Variations in the Efficacy of Resistant Maltodextrin on Body Fat

Dec 9, 2013 - Department of Food Science and Biotechnology, National Chung Hsing University ... KEYWORDS: Resistant maltodextrin, body fat, high-fat d...
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Variations in the Efficacy of Resistant Maltodextrin on Body Fat Reduction in Rats Fed Different High-Fat Models Hui-Fang Chu,†,∥ Min-Hsiung Pan,§ Chi-Tang Ho,‡ Yu-Han Tseng,† William Wei-Li Wang,† and Chi-Fai Chau*,†,⊥ †

Department of Food Science and Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan Department of Food Science, Rutgers University, New Brunswick, New Jersey 08901, United States § Institute of Food Science and Technology, National Taiwan University, Taipei, 10617, Taiwan ∥ Standard Chem. Pharm. Co., Ltd., 154 Kaiyuan Road, Sinying City, Tainan County 73055, Taiwan ⊥ Agricultural Biotechnology Center, National Chung Hsing University, 250 Kuo-Kuang Road, Taichung 40227, Taiwan ‡

ABSTRACT: Many studies have utilized a variety of methods to induce obesity in rodents, but they often received inconsistent results. The present study intended to use resistant maltodextrin (RMD) as a means to investigate the variations in its efficacy on body fat accumulation under the influence of four high-fat (HF) models of 23% or 40% total fat, comprising soybean oil, lard, and/or condensed milk. Results indicated that integrating condensed milk into the diets could help increase diet intake, boost energy intake, increase weight gain, and enhance fat formation. Supplementation of RMD (2.07 g/kg) notably reduced total body fat levels in three HF models, with the exception of a condensed-milk-added 40%-fat diet that may have misrepresented the functions of RMD. The uses of the 23% HF diets, with and without milk, and the milk-free 40% HF diet were therefore recommended as suitable models for antiobesity evaluations of RMD, or other fiber-rich products. KEYWORDS: Resistant maltodextrin, body fat, high-fat diet

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INTRODUCTION Obesity is a medical condition that facilitates the development of metabolic disorders including diabetes, hypertension, and cardiovascular disease.1 In recent decades, many studies, including human trials and animal tests, have been widely performed to investigate the relationship between dietary lipid absorption and body fat accumulation, in hopes of finding ways to reduce lipid absorption and body weight.2−4 To study the mechanisms involved in body fat reduction, obese rodent models are commonly used. A variety of methods have been developed to induce obesity in rodents. For example, obesity could be induced by feeding them fat-enriched, highsugar, or high-calorie diets. Among these diet choices, a high-fat (HF) diet was commonly used to induce obesity in rodents. A wide range of fat contents, ranging from 10% to 63% (w/w), have been used in different studies, with fat contents around 23% and 40% being the two most frequently used models.5 Dietary lipid types also varied between animal-derived fats (e.g., lard or beef tallow) and plant oils (e.g., corn or safflower oil) in previous studies. In some studies, a portion of condensed milk or fructose was also added into the HF diets to help induce obesity.6,7 However, different combinations of fat contents and fat types have been found to induce diversified increases in body fat, ranging from 38% to 169%.8,9 In the past few decades, the potential inhibitory effects of many food ingredients on lipid absorption and its accumulation in body have been investigated, but the results have not always been consistent.8−12 For instance, though green tea (at 1−3 mg/kg per day) has commonly been reported to have body-fatreducing effects, contradicting results were observed between rats fed a 15%-fat HF diet and those fed a 30%-fat HF diet.12,13 © 2013 American Chemical Society

It was therefore speculated from these studies that different HF feeding models could lead to different outcomes to the assessments of the same ingredient. New ingredients possessing potential for body fat-reducing effect have been reported in recent years. Resistant maltodextrin (RMD), as one of the candidates, is a type of colorless and tasteless water-soluble fiber, composed of shortchain glucose polymers that are resistant to digestion in the human digestive system. Studies have reported that RMD could delay absorption of carbohydrates, reduce dietary lipid absorption and serum triglyceride level, and suppress elevation of postprandial blood glucose.14−17 Its high stability against temperature variations and acidic conditions has driven RMD to become a popular water-soluble fiber component in many nutritional supplements. The present study intends to use RMD as a means to demonstrate and compare the various possible influences of different HF diet compositions on body fat accumulation in rats. In particular, the variations in the efficacy of RMD in different HF dietary models will be accurately evaluated and discussed. Relationships between different HF diets and food intake, body weight, visceral fat, or total body fat will also be addressed. Received: Revised: Accepted: Published: 192

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Table 1. Compositions of the Normal Chow Diet and the Experimental High-Fat Diets 23% fat high fat diet (with condensed milk)a

23% fat high fat dieta ingredient (g/100 g diet) chow oil lard condensed milkc casein supplementation of RMD (g/kg bw)d carbohydrate fat protein

23-C

23-1xF

23-2xF

81 4 15

81 4 15

81 4 15

1.03 39 23 19

39 23 19

23M-C

23M-1xF

52 5 13 30

23M-2xF

52 5 13 30

2.07

52 5 13 30

1.03

39 23 19

42 23 14

40% fat high fat dieta 40-C 63 10 27

2.07

42 23 14

42 23 14

40-1xF

40-2xF

63 10 27

63 10 27

1.03 31 40 14

31 40 14

40% fat high fat diet (with condensed milk)a 40M-C

40M-1xF

40M-2xF

(ND)

29 12 24 30 5

29 12 24 30 5 1.03

29 12 24 30 5 2.07

100

30 40 14

30 40 14

30 40 14

2.07 31 40 14

normal chow dietb

49 5 23

a

High-fat basal diet groups (23-C, 23M-C, 40-C, and 40M-C) were used as controls for their corresponding RMD-supplemented groups including low doses (23-1xF, 23M-1xF, 40-1xF, and 40M-1xF, respectively) and high doses (23-2xF, 23M-2xF, 40-2xF, and 40M-2xF, respectively). bChow (PMI Nutrition International, St. Louis, MO) contained crude protein (23.0 g/100 g), crude lipid (4.5 g/100 g), and carbohydrate (72.5 g/100 g). c Condensed milk contained crude protein (7.3 g/100 g), crude lipid (8.2 g/100 g), and carbohydrate (84.5 g/100 g). dThe energies of 23-C, 23M-C, 40-C, and 40M-C diets were 443.2, 432.4, 544.7, and 517.1 kcal/100 g, respectively, while that of ND diet was 336 kcal/100 g.

Table 2. Effects of Different High Fat Diets on Food Intake, Energy Intake, Fat Intake, Body Weight Gain, and Feed Efficiency in Ratsa 23% fat high fat diet food intakeb (g) energy intake (kcal) fat intakeb (g) body weight gainb (g) feed efficiencyb

23% fat high fat diet (with condensed milk)

40% fat high fat diet

40% fat high fat diet (with condensed milk)

normal chow diet

23-C

23-1xF

23-2xF

23M-C

23M-1xF

23M-2xF

40-C

40-1xF

40-2xF

40M-C

40M-1xF

40M-2xF

(ND)

1272m 5632m

1258 5575

1268 5619

1428n 6168n

1427 6164

1401 6051

1042o 5677m

1040 5667

1030 5615

1339p 6925o

1232 6372

1253 6478

1509n 5071p

292m 277mn

289 267

292 259

328n 299n

328 296

322 277

417o 260m

416 260

412 253

536p 299n

493 278

501 280

76q 196o

21.7m

21.1

20.4

20.9m

20.9

19.8

25.0n

25.0

24.5

22.4n

22.5

22.3

13.0o

Values with different letters (m−q) among the five diets (23-C, 23M-C, 40-C, 40M-C, and ND) are significantly different (Duncan, p < 0.05). b Data are expressed as mean (n = 8). a

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area calculation as recommended by the U.S. FDA.18 The actual amounts of RMD supplement for the rats were constantly recalculated every three days to adjust for changes in body weights throughout the test period. Animals were allowed free access to food and water during the experimental period. Food intake and body weights were recorded daily. At the end of the experimental period, animals were anesthetized by carbon dioxide after fasting for 12 h. After blood samples were drawn from the orbital sinus, the anesthetized rats were sacrificed by exsanguination. The visceral fat pads were immediately excised, blot dried, and weighed. The coats were shaved and the remaining carcasses were then weighed and stored at −20 °C until analysis. The institutional guidelines for the care and use of laboratory animals were carefully followed. This study protocol was approved by the Institutional Animal Care and Use Committee of National Chung Hsing University. Feed Efficiency. Feed efficiency was determined after 8 weeks on the experiment diets for each rat using the following formula:

MATERIALS AND METHODS

Experimental Diets and Design. One hundred and four male Sprague−Dawley rats (6 weeks old) weighing 137 ± 5 g were purchased from the National Laboratory Animal Center (Taipei, Taiwan). The animals were individually housed in stainless steel screen-bottomed cages and placed in a room maintained at 22 ± 2 °C with a 12-h light/dark cycle. After a two-week acclimation period, the rats were divided into eight weight classes of thirteen animals each. The rats in each weight class were randomly assigned to one of the thirteen diet groups, including one normal chow diet (ND), and twelve HF diet experimental groups. The compositions of the ND diet and twelve high-fat experimental diets are shown in Table 1. All HF diets contained either 23% or 40% (w/w) total fat contents. The HF diet groups included soybean oil and lard, with or without condensed milk. Specifically, the twelve high-fat diets were designed for 4 distinct HF-diet arrangements (namely, 23, 23M, 40, and 40M), each with its own experimental control (-C) group, low-dose treatment (-1xF) group, and high-dose treatment (-2xF) group. In more detail, the twelve HF-diet groups comprised three groups (23-C, 23-1xF, and 23-2xF) receiving 23%-fat diets without condensed milk, three groups (23M-C, 23M-1xF, and 23M2xF) receiving 23%-fat diets with condensed milk, three groups (40-C, 40-1xF, and 40-2xF) receiving 40%-fat diets without condensed milk, and three groups (40M-C, 40M-1xF, and 40M-2xF) receiving 40%-fat diets with condensed milk. Animals in all -1xF groups received a single dose of RMD (1.03 g/kg body weight) each day, and each animal in the -2xF groups was given a double dose of RMD (2.07 g/kg body weight) every day. The doses of RMD (at 1.03 and 2.07 g/kg) are approximately equivalent to 10 and 20 g/day, respectively, for a 60-kg human. These dose equivalents are in accordance with body surface

Feed efficiency = body weight gained (g)/food intake(g) × 100 Measurement of Total Visceral Fat. Total visceral fat was defined as the sum of the mesenteric, epididymal, and perirenal fat depots.19 All fat along the mesentery starting at the lesser curvature of the stomach and ending at the sigmoid colon was considered mesenteric fat. At sacrifice, the mesenteric, epididymal, and perirenal fat depots were dissected from the rats and weighed before freezing.

Visceral fat% = total visceral fat (g)/final body weight (g) × 100 Measurement of Crude Carcass Fat. For the present study, the carcass was defined as the entire shaved rat torso minus the visceral fat 193

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Figure 1. Effects of different diet models on visceral fat mass in control groups. (A) Epididymal fat of normal diet (ND) group; (B) peri-renal fat of normal diet (ND) group; (C) epididymal fat of nonmilk 23%-fat control (23-C) group; (D) peri-renal fat of nonmilk 23%-fat control (23-C) group; (E) epididymal fat of milk-containing 23%-fat control (23M-C) group; (F) peri-renal fat of milk-containing 23%-fat control (23M-C) group; (G) epididymal fat of nonmilk 40%-fat control (40-C) group; (H) peri-renal fat of nonmilk 40%-fat control (40-C) group; (I) epididymal fat of milkcontaining 40%-fat control (40M-C) group; (J) peri-renal fat of milk-containing 40%-fat control (40M-C) group. pads removed during sacrifice. Following the method of Janis et al. with slight modifications, rat carcasses were dried at 80 °C for 4 h, followed by drying at 105 °C for another 24 h.20 Dried carcasses were weighed and ground individually without deboning. Furthermore, fat extractions were performed on all shaved coats and the carcasses. Following the AOAC method with slight modifications, carcass fats were extracted from the dried carcass powder by ether (1:20, w/v), and total crude carcass fats were quantified gravimetrically after evaporating the solvents in the lipid extracts.21

condensed milk-feeding groups were higher than those (5575− 5677 kcal) of the other milk-free HF groups. In terms of the body weight changes during the experimental period, all four HF control groups gained significantly (p < 0.05) more weight (133−153%) than the ND group due to higher fat intake in these HF groups. Similarly, the feed efficiencies of the four HF control diets (20.9−25.0) were significantly (p < 0.05) higher than that of ND diet (13.0) (Table 2). The results revealed that fat intake and feed efficiency were positively correlated. It seemed that the fat component was a major factor affecting the feed efficiency while both condensed milk and RMD supplementation only led to some slight but consistent decreases in feed efficiencies. The apparent differences in visceral fat sizes are visually presented in Figure 1. The organs were removed before the measurement of fat mass. The ND control group was shown to have the lowest fat mass in the epididymal and peri-renal area (Figure 1A and B), while all four HF diet control groups had greater fat mass than ND, with the milk-containing 40%-fat diet (40M-C) control group showing the greatest fat mass in the same visceral area (Figure 1I and J). More specifically, Table 3 shows that the visceral accumulations of fat in four HF control groups were all markedly (p < 0.05) higher (1.6- to 2.4-fold)

Carcass fat% = crude carcass fat (g)/final body weight (g) × 100 Determination of Body Fat Percentage. Total body fat was defined as the sum of total visceral fat and crude carcass fat. Body fat percentage of each rat was therefore calculated using the following formula:

Body fat (%) = (visceral fat (g) + crude carcass fat (g)) /final body weight(g) × 100 Statistical Analysis. All experiments were performed on groups of eight animals. Data are presented as means ± standard deviation. Numerical data were analyzed with SPSS 19.0 statistics software (Chicago, IL, USA). The significance level was set to p < 0.05 (Duncan).

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RESULTS The food intakes, energy intakes, fat intakes, body weight gains, and feed efficiencies of the animals fed the different diets are shown in Table 2. After the acclimation period, there were no differences in the initial body weights (249−280 g) among the thirteen dietary groups. Throughout eight weeks of observation, all animals remained healthy and active. All animals on the four HF control diets (i.e., 23-C, 23M-C, 40-C, and 40M-C) consumed lesser amounts of feed (−5 to −31%) cumulatively than the ND group (1509 g). Feed consumptions for the 40%fat groups (40-C and 40M-C) were lower than those of the 23%-fat groups (23-C and 23M-C, respectively). Owing to the higher energy density in the 40%-fat diets (Table 1), the actual fat and energy intakes in the 40%-fat groups were significantly higher, demonstrating that the actual energy intake could be a collective consequence of the consumption level and energy density. Furthermore, it was also noted that the incorporation of condensed milk into the HF diets might help increase food intakes. Total energy intakes (6051−6925 kcal) for all six

Table 3. Effects of the Administration of RMD on Visceral Fat Percentagea high-fat controlsb treatment 23% fat 23% fat (with condensed milk) 40% fat 40% fat (with condensed milk)

RMD treatment groupsc

(without RMD)

low dose (1.03 g/kg bw)

high dose (2.07 g/kg bw)

9.9 ± 1.0nx 13.5 ± 1.3ox

9.5 ± 0.7xy 12.4 ± 1.0x

8.6 ± 1.0y 10.5 ± 0.7y

13.0 ± 1.2ox 15.5 ± 1.7px

12.6 ± 1.5x 15.5 ± 0.9x

10.9 ± 1.5y 15.3 ± 1.0x

Data are expressed as mean ± standard derivation (n = 8). bThe visceral fat percentage of the ND group (6.4 ± 1.4%) was significantly (p < 0.05) lower than that of all high-fat controls. Values with different letters (n−p) in the high-fat control column are significantly different (Duncan, p < 0.05). cValues in the same row with different letters (x− y) are significantly different (Duncan, p < 0.05). a

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accumulations in all four HF control groups were significantly (p < 0.05) higher (1.67- to 2.0-fold) than that of the ND group (3.3%). Among the four HF controls, the 40%-fat diet with condensed milk was again the most effective model in accumulating fat (6.6%). In the other three models (i.e., 23C, 23M-C, and 40-C), different amounts of fat consumption (292−417 g) and total energy intakes (5635−6359 kcal) (Table 2) merely led to comparable levels of carcass fat accumulation (5.5% to 5.8%). Nonetheless, administration of RMD at 2.07 g/kg was again able to significantly reduce (p < 0.05) the carcass fat (−16% to 28% against the controls) in different HF models, except the 40M model. It was interesting to note that RMD was similarly more effective in reducing the carcass fat in diets without condensed milk. These results reaffirmed that the ability of RMD in reducing fat accumulation was basically affected by dietary compositions such as fat content and condensed milk. Lastly, the present study also compared total body fat in the animals as a sum of total visceral fat and crude carcass fat. As shown in Figure 2, the total body fat accumulations in all four HF control groups were significantly (p < 0.05) higher (1.3- to 2.3-fold) than that of the ND group (9.7%), with a visceral-tocarcass fat ratio of approximately 2:1. Higher levels of body fat (p < 0.05) were observed for groups with higher dietary fat consumption as well as with condensed milk. Specifically, the effectiveness of the four HF controls in inducing the accumulations of total body fat was ranked as follows: 40MC (22.1%) > 23M-C (19.0%) ≥ 40-C (18.8%) > 23-C (15.7%), demonstrating that HF diets with condensed milk could produce greater amounts of body fat than HF diets alone, regardless of fat content. In contrast, the ability of RMD in reducing body fat accumulation declined in the reverse order,

than that of the ND group (6.4%). The visceral fats of 40%-fat HF controls (40-C and 40M-C) were significantly (p < 0.05) higher than those of the 23%-fat controls (23-C and 23M-C, respectively). The incorporation of condensed milk in both the 23%- and 40%-fat diets led to significant (p < 0.05) increases in visceral fat (1.36- and 1.19-fold, respectively) against their corresponding milk-free diets. Furthermore, our results revealed that the administration of RMD at a high dose (2.07 g/kg) could result in significant (p < 0.05) reductions in the levels of visceral fat (−13% to −22% against the controls) among different HF models excluding the 40M model. Moreover, the effects of RMD administration on crude carcass fat (nonvisceral fat) accumulation are demonstrated in Table 4. Similar to the findings in the visceral fat, the carcass fat Table 4. Effects of the Administration of RMD on Crude Carcass Fat Percentagea high fat controlsb treatment 23% fat 23% fat (with condensed milk) 40% fat 40% fat (with condensed milk)

RMD groupsc

(without RMD)

low dose (1.03 g/kg bw)

high dose (2.07 g/kg bw)

5.8 ± 0.4nx 5.5 ± 0.5nx

5.5 ± 0.6x 5.2 ± 0.5x

4.2 ± 0.5y 4.6 ± 0.5y

5.8 ± 0.5nx 6.6 ± 0.9ox

5.6 ± 0.5x 6.3 ± 0.3x

4.7 ± 0.4y 6.5 ± 0.8x

Data are expressed as mean ± standard derivation (n = 8). bThe carcass fat percentage of the ND group (3.3 ± 0.8%) was significantly (p < 0.05) lower than that of all high-fat controls. Values with different letters (n−o) in the high-fat control column are significantly different (Duncan, p < 0.05). cValues in the same row with different letters (x− y) are significantly different (Duncan, p < 0.05). a

Figure 2. Effects of different diet groups on total body fat percentage. Bars with different letters (m−r) are significantly different (Duncan, p < 0.05). 195

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and misrepresented in a 40%-fat diet model when used with condensed milk. Thus, it should be noted that the 40M diet model might be a nutrient-wise extreme diet, with micronutrient contents close to the minimum limit of daily requirement, for inducing obesity, and thus it should not be considered as an appropriate model for the above-mentioned evaluation of RMD at the present dosages. In sum, it was concluded from our results that the composition of HF models could affect the consistency of the evaluations of a sample’s efficacy for comparison purposes. Both 23%-fat models (with and without condensed milk) and the 40%-fat diet without condensed milk can be considered as suitable experimental models for body fat reduction assessment trials of RMD or other fiber-rich products. However, since the recommended daily total fat intake for adults (ages 19 and older) is between 20 and 35% of dietary calories according to the USDA,26 having 40% fat in an experimental diet (equivalent to about 67% of dietary calories) is in fact considered extremely high for attempting to mimic the actual dietary patterns of the general population. Thus, when shorter periods of obesityinduction or greater levels of body fat formation were desired, the inclusion of condensed milk in HF diets (around 23% dietary fat) could be considered over milk-free HF diets.

with the 40M diets showing the least body fat reduction after the RMD supplementation.

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DISCUSSION From many in vivo studies on the abilities of various ingredients to affect accumulation of body fat, a multitude of high-fat diets with fat levels between 10 and 63% have been used. Total fat contents of 23% and 40% were chosen for this study based on the prevalence of common fat levels used in previous studies.5 Condensed milk has also been incorporated into two of the experimental models as an extra palatable component, since such a supplementation was practiced in some high-fat studies, for the purposes of boosting dietary intake and levels of obesity.5,22 In addition, after comparing the nutrient profiles of the experimental diets to the estimated nutrient requirements, casein was incorporated into the 40 M diet to compensate for the protein content for the maintenance of the rats. After feeding the rats for eight weeks, the findings in our study agreed with the observations that both the dietary fat level and uses of condensed milk played important roles in total body fat accumulation.6,14 The consumption of condensed milk was actually found to be associated with higher body fat levels (Table 3), though the 23%-fat (with condensed milk) and 40%fat groups were found to have similar amounts of visceral fat. Such a connection between palatable dietary component and visceral fat formation has previously been reported in some other studies.22,23 Therefore, it was inferred that the addition of condensed milk (84.5% carbohydrate) would induce obesity more effectively in rats through improving feed and energy intake, and the combination of condensed milk and high levels of dietary fat might have a concrete effect on boosting the visceral fat accumulation of a 23%-fat diet to a level comparable to that of a milk-free 40%-fat diet. Kishimoto et al. has suggested that resistant maltodextrin could potentially suppress lipid absorption and promote lipid excretion by inhibiting the decomposition of micelles and the release of fatty acids from micelles in the lipid absorption process.15 Similarly, our results demonstrated that long-term consumption of RMD at 2.07 g/kg under various high-fat models (excluding the 40% fat diet with condensed milk) could be promising in reducing the body fat effectively (p < 0.05) (Figure 2). The works from other authors have also proclaimed the efficacy of resistant maltodextrin on body fat accumulation. In 2004, Okuma and Kishimoto asserted that persistent RMD consumption could significantly decrease body fat ratio and body fat area in obese objects.17 Later in 2007, Gordon has reported that providing 30 g of RMD to overweight hyperlipidemia patients in addition to their daily regular diet could significantly reduce body fat ratio and the area of visceral and subcutaneous fats, though total weight did not significantly decline, in three months.24 More recently, Hashizume et al. also recorded that providing metabolic syndrome patients with 27 g of RMD for 12 weeks in addition to their normal diet could significantly decrease waist circumference and visceral fat area.25 The consistency of these studies reinforced our observations on the efficacy of RMD on body fat reduction. Nonetheless, our results also suggested that the promotional effects of condensed milk plus high fat (i.e., 40 M groups) might have been too effective in inducing body fat accumulation, which then resulted in the diminishment of the fat-reduction capability of the high dose RMD supplement. In other words, the functions of RMD might be underestimated

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AUTHOR INFORMATION

Corresponding Author

*Phone: (886)-4-22852420. Fax: (886)-4-22876211. E-mail: [email protected]. Mail: Department of Food Science and Biotechnology, National Chung Hsing University, 250 Kuokuang Road, Taichung 40227, Taiwan. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We appreciate Sina Vakili for his technical support. This work is supported in part by the Ministry of Education, Taiwan, ROC, under the ATU plan.

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ABBREVIATIONS USED HF, high fat; RMD, resistant maltodextrin; ND, normal chow diet

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REFERENCES

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dx.doi.org/10.1021/jf404809v | J. Agric. Food Chem. 2014, 62, 192−197