booklet for face-to-face education included all the major themes except for the 'tips for eating behaviors' to help acknowledge basic relation between NAFLD and diet and crucial dietary modification issues. The handout for phone-mediated education was designed to cover the major theme of 'tips for eating behaviors'.

Application of educational materials

Subjects

To assess practical usability of nutrition education using the developed materials, subjective compliance and difficulty levels were examined in a sample of NAFLD patients. A total 106 patients recruited from 5 general hospitals in Seoul, Chuncheon, and Cheonan were randomly assigned to a low-carbohydrate and low-simple sugar weight control diet group or a general weight control diet group. The inclusion criteria included NAFLD diagnosis by abdominal ultrasonic waves or computed tomography (CT) scan within recent 3 months, ages between 20-60 year-old, ALT or AST over 40 U/L before treatment, and usual alcohol consumption lower than 140 g/week for males and 70 g/week for females, no use of special dietary or physical activity regimen and insulin therapy, and body mass index less than 35 kg/m2. The study was conducted between April and October, 2012. Overall process of the research was approved by the institutional review board (HYUH IRB 2012-C-09 of Hanyang University Hospital).

Data collection

Each participant received a 6-week nutrition education program consisting of a face-to-face education session and two phone education sessions (Figure 2). The developed materials were used for the low-carbohydrate and low-simple sugar weight control diet group and general weight control information materials were used for the control group. Before the first education session, data on age, weight, height waist circumference, and blood pressure were collected. Waist circumference was measured around the navel with a tape measure and blood pressure was measured with the blood pressure gauge after 5 minutes rest. Subjective difficulty and compliance levels were evaluated three times (2nd week, 4th week, and 6th week of nutrition education) during the education period. Both subjective levels of difficulty (1: very easy, 6: very difficult) and compliance (1: not comply at all, 6: comply very much) were evaluated using 6-point Likertscale.

Statistical analysis

All statistical analysis was conducted utilizing SAS 9.2 version (statistical analysis system, SAS Institute, Cary, NC, USA). Data were described with means and standard deviations. Comparisons between low-carbohydrate and low simple-sugar diet education group and general weight control education group were analyzed with student t-test. Significance level of all statistical verification was 0.05.

Results

Development of booklet for face-to-face education

A booklet was developed in a total 9 pages of B5 size paper excluding the front and the rear cover, and titled as 'Fatty liver, how can we eat?' The font sizes of 20, 15, and 12 were used for the title, sub-title, and text, respectively (Figure 3).

1) 'Let us learn about the fatty liver'

The first two pages of the booklet briefly explain definition and seriousness of fatty liver, the relation between diet and fatty liver, and issues on misunderstanding and curiosity of fatty liver. Simple sugar and starch are emphasized as risk factors of fatty liver, besides fat, using visual images.

2) 'What is a low-carbohydrate and low-simple sugar diet?'

Page 3 presents effects of low-carbohydrate and low-simple sugar diet in relation to fatty liver disease. It introduces the concept of low-carbohydrate and low-simple sugar diet, high carbohydrate food items, the mechanism through which carbohydrate, particularly fructose, can easily accumulate in the body, and multiple advantages of low-carbohydrate and low-simple sugar diet.

3) 'Importance of weight control'

Page 4 begins with the reason why normal weight maintenance is important for NAFLD patients [11]. Information on how to calculate body mass index, how to assess obesity using body mass index, and how to estimate his/her own energy intake required for achieving healthy body weight subsequently follows.

4) 'Meal plan'

Page 5 and 6 suggest practical information that can be referred to plan balanced diet for required calorie intake. A portion size for each of major food items across 6 food groups was introduced with the corresponding food figure, and recommended daily food group consumption patterns based on low-carbohydrate and low-simple sugar diet were presented across calorie intakes from 1,200 kcal/day to 1,800 kcal/day.
Page 7 presents an example of daily menu plan of low-carbohydrate and low-simple sugar diet. The menu plan for a day was suggested as two types, a 'traditional Korean diet' and a 'convenient & dining-out diet' to reflect various dietary characteristics.

5) 'Behavior guides for healthy liver'

Page 8 suggests 5 eating behavior guidelines to reduce carbohydrate and simple sugar intake. The suggested guidelines are as follows: ① Change your rice bowl into a small one; ② Take out a third of rice when eating out; ③ Avoid white foods such as white rice, white flour, and white table sugar; ④ Drink mineral water, black coffee, and tea instead of carbonated drink, fruit juice and coffee with sugar or syrup; ⑤ Avoid sweet foods such as chocolate, candies, and cookies.

Development of a handout for phone-mediated education

Phone-mediated education material was developed in a 4-page handout of A4 size (Figure 4). This material focuses on practical information directly applicable when selecting food items in daily life. The 'Seoul Namsan' font was used with 28 font size for title, 20 for sub-title, 12-14 for text, and 18 for emphasized text.
Page 1 shows foods that should be avoided, their substitution foods, and fruit items with relatively high simple sugar amount [43]. Page 2 explains how to read a nutrition label and a food ingredient list to cautiously select low-simple sugar food products. Also selection of natural foods rather than processed foods was emphazied [44]. The next page focuses on popular beverages high in simple sugar content, and the last page presents a total of 5 salad dressing recipes low in simple sugar.

Application of the developed educational materials

Subjects

A total of 106 subjects who participated in preliminary application of nutrition education using the developed materials were randomly assigned to either a general weight control diet group (N=54) or a low-carbohydrate and low-simple sugar diet group (N=52) (Table 2). No significant differences in age, weight, body mass index, waist circumference, blood pressure, and fasting blood glucose were observed between two groups, reflecting the random assignment was performed well.

Subjective level of difficulty and compliance

Figure 5 displays subjective levels of difficulty and compliance at the 2nd, 4th, and 6th week. Subjective difficulty level was significantly higher in the low-carbohydrate and low-simple sugar diet group compared to the general weight control group at the 2nd week (3.98±0.91 vs. 3.62±0.72, p=0.035), but such a discrepancy disappeared afterward. No significant difference was found for subjective compliance between the groups at each time.

Discussion

This research developed nutrition education material for low-carbohydrate and low-simple sugar diet targeting NAFLD patients and evaluated the applicability by assessing subjective difficulty and compliance levels during the 6-week education period. One of the distinct characteristics of the developed materials is that they are based on low-carbohydrate and low-simple sugar diet which is apart from traditional Korean macronutrient composition. Fifty percent of calorie intake from carbohydrate was selected as a main purpose based on the recent domestic literatures [394045] and clear distinctness from general weight control diet. With regard to simple sugar intake, fruit intake once or twice a day was recommended to minimize consumption of added simple sugar. Another characteristic of the developed materials is that they were designed to be administered in an individual nutrition education setting. Specifically, the materials was designed to apply for compliance of daily energy requirement and daily food group consumption pattern for each recipient's own condition. Individually customized nutrition education was more effective in reducing fat intake and increasing fruit and vegetable intake compared to general nutrition education [4647]. The subjective difficulty level was higher in the low-carbohydrate and low-simple sugar diet group compared to the general weight control diet group after the first education session. This may be due to relatively less familiarity of the low-carbohydrate and low-simple sugar diet as a dietary regimen for NAFLD. While correlation between high fat intake and fatty liver is commonly recognized and widely known, the low-carbohydrate and low-simple sugar diet is not familiar to public. However, as the education continued, the degree of subjective difficulty showed no difference from the general weight control diet group. This implies that the low-carbohydrate and low-simple sugar education can be applied to Korean adults who usually take carbohydrate-based diet if education is given with proper intensity, method, and materials.
Both groups showed relatively high subjective compliance levels, with no difference between the groups. Such a finding implies an important meaning in respect that compliance to macronutrient modification diet is a strong predictable factor of weight control success [48]. A recent study reported that hyperglycemic diabetes female patients experienced improper blood glucose control when following low-fat diet [49]. Also a study comparing low-fat diet and low-carbohydrate diet found that insulin resistant participants showed lower compliance to low-fat diet compared to highly insulin sensitive participants. On the contrary, no significant difference in compliance degree for low-carbohydrate diet was observed between insulin resistant and insulin sensitive participants [50]. These findings can be interpreted that the patients with insulin resistance showed low compliance to low-fat diet due to their lower satiety level in case of low-fat diet. However, we observed reasonably high compliance degree in both groups despite subjects' fasting glucose level beyond the healthy range. This difference may came from, at least partly, a large gap in fat content of diet.

Conclusion

This research developed educational materials focusing on low-carbohydrate and low simple-sugar diet and practical dietary method for Korean NAFLD patients. Findings from the application process of the developed materials and the patients' responses suggest that the developed nutrition education materials for low-carbohydrate and low-simple sugar diet are reasonably applicable to general Korean NAFLD patients. Further research to examine clinical effects of nutrition education for NAFLD patients using the developed materials is necessary.

Figures and Tables

Figure 1

Flow chart of nutrition education material development.

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Figure 2

Application process of nutrition education materials.

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Figure 3

Booklet for face-to-face nutrition education.

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Figure 4

Handouts for telephone-mediated nutrition education.

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Figure 5

Comparison of subjective difficulty and compliance between the low-carbohydrate and low-simple sugar diet and the general weight control diet group. *p < 0.05.

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Table 1

Composition of nutrition education materials

cnr-4-250-i001
Major theme Sub-theme Type
Understanding of fatty liver disease Basic knowledge of fatty liver disease Booklet for face-to-face education
Relation between fatty liver disease and eating behaviors
Risk of fatty liver disease
Understanding of low-carbohydrates and low-simple sugar diet Definition of low-carbohydrates and low-simple sugar diet
Adequate energy intake
Carbohydrate intake and body fat accumulation
Importance of weight control Effects of weight loss to liver function
Calculation of body mass index
Estimation of individualized daily energy need
Meal plan Food serving size chart
Recommended food group intake pattern
Examples of daily meal plan
Tips for eating behaviors Healthy choice for low-simple sugar diet Handout for phone- mediated education
How to read nutrition facts label
Simple sugar amount in some snacks, beverages and fruits
Recipes for dressings low in simple sugar
Table 2

Basic characteristics of subjects

cnr-4-250-i002
General weight control diet
(n = 54)
Low-carbohydrate & low-simple sugar diet
(n = 52)
t-value
Age, year 42.4 ± 13.0* 43.6 ± 11.8 -0.51
Weight, kg 76.6 ± 15.2 78.1 ± 17.3 -0.46
BMI, kg/m2 27.0 ± 3.9 27.3 ± 4.3 -0.32
Waist, cm 91.9 ± 10.9 93.1 ± 12.1 -0.52
Systolic blood pressure, mmHg 126.7 ± 14.8 126.1 ± 13.5 0.21
Diastolic blood pressure, mmHg 77.2 ± 11.2 76.6 ± 9.8 0.28
Fasting blood glucose, mg/dL 102.8 ± 21.2 103.8 ± 17.2 -0.26

*Mean ± SD.

By student t-test.

Ackowledgment

This research was supported by grants from Ministry of Food and Drug Safety (12161KFDA159).

Notes

Conflict of interest The authors have declared no conflict of interest.

References

1. Becker U, Deis A, Sørensen TI, Grønbaek M, Borch-Johnsen K, Müller CF, Schnohr P, Jensen G. Prediction of risk of liver disease by alcohol intake, sex, and age: a prospective population study. Hepatology. 1996; 23:1025–1029.
crossref
2. Clark JM. The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol. 2006; 40:Suppl 1. S5–S10.
3. Ministry of Health and Welfare, Korea Centers for Disease Control and Prevention. Metabolic syndrome prevalence among Korean adults aged 30 years and older: based on 2007-2010 Korean National Health and Nutrition Examination Survey. Cheongwon: Korea Centers for Disease Control and Prevention;2012.
4. Jeong EH, Jun DW, Cho YK, Choe YG, Ryu S, Lee SM, Jang EC. Regional prevalence of non-alcoholic fatty liver disease in Seoul and Gyeonggi-do, Korea. Clin Mol Hepatol. 2013; 19:266–272.
crossref
5. Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S. Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology. 2005; 42:44–52.
crossref
6. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology. 1998; 114:842–845.
crossref
7. Lewis JR, Mohanty SR. Nonalcoholic fatty liver disease: a review and update. Dig Dis Sci. 2010; 55:560–578.
crossref
8. Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis. 2010; 28:155–161.
crossref
9. Petersen KF, Dufour S, Feng J, Befroy D, Dziura J, Dalla Man C, Cobelli C, Shulman GI. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci U S A. 2006; 103:18273–18277.
crossref
10. Deurenberg P, Deurenberg-Yap M, Guricci S. Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev. 2002; 3:141–146.
crossref
11. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes. 2005; 54:603–608.
crossref
12. Huang MA, Greenson JK, Chao C, Anderson L, Peterman D, Jacobson J, Emick D, Lok AS, Conjeevaram HS. One-year intense nutritional counseling results in histological improvement in patients with non-alcoholic steatohepatitis: a pilot study. Am J Gastroenterol. 2005; 100:1072–1081.
crossref
13. Sanyal AJ. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology. 2002; 123:1705–1725.
crossref
14. Andersen T, Gluud C, Franzmann MB, Christoffersen P. Hepatic effects of dietary weight loss in morbidly obese subjects. J Hepatol. 1991; 12:224–229.
crossref
15. Westerbacka J, Lammi K, Häkkinen AM, Rissanen A, Salminen I, Aro A, Yki-Järvinen H. Dietary fat content modifies liver fat in overweight nondiabetic subjects. J Clin Endocrinol Metab. 2005; 90:2804–2809.
crossref
16. Machado MV, Ravasco P, Jesus L, Marques-Vidal P, Oliveira CR, Proença T, Baldeiras I, Camilo ME, Cortez-Pinto H. Blood oxidative stress markers in non-alcoholic steatohepatitis and how it correlates with diet. Scand J Gastroenterol. 2008; 43:95–102.
crossref
17. Schwarz JM, Neese RA, Turner S, Dare D, Hellerstein MK. Short-term alterations in carbohydrate energy intake in humans. Striking effects on hepatic glucose production, de novo lipogenesis, lipolysis, and wholebody fuel selection. J Clin Invest. 1995; 96:2735–2743.
crossref
18. Kang H, Greenson JK, Omo JT, Chao C, Peterman D, Anderson L, Foess-Wood L, Sherbondy MA, Conjeevaram HS. Metabolic syndrome is associated with greater histologic severity, higher carbohydrate, and lower fat diet in patients with NAFLD. Am J Gastroenterol. 2006; 101:2247–2253.
crossref
19. Kwon OW, Jun DW, Lee SM, Lee KN, Lee HL, Lee OY, Yoon BC, Choi HS. Carbohydrate but not fat is associated with elevated aminotransferases. Aliment Pharmacol Ther. 2012; 35:1064–1072.
crossref
20. Benjaminov O, Beglaibter N, Gindy L, Spivak H, Singer P, Wienberg M, Stark A, Rubin M. The effect of a low-carbohydrate diet on the nonalcoholic fatty liver in morbidly obese patients before bariatric surgery. Surg Endosc. 2007; 21:1423–1427.
crossref
21. Haufe S, Engeli S, Kast P, Böhnke J, Utz W, Haas V, Hermsdorf M, Mahler A, Wiesner S, Birkenfeld AL, Sell H, Otto C, Mehling H, Luft FC, Eckel J, Schulz-Menger J, Boschmann M, Jordan J. Randomized comparison of reduced fat and reduced carbohydrate hypocaloric diets on intrahepatic fat in overweight and obese human subjects. Hepatology. 2011; 53:1504–1514.
crossref
22. Solga S, Alkhuraishe AR, Clark JM, Torbenson M, Greenwald A, Diehl AM, Magnuson T. Dietary composition and nonalcoholic fatty liver disease. Dig Dis Sci. 2004; 49:1578–1583.
crossref
23. Samaha FF, Iqbal N, Seshadri P, Chicano KL, Daily DA, McGrory J, Williams T, Williams M, Gracely EJ, Stern L. A low-carbohydrate as compared with a low-fat diet in severe obesity. N Engl J Med. 2003; 348:2074–2081.
crossref
24. Ebbeling CB, Leidig MM, Feldman HA, Lovesky MM, Ludwig DS. Effects of a low-glycemic load vs low-fat diet in obese young adults: a randomized trial. JAMA. 2007; 297:2092–2102.
crossref
25. Hession M, Rolland C, Kulkarni U, Wise A, Broom J. Systematic review of randomized controlled trials of low-carbohydrate vs low-fat/low-calorie diets in the management of obesity and its comorbidities. Obes Rev. 2009; 10:36–50.
crossref
26. Lim JS, Mietus-Snyder M, Valente A, Schwarz JM, Lustig RH. The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol. 2010; 7:251–264.
crossref
27. Bergheim I, Weber S, Vos M, Krämer S, Volynets V, Kaserouni S, McClain CJ, Bischoff SC. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol. 2008; 48:983–992.
crossref
28. Abid A, Taha O, Nseir W, Farah R, Grosovski M, Assy N. Soft drink consumption is associated with fatty liver disease independent of metabolic syndrome. J Hepatol. 2009; 51:918–924.
crossref
29. Abdelmalek MF, Suzuki A, Guy C, Unalp-Arida A, Colvin R, Johnson RJ, Diehl AM. Nonalcoholic Steatohepatitis Clinical Research Network. Increased fructose consumption is associated with fibrosis severity in patients with nonalcoholic fatty liver disease. Hepatology. 2010; 51:1961–1971.
crossref
30. Ministry of Health and Welfare, Korea Centers for Disease Control and Prevention. Korea Health Statistics 2012: Korea National Health and Nutrition Examination Survey (KNHANES V-3). Cheongwon: Korea Centers for Disease Control and Prevention;2013.
31. Wright JD, Wang CY. Trends in intake of energy and macronutrients in adults from 1999-2000 through 2007-2008: NCHS data brief no. 49. Hyattsville (MD): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics;2010.
32. Rotman Y, Koh C, Zmuda JM, Kleiner DE, Liang TJ. NASH CRN. The association of genetic variability in patatin-like phospholipase domaincontaining protein 3 (PNPLA3) with histological severity of nonalcoholic fatty liver disease. Hepatology. 2010; 52:894–903.
crossref
33. Lee HJ. Effect of individual health education the medical clinic of public health centers on knowledge, self-efficacy, and self-care behavior in clients with hypertension [master's thesis]. Seoul: Yonsei University;2003.
34. Choi JC. An analysis of effects of intervention methods for community-based prevention of cardiovascular diseases [Ph.D. thesis]. Gimhae: Inje University;2005.
35. Ju K, So H. Effects of the nutrition education program on self-efficacy, diet behavior pattern and cardiovascular risk factors for the patients with cardiovascular disease. J Korean Acad Nurs. 2008; 38:64–73.
crossref
36. Hong SM, Kim HJ. A study of calcium status and effect of nutrition education of prevention osteoporosis in middle-aged women. J Korean Diet Assoc. 2001; 7:159–166.
37. Kim TY, Um SH. Older adults with type 2 diabetes improve glycemic control after nutritional education program at the public health center. J Korean Diet Assoc. 2004; 10:205–217.
38. Kim S, Sohn C, Chung WY. Effects of medical nutrition therapy on food habits and serum lipid levels of hypercholesterolemic patients. J Korean Diet Assoc. 2005; 11:125–132.
39. Korean Association for the Study of the Liver. Clinical practice guidelines for non-alcoholic fatty liver disease. Seoul: Korean Association for the Study of the Liver;2013.
40. Joo DR. Dietary therapy for non-alcoholic fatty liver disease and obesity. Clin Mol Hepatol. 2008; 14:s61–s72.
41. Lee YM. Practical use of media for nutrition education. Korean J Nutr. 2000; 33:923–939.
42. The Korean Nutrition Society. Dietary reference intakes for Koreans. 1st rev. Seoul: The Korean Nutrition Society;2010.
43. United States Department of Agriculture, Agricultural Research Service. National nutrient database for standard reference, release 26 [Internet]. 2012. cited 2012 April 1. Available from http://ndb.nal.usda.gov/ndb/search/list.
44. Ministry of Food and Drug Safety (KR). Reduction of simple sugar content [Internet]. 2010. cited 2012 April 1. Available from http://www.mfds.go.kr/nutrition/index.do?nMenuCode=29.
45. Jun DW. Practice guideline for the diagnosis and management of nonalcoholic fatty liver disease. Korean J Gastroenterol. 2012; 60:64–66.
crossref
46. Contento I, Balch GI, Bronner YL, Lytle LA, Maloney SK, Olson CM, Swadener SS. The effectiveness of nutrition education and implications for nutrition education policy, programs, and research: a review of research. J Nutr Educ. 1995; 27:277–418.
47. Eyles HC, Mhurchu CN. Does tailoring make a difference? A systematic review of the long-term effectiveness of tailored nutrition education for adults. Nutr Rev. 2009; 67:464–480.
crossref
48. Alhassan S, Kim S, Bersamin A, King AC, Gardner CD. Dietary adherence and weight loss success among overweight women: results from the A to Z weight loss study. Int J Obes (Lond). 2008; 32:985–991.
crossref
49. Shikany JM, Margolis KL, Pettinger M, Jackson RD, Limacher MC, Liu S, Phillips LS, Tinker LF. Effects of a low-fat dietary intervention on glucose, insulin, and insulin resistance in the Women's Health Initiative (WHI) dietary modification trial. Am J Clin Nutr. 2011; 94:75–85.
crossref
50. McClain AD, Otten JJ, Hekler EB, Gardner CD. Adherence to a low-fat vs. low-carbohydrate diet differs by insulin resistance status. Diabetes Obes Metab. 2013; 15:87–90.
crossref
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Seung Min Lee
https://orcid.org/http://orcid.org/0000-0003-3046-8010

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