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Available online: http://journal.ipb.ac.id/index.php/jgizipangan J. Gizi Pangan, July 2018, 13(2):79-86 Accredited based on DGHE, Republic of No.12/M/Kp/II/2015 DOI: 10.25182/jgp.2018.13.2.79-86 ISSN 1978-1059 EISSN 2407-0920

Potential of Bioactive Components in Tempe for the Treatment of Obesity Made Astawan1*, Yunita Siti Mardhiyyah1, Christofora Hanny Wijaya1 1Department of Food Science and Technology, Faculty of Agricultural Engineering and Technology, Bogor Agricultural University, Bogor 16680

ABSTRACT

Obesity has become a global health issue and is one of the factors that trigger degenerative diseases. The correct food consumption management could be a solution for treating obesity. is a food that is rich in bioactive components and has antiobesity properties through various mechanisms. In Indonesia, nearly 60% of the are consumed in the form of tempe. The process of fermenting soybeans into tempe causes a bioconversion of nutrients and bioactive components, improving the active physiological abilities. The bioactive components that play a role in the treatment of obesity are , , and peptides. These bioactive components help in reducing body weight, lowering the body ratio and improve lipid profile. Thus, optimation and popularization of tempe as a functional food in the daily menu supported with correct tempe processing could be a solution in treating obesity.

Keywords: isoflavones, obesity, , soybean, tempe

INTRODUCTION which have active physiological properties in treating obesity (Bhathena & Velasquez 2002; Obesity has become a worldwide health is- Velasquez & Bhathena 2007). In Indonesia, near- sue and is believed to be one of the factors that ly 60% of soybeans are consumed in the form trigger degenerative diseases and metabolic prob- of tempe with an average tempe consumption lems such as diabetes mellitus (DM), coronary of 10.1 kg per person per year (Astawan et al. heart diseases (CHD), dyslipidemia, hyperten- 2017). The process of fermenting soybeans into sion, and arthritis (Yuliana et al. 2011; Velasquez tempe can also improve its nutritional value and & Bhathena 2007). WHO (2014) highlighted that benefits for health (Nout & Kries 2005; Astawan 65% of the world population is overweight and 2008). obese and has a higher mortality risk than mal- Many studies pertaining to the use of soy- nourished people. Based on the WHO standard, and soybean products in the treatment of a BMI greater than 25 kg/m2 is categorized as obesity have been conducted, however not many overweight, and a BMI greater than 30 kg/m2 is discuss the possibilities of utilizing tempe which categorized as obese. is a fermented soybean product as a component Aside from the lack of physical activities, in treating obesity. Against this backdrop, the re- poor food consumption pattern such as excessive view will discuss the possibilities of using tempe consumption of foods rich in fat and as a soybean-derived functional food in the treat- is considered as a main cause of obesity (WHO ment of obesity. 2011). Therefore, strategies in treating obesity in- clude reduction of the amount of energy absorbed 1. The Bioactive components of soybeans and by the body, using appetite suppressants, inhibit- tempe ing nutrient absorption, increasing metabolism, The main ingredient of tempe is soybeans and lipid modulation (inhibiting the differentia- (Glycine max), therefore bioactive components tion and proliferation of adipocytes, and reducing of soybeans (Table 1) would most likely be found lipogenesis and increasing lipolysis) (Yun 2010). in tempe, or might even be more “activated” due Complications due to obesity and other to the process. Tempe is made from degenerative diseases have encouraged the con- soybean through a number of steps, namely soak- sumption of low-energy, low-fat, high-fiber, and ing, boiling, removing the cotyledon husk, add- -rich foods (Bhathena & Velasquez ing (the mold Rhizopus spp.), and ferment- 2002). Soybeans have been reported to contain ing at 30-37°C for 36-48 hours (Nout & Kries such quality, it has various bioactive components 2005). Fermentation changes various compo-

*Corresponding Author: tel: +62251-8626725; email: [email protected]

J. Gizi Pangan, Volume 13, Number 2, July 2018 79 Astawan et al. nents in soybeans, producing tempe which has al. (2014) reported that fermentation with BAL an enhanced nutritional content and improved is also commonly used for the production of bio- bioactive components and is more beneficial for active peptides. These bioactive components will health than soybeans (Astawan et al. 2017). Table lend active physiological properties for health. 1 shows the bioactive components in soybean and The amount and types of bioactive compo- the benefit for health. nents produced during the fermentation of tempe The technology of tempe-making is “ad- are influenced by the enzymatic activities of the opted” in food technology as the term Solid State . Efriwati and Nuraida (2013) Bioconversion (SSB) or Solid State Fermentation demonstrated that differences during the tempe (SSF) by exploiting various which are usu- production process will yield different mac- ally used in traditional fermentation processes ronutrient components (carbohydrate, fat, and such as Rhizopus sp, Aspergillus sp., protein) in the tempe and also differences in the sp., et cetera (Maiti & Majumdar 2012; McCue content. Differences in the tempe pro- et al . 2005; Sanchez-Magana et al. 2014). Fer- duction method create a possibility for different mentation of soybeans using the mold Rhizopus microbes to exist and to take part in the tempe spp. is favored because the application is simple fermentation process (Barus et al. 2008). The dif- and able to produce products with a palatable fla- ferences in microorganisms will determine the vor (Sanchez-Magana et al. 2014; Wijaya et al. differences in proteolytic, lipolytic, and glycolyt- 2007). ic activities, and these will determine differences Fermentation will increase the content in the bioconversion of fat, protein, carbohydrate of small molecules such as free fatty acids and and other components (Tope 2014). amino acids (Ali et al. 2016) and the isoflavone A number of in vitro tests revealed a few aglycone (Haron et al. 2009), as well as produce bioactive components in soybeans and products bioactive peptides (Gibbs et al. 2004). This is derived from soybeans that play a role in the due to the enzymatic activity of microorganisms treatment of obesity such as phenolic (isoflavone) which works on the soybean substrate, for exam- component and peptides. Some of the mecha- ple, (BAL), mold, and yeast nisms of these components can be seen in Table (Gibbs et al. 2004; Barus et al. 2008). Singh et 2.

Table 1. The bioactive components in soybeans and the benefits for health (Sugano 2006)

Component Health benefits Protein Hypocholesterolemic, antiatherogenic, reduces weight Peptide Easily absorbed, reduces weight Immunity, anticarcinogenic Anticarcinogenic Improves the function of the digestive tract, prevents colon cancer, regulates the metabolism of fat Prebiotic, improves the function of the digestive tract Phytin Regulates carbohydrate metabolism, anticarcinogenic, aids in absorption Saponin Regulates fat metabolism, antioxidant Isoflavone Esterogen functions, prevents osteoporosis, anticarcinogenic Linoleic acid Essential , hypocholesterolemic Linolenic acid Essential fatty acid, hypocholesterolemic, improves the function of the cardiovascular sys- tem, antiallergy Increases the metabolism of fat, maintains nervous functions Antioxidant, prevents cardiovascular diseases Hypocholesterolemic, prevents prostate cancer K Aids in blood clotting, prevents osteoporosis Mg Essential mineral, prevents cardiovascular problems

80 J. Gizi Pangan, Volume 13, Number 2, July 2018 Tempe for the treatment of obesity

Table 2. Bioactive components in tempe for the treatment of obesity

Bioactive Active physiological Product Research method References component properties Soybean tempe E peptide and I Antioxidant through Positive antioxidant activity, Gibbs et al. with R.oligosporus peptide the ferric thiocyanate and E peptide also has an ACE (2004) NRRL 2710 method inhibition property with an

IC50 of 0.6±0.1μM Solid state biopro- Phenolic com- Inhibition of amylase, Maximum inhibition of amy- McCue et al. cessed soybeans ponent α-glucosidase, and lase on day 4 of fermentation (2005) with R.oligosporus antioxidant through with an inhibition index (AI) the DPPH method of 2.08. Highest glucosidase inhibition on day 6 of fermen- tation, AI=1.1. A correlation of R=0.85 between antioxidant activity and amylase inhibition Solid state bio- Phenolic com- Inhibition of amylase, Highest antioxidant on fermen- Maiti and Ma- conversion (SSB) ponent α-glucosidase, and tation day 4, 57.4% higher than jumdar (2012) of soybeans with antioxidant through soybeans without fermenta- R.oligosporus the DPPH method tion, highest amylase inhibi- tion on day 6 of fermentation, AI=3.6, highest glucosidase inhibition on day 6 of fermen- tation, AI = 2.0

1.1. Phenolic component and isoflavone Figure 1 shows the chemical structure of soybean In Indonesia, soybeans are processed isoflavones according to Shaoet al. (2009). into tempe, , , , and soymilk. Isoflavones also play many roles in the Among those soybean products, tempe is the inhibition of carbohydrate-digesting . food with the highest isoflavone aglycone thus Lee and Lee (2001) demonstrated that provide higher bioavailability compared to other is an effective α-glucosidase inhibitor, soybean products (Haron et al. 2009). Raw tempe is reversible, slow-binding and non-competitive. has an isoflavone content of 54 mg/100 g (bb), The product of soybean fermentation using R. while tofu and soymilk have a lower isoflavone oligosporus demonstrated an amylase inhibition content of 43 and 28 mg/100 g (bb), respectively. of 1.5-2.0 AI (Amylase Inhibition Index) which Mold fermentation helps activate the soy- correlated with the total phenol value (R=0.59) ’s isoflavone component (Figure 1) from the (McCue et al. 2005; Maiti & Majumdar 2012). glycone form ( and ) to aglycone In addition, Genistein also has a potential ( and genistein) that are more readily as an antiobesity through the activation of the absorbed by the body (Astawan 2008) and also AMP-activated kinase (AMPK) in the inhibition increases the antioxidant activity (Astawan et al. of lipid differentiation (Hwang et al. 2005). Ge- 2013). Efriwati and Nuraida (2013) found that nistein (20-200 uM) could significantly inhibit the genistein and daidzein contents of tempe were 90% of adipose tissue differentiation from 3T3- 9.4-10.0 and 93.4-101.2 mg/100 g tempe (b.k), L1 cells and also induce apoptosis (43%) in ma- respectively. Haron et al. (2009) found that the ture adipose tissue (Hwang et al. 2005). In vivo total isoflavone aglycone was 54 mg/100 g tempe testing of 0.2% genistein + 0.5% L-carnitine in (b.k) with almost identical amounts of daidzein C57BL/6J rats with high-fat feed demonstrated a and genistein, 26±6 mg and 28±11 mg. decrease in body weight of 254% after 12 weeks The bioconversion of glycone isoflavone of the experiment. This was believed to be due to and the improved bioavailability of isoflavone a PPAR activation inhibition mechanism (Yang et would increase the active physiological proper- al. 2006). Numerous benefits of soybean isofla- ties of tempe in comparison to soybean, for ex- vones and their increased amount in tempe create ample in condition such as hypotriacylglycerol an opportunity to utilize tempe in the treatment (Watanabe et al. 2006) and hypocholesterolemic of obesity. (Astuti 1997) that usually occur in obesity cases.

J. Gizi Pangan, Volume 13, Number 2, July 2018 81 Astawan et al.

Figure 1. The chemical structure of soybean isoflavones (Shaoet al. 2009)

1.2. Protein and or peptides have antiobesity properties through a number of Other components of soybeans that play a mechanisms such as anorexia or appetite sup- part in obesity treatment are protein and peptides. pression, inhibition of lipogenesis in the liver Wang and Huang (1984) discovered a protein (decreasing the triglyceride and cholesterol levels found in soybean, sunflower seeds, , and in the blood), and inhibition of the activation of cucumber seeds which have an antiobesity poten- the hormone cholecystokinin (CCK), causing sa- tial through a lipase inhibition mechanism. The tiety. Jang et al. (2008) stated that in overweight inhibition effect was strongly influenced by heat rats induced by high-fat feed, supplementation of and the role of protease and was not dependent peptides from black soybeans for 13 weeks has on the amount of the enzyme lipase but depended shown weight loss, decreased leptin level and de- on the amount of substrate. A large amount of creased appetite compared to the controls. substrate eliminated the lipase inhibition effect, thus in the application, limitation of fat consump- 2. The Effect of soybeans and tempe in obesity tion was also required for an optimum lipase in- treatment hibition benefit. A few in vivo studies related to the effect The lipase inhibition mechanism is be- of soybean and or tempe consumption on obese lieved to be through the binding of protein on test animals can be seen in Table 3. Obesity is the surface of the substrate micelle, preventing usually associated with insulin resistance and the normal lipase function which works on the abnormalities in lipid metabolism in the form interfacial area between the medium (water) and of increased overall lipid production such as in- the surface of the micelle (Wang & Huang 1984). creased free fatty acids, triglycerides, and LDL This soybean protein component is believed to (Yuliana et al. 2011). Metabolomic issues such still be present in tempe, or the lipase inhibition as dyslipidemia and or diabetes as an effect of activity in tempe could still be maintained by oth- obesity can be managed by consuming soybeans, er, smaller proteins or peptides produced through soybean products such as tempe, or soybean hy- tempe fermentation. Gibbs et al. (2004) demon- drolysate as a source of protein. Watanabe et al. strated an increase in dissolved protein in tempe (2006) and Astawan et al. (2015) demonstrated compared to soybean, plus antioxidant properties an improvement in lipid profile, especially an in- and other active physiological actvities. crease in HDL due to consumption of tempe feed Singh et al. (2014) stated that bioactive (isocaloric) compared to consumption of casein peptides from soybeans and its products also or soybean.

82 J. Gizi Pangan, Volume 13, Number 2, July 2018 Tempe for the treatment of obesity

Table 3. In vivo studies related to the effect of soybean and or tempe consumption on obesity treatment

Model Feed and Amount Time Results References Wistar male rats Three groups: casein, soy- 6 weeks No difference in weight. Watanabe bean, and tempe-GABA A significant difference in cholesterol et al. (2006) with R. microspores inocu- and triacylglyceride levels in plasma, lum fermented aerobically namely casein>soybean>tempe-GA- and anaerobically. BA. Isoprotein (30% ), previ- The highest HDL in the tempe-GABA ously fed high-fat feed group. (20%) The highest LDL in the casein group. Adult male Three groups: casein, pro- 4 weeks Adult rats: lower fat absorption in SPI Aoyama Sprague-Dawley tein soybean isolate (SPI), and SPI-H compared to that in casein, et al. 2000a rats and yellow and soybean protein hy- total cholesterol, and blood glucose KK mice, made drolysate (SPI-H) lower in SPI-H. obese Low-calorie feed (60%), Mice: significantly lower body fat in high protein (35%) and SPI and SPI-H than in casein. low fat (5%), previously fed high-fat feed (30%) Male yellow Four groups: casein 2 weeks A significant descrease in the body Aoyama KK mice, made (WPI), casein hydrolysate weight of SPI-H rats compared to WPI et al. 2000b obese (WPI-H), soybean protein and WPI-H. Total plasma cholesterol, isolate (SPI), and soybean blood glucose, and body fat level lower protein hydrolysate isolate in SPI-H than in WPI and WPI-H. (SPI-H) Feed as in Aoyama et al. 2000a Obese (weight: Fours groups: 20% casein 20 The isoflavone group had a significant Ali et al. 125 g) and nor- (normal), casein +0.1% weeks loss of body weight, epididymal, peri- 2004 mal (96 g) SHR/ isoflavone, casein +0.1% renal, subdiaphragmatic, ileal fat pad N-cp rats , casein +0.1% fat weight, and total cholesterol com- isoflavone +0.1% probi- pared to the other treatments in obese otic; Isocaloric. rats.

An experiment using low calorie (60 %), acid components in tempe had a better hypotriac- high protein (35%) and low fat (5%) feed in obese ylglyceride effect than soybeans or casein. rats demonstrated a decrease in body weight and Tempe, which contain protein composition an improvement in the condition of the body that has been fermented into peptides (similar to fat in rats fed with soybean protein isolate and the condition in soybean protein hydrolysate) soybean hydrolysate compared to those fed with and supported by higher isoflavone component casein and milk protein hydrolysate (Aoyama et than soybeans (Haron et al. 2009) or soybean al. 2000a, Aoyama et al. 2000b). The mechanism hydrolysate, is of course expected to have more involved were decrease in perirenal fat and blood benefits for health including for obesity - treat glucose concentration. Furthermore, Kagawa et ment. Unfortunately, no studies in place aimed al. (1996) suspected that the fat reduction effect at pertaining to this subject. The author has not was due to the activity of the tetrapeptide found found any clinical studies regarding the use of in soybeans. tempe in humans for the purpose of obesity con- In addition to protein and or peptides ac- trol. However, one human study conducted by tivities, the decrease in body weight and the im- Astuti (1997) has demonstrated the benefits of provement in the lipid condition was also due to tempe in improving the lipid or dyslipidemia the activity of isoflavone (genistein, daidzein, and status which is also commonly found in obesity ) (Ali et al. 2004) found in soybeans and cases (Table 4). tempe. Further, Watanabe et al. (2006) demon- Many clinical studies pertaining to the strated that the protein, isoflavone and free amino use of soybeans in obesity treatment have been

J. Gizi Pangan, Volume 13, Number 2, July 2018 83 Astawan et al.

Table 4. Studies in humans pertaining to the effect of consuming soybeans and or tempe in obesity treat- ment (Astuti 1997)

Product Research method Results Tempe formula-based food 24 volunteers (8 men, 16 wom- A decline in total cholesterol (8.6% in men, en), daily consumption of a tem- 10.25% in women), a decline in LDL (12% pe-based drink for three months in men, 9.67% in women), a decline in MDA (23% in men, 15% in women). conducted. Cope et al. (2008) reported in a re- could trigger obesity. Haron et al. (2009) stated view that a number of soybean-based food pro- that in 100 g raw tempe there is 205 ± 56 mg ducts will reduce body weight and eliminate fat (dry weight) of isoflavone and the process when consumed isocalorically. This was proven would decrease the isoflavone by 45% to merely through in vivo testing using model animals, 113 ± 41 mg per 100 g (dry weight) of fried tem- though there are very few supporting clinical pe. The correct tempe processing such as boiling studies in humans. or without frying or other processes that Zhang et al. (2013) have conducted a involve little fat could be considered as an alter- meta-analysis of the efficacy of the consump- native (Muaris 2016) in the optimation of tempe tion of a soybean isoflavone supplement on body in obesity treatment diets. weight, fasting blood glucose, and insulin in Daily consumption of tempe in adequate post-menopausal non-Asian women. Nine stu- amounts could support the daily -based pro- dies with 528 panelists for the parameter of body tein and isoflavone intake. In 1995, the US FDA weight, 11 studies with 1,182 panelists for the declared that a minimum of 25 grams of plant- parameter of blood glucose, and 11 studies with based protein needs to be consumed daily as a 1,142 panelists for the parameter insulin have part of a low fat and low cholesterol diet. Utari been analyzed. These studies have demonstrated et al. (2011) suggested consumption of at least significant weight loss and a decrease in blood medium-sized slices of tempe (approximately glucose and insulin in post-menopausal female 150 grams of tempe/day) cooked by or panelists who had been given isoflavone as a boiling to improve the lipid profile. Consump- supplement compared to the control group which tion of that amount of tempe is equivalent to the was given a placebo. Furthermore, supplementa- consumption of 35 mg/day of isoflavone and is tion of isoflavone for a short time (<6 months) in line with the recommended daily isoflavone could significantly decrease weight, while long- consumption which is 30-100 mg/day (Messina term supplementation (>6 months) could signifi- & Messina 2003). The effectiveness of tempe as cantly decrease blood glucose. A more significant a functional food in obesity cannot be achieved in weight loss was achieved through the consump- a short time or with a certain dossage. Consum- tion of a low dosage of supplement (<100 mg) ing tempe regularly with appropriate processing and for those who were overweight (BMI <30) in the long term should be incorporated in the compared to those who were obese (BMI >30). healthy living habit.

3. Tempe as a functional food in obesity treat- CONCLUSION ment Considering the various potentials of the Based on the literature study, it is known bioactive components in tempe as an antiobe- that soybeans are beneficial in the treatment of sity, tempe could be made into an appropriate obesity and its complications. Soybeans help diet menu. Yenrina et al. (2006) stated a survey reduce body weight and improve the body lipid of 2,080 households on Island revealed that condition. The bioactive components which are they consumed processed soybean products such presumed to play a role are soybean protein, pep- as tofu, tempe, , soybean sprouts, tofu tides, and isoflavone. The fermentation of soy- skin, and soy sauce in daily basis. Unfortunately, beans into tempe can increase the amount and many of the processes involved frying, especially ability of these bioactive components. Optima- for tempe. tion and popularization of tempe consumption as The frying process would increase fat in- a functional food in the daily diet, supported with take (from the cooking oil absorbed by the pro- correct tempe processing (without frying), could duct), indirectly increasing the caloric intake and be a solution in obesity treatment.

84 J. Gizi Pangan, Volume 13, Number 2, July 2018 Tempe for the treatment of obesity

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