Bioactive Compounds, Nutritional Value, and Potential Health Benefits of Indigenous Durian (Durio Zibethinus Murr.): A Review

Durian (Durio zibethinus Murr.) is an energy-dense seasonal tropical fruit grown in Southeast Asia. It is one of the most expensive fruits in the region. It has a creamy texture and a sweet-bitter taste. The unique durian flavour is attributable to the presence of fat, sugar, and volatile compounds such as esters and sulphur-containing compounds such as thioacetals, thioesters, and thiolanes, as well as alcohols. This review shows that durian is also rich in flavonoids (i.e., flavanols, anthocyanins), ascorbic acid, and carotenoids. However, limited studies exist regarding the variation in bioactive and volatile components of different durian varieties from Malaysia, Thailand, and Indonesia. Experimental animal models have shown that durian beneficially reduces blood glucose and cholesterol levels. Durian extract possesses anti-proliferative and probiotics effects in in vitro models. These effects warrant further investigation in human interventional studies for the development of functional food.


Nutritional Composition of Different Durian Varieties
The energy content of durian is in the range of 84-185 kcal per 100 g fresh weight (FW) ( Table 1) [6,18,19]. This range is somewhat similar to that of the United States Department of Agriculture (USDA), Malaysian, and Indonesian food composition databases [20][21][22]. Durian aril of the Thailand variety of Kradum showed the highest energy content at 185 kcal compared with other durian varieties [6,12,13]. Indonesian variety of Hejo showed the lowest energy content at 84 kcal per 100 g FW of durian aril [6]. The higher and lower energy contents are attributed to the difference in carbohydrate content. The carbohydrate content varies between different durian varieties in the range between 15.65 to 34.65 g per 100 g FW [6,12,13]. The range of carbohydrate content is similar to that of USDA, Malaysian and Indonesian food composition data, at 27.09 g, 27.90 g, and 28.00 g per 100 g FW, respectively [31][32][33]. The energy content of durian is the highest compared with other tropical fruits such as mango, jackfruit, papaya, and pineapple [31]. * For [6], energy was calculated by Atwater factor (1 g protein = 4 kcal, 1 g carbohydrate = 4 kcal, 1 g fat = 9 kcal) [34].
Protein content of different durian varieties is in the range of 1.40 to 3.50 g per 100 g FW [6,12,13]. This range is similar to that of USDA, Malaysian, and Indonesian food composition data, at 1.47 g, 2.70 g, and 2.50 g per 100 g fresh weight (FW), respectively [31][32][33]. Durian contains a high amount of fat and is in the range of 1.59 to 5.39 g per 100 g FW, a figure comparable to the data from USDA, Malaysian, and Indonesian food composition databases at 5.33 g, 3.40 g, and 3.00 g of fat per 100 g FW, respectively [6,12,13,[31][32][33]. The fat content of durian is somewhat comparable to one-third of ripe olives [31]. Total sugar of Malaysian, Thailand, and Indonesian durian varieties is in the range of 7.52 to 16.90 g, 14.83 to 19.97 g, and 3.10 to 14.05 g per 100 g FW, respectively ( Table 2). The Thailand variety of Kradum showed the highest total sugar, at 19.97 g per 100 g FW. Sucrose was the predominant sugar in durian, with 5.57 to 17.89 g per 100 FW, followed by glucose, fructose, and maltose. However, the Malaysian variety of D24 contains higher amounts of fructose than glucose.  Table 3 shows fatty acid compositions of different durian varieties. Thailand durian varieties showed higher monounsaturated fatty acids (MUFA) than saturated fatty acids (SFA) and polyunsaturated fatty acids (PUFA), with exception of Monthong. Palmitic acid (16:0) was the major SFA, in the range of 84.57 to 1696.00 mg per 100 g FW, while oleic acid (18:1) was the major MUFA found in the matured or fully ripened durian (64.89 to 2343.30 mg per 100 g FW). However, each study used a different technique for fatty acid analysis. Gas chromatography was used by Charoenkiatkul et al. (2015) while high pressure liquid chromatography was used by Haruenkit et al. (2010) [13,14]. Both MUFA and SFA might be involved in various metabolic pathways, including the regulation of transcription factors and the expression of multiple genes related to inflammatory processes [37][38][39].  Table 4 shows the mineral compositions of ripe Thailand durian. Durian is high in potassium in the range from 70.00 to 601.00 mg per 100 g FW [11,13,14,[31][32][33]. This is comparable to potassium-rich fruit such as banana, with the value of 358.00 mg per 100 g FW [31]. Phosphorus, magnesium, and sodium are in the range of 25.79 to 44.00, 19.28 to 30.00, and 1.00 to 40.00 mg per 100 g FW, respectively. Durian is also a source of iron, copper, and zinc with the range of 0.18 to 1.90, 0.12 to 0.27 and 0.15 to 0.45 mg per 100 g FW, respectively. The Thailand variety of Chanee showed the highest level of iron, zinc and potassium among the studied durian [12,[19][20][21][22]29]. Durian also contains vitamin A, different types of vitamin B, and vitamin E [13][14][15][31][32][33].  Table 5 shows soluble, insoluble, and total dietary fibres in Thailand durian varieties. However, there are limited data available for Indonesian and Malaysian varieties. The total dietary fibre is in the range from 1.20 to 3.39 g per 100 g FW for Thailand Monthong variety. However, it must be noted that different analyses were used between studies. Soluble dietary fibre varied from 0.74 g (Puang Manee) to 1.40 g (Monthong) per 100 g FW while insoluble dietary fibre is in the range from 0.60 g (Kan Yao) to 2.44 g (Chanee) per 100 g FW [10,12,16].
Ethanol was the predominant alcohol compound in Malaysian and Indonesian varieties in the range from 590.00 to 720.00 ng per g and 419.90 to 1091.30 ng per g fresh weight (FW), respectively. Another three alcohols were detected in durian as 2-methyl-1-butanol, 3-methyl-1-butanol and 2,3-butanediol in Malaysian and Indonesian durian [7,45]. Weenen et al. (1996) detected additional alcohols in durian Cane, Kodak, and Bobo from Indonesia as hexadecanol, 9-octadecen-1-ol (cis and trans), and isobutyl alcohol [44]. Voon  3-Hydroxy-2-butanone (a ketone) was identified in the Indonesian variety in the range of 56.20 to 84.20 ng per g FW [7,42]. Durian Matahari showed the highest amount of 3-hydroxy-2-butanone with 84.20 ng per g FW and the lowest in Hejo with 56.20 ng per g FW [42]. 3-Hydroxy-2-butanone (common name: acetoin) has a pleasant yogurt creamy odour and a fatty butter taste. It is present in vinegar and alcoholic beverages [47]. Another ketone was identified as 2-hydroxy-3-pentanone in durian varieties from Indonesia, Kodak, Cane, and Bobo [44]. However, 2-hydroxy-3-pentanone has an unfavourable odour like fishy and earthy [48]. For aldehydes, acetaldehyde detected in Indonesian variety of Hejo, Matahari, and Ajimah in the range of 33.90 to 62.20 ng per g FW [42]. Acetaldehyde contributed to the fruity and sweet aroma in durian [49].
Esters are the second most abundant bioactive compounds in durian after sulphur. Esters were the volatiles that contributed to the sweet odour to durian, more than aldehyde, while aldehyde contributed more to the fruity note. The major ester compounds in Malaysian durian varieties (D101, D2, and D24) were characterized as propyl 2-methylbutanoate, ethyl propanoate, propyl propanoate and methyl 2-methylbutanoate [7]. Ethyl 2-methylbutanoate was detected as major ester in Indonesian varieties of Hejo, Matahari, and Ajimah [42]. Ethyl propanoate, methyl propanoate, propyl propanoate, ethyl 2-methyl propanoate and 3-methylbutyl propanoate volatiles have similar structure and differ only in the number of carbon atoms (ethyl, methyl) [50]. Ethyl propanoate is the major ester detected in Malaysian and Indonesian durians in the range of 0.00 to 3110.00 ng per g FW. It was noted that Malaysian durian variety showed much higher content of ethyl propanoate than Indonesian variety [7,42].

Health Benefits of Durian
Durian is rich in macronutrients (sugars and fat) and micronutrients (potassium), dietary fibres, and bioactive and volatile compounds. An intake of one serving size of durian aril (155 g) contributes to 130 to 253 kcal and is equivalent to one large pear and four small apples without skin, respectively [6,[31][32][33]. Durian is energy-dense due to sugar and fat content and hence, might contribute to daily energy intake and will also increase postprandial blood glucose.

Effects of Durian on Blood Glucose
Durian is high in sugar, but supplementation of 5% freeze-dried Monthong (Thailand variety) in 1% cholesterol-enriched diets in rats for 30 days did not raise the plasma glucose level compared with control diet [41]. In humans, Robert et al. (2008) showed that durian had the lowest glycaemic index (GI = 49) compared with watermelon (GI = 55), papaya (GI = 58), and pineapple (GI = 90) [51]. The low GI value for durian might be due to the presence of fibre and fat. Fibre slows digestion in the digestive tract and will slow down the conversion of the carbohydrate to glucose, thus lower the GI of food [52]. Fat does not have a direct effect on blood glucose response, but it may influence glycaemic response indirectly by delaying gastric emptying, and thus slowing the rate of glucose absorption [53].
Durian is rich in potassium and is similar to potassium-rich fruit, i.e., banana [31]. A meta-analysis study showed that there was a linear dose-response between low serum potassium and risk of type 2 diabetes mellitus [54]. Chatterjee et al. (2017) demonstrated that potassium chloride supplementation reduced the worsening effect of fasting glucose in African-Americans compared with placebo [55]. Collectively, the evidence has shown that potassium content in durian might play a role in the regulation of blood glucose. The effect of durian on blood glucose has not been thoroughly explored both in animal and human studies, and hence, warrants further investigation. Potassium might play a role in glucose homeostasis but might also have negative implications in certain conditions. For instance, those with chronic kidney disease (CKD), diabetes mellitus (DM), and heart failure (HF) or on pharmacological therapies may develop hyperkalaemia [56].

Cholesterol-Lowering Properties of Durian
Anti-atherosclerotic properties of durian aril have been reported in experimental rat models [10,11,20,22,40,41]. Previous in vitro and in vivo studies investigated the health benefits of durian (Monthong variety) on lipid profiles [10,11,22]. Haruenkit et al. (2007) showed that rats fed with durian significantly (p < 0.05) reduced postprandial plasma total cholesterol (TC) and low-density lipoprotein cholesterol (LDL-C) with 14.9% and 21.6%, respectively, compared with control group [10]. Gorinstein et al. (2011) showed a reduction in the levels of plasma TC (12.1%), LDL-C (13.3%), and triglycerides (TG) (14.1%) compared with the control group [11]. The results were consistent when tested with other durian from Thailand varieties (Chanee and Kan Yao) compared with control. Leontowicz et al. (2011) showed that rats supplemented with ripe durian had significantly lowered TG (26.3%), but not significant in TC (4.8%) and LDL-C (6.3%). Histological analysis demonstrated that ripe durian protected the liver and aorta from exogenous cholesterol loading and protected the intimal surface area of the aorta [20]. Durian also demonstrated the ability to hinder postprandial plasma lipids compared with snake fruit and mangosteen [10,11,22]. Previous studies have showed that propionate (0.6 mmol/L) inhibited fatty acid and cholesterol synthesis in isolated rat hepatocytes [57]. In our review, three different propionate esters were identified, i.e., ethyl propionate, methyl propionate and propyl propionate. These esters could be a potent inhibitor for free fatty acids and cholesterol synthesis but this warrants further investigations. However, these esters are highly volatile and could be easily vaporized during sample processing and storage [57].

Anti-Proliferative Activity
The polyphenol and flavonoid contents of durian are in the range of 21.44 to 374.30 mg GAE and 1.90 to 93.90 mg CE per 100 g FW. The mechanisms of action of polyphenols strongly relates to their antioxidant activity. Polyphenols are known to decrease the level of reactive oxygen species in the human body [58]. The phenolic groups present in the polyphenol structure can accept an electron to form relatively stable phenoxyl radicals, thereby disrupting chain oxidation reactions in cellular components [59]. On the other hand, polyphenols could induce apoptosis and inhibit cancer growth [60][61][62][63]. There are many studies pointing out an essential role of polyphenolic compounds as derived from vegetables, fruits, or herbs in the regulation of epigenetic modifications, resulting in the antiproliferative protection [64]. Jayakumar and Kanthimathi studied the anti-proliferative activity of durian using a breast cancer cell line (MCF-7). This study showed that durian fruit can be considered as potential sources of polyphenols with protective effects against nitric oxide-induced proliferation of MCF-7 cells, an oestrogen receptor-positive human breast cancer cell line [65]. At a concentration of 600 µg/mL, durian fruit extracts inhibited MCF-7 cell growth by 40%. However, an in vivo study is needed to confirm this effect.

Probiotic Effects
Durian aril is rich in sugar with total sugar content between 3.10 to 19.97 g per 100 g FW. The moisture content of durian aril is 56.1 g to 69.3 g per 100 g FW and pH between 6.9 to 7.6 [5,13,31]. These could be an optimum condition for bacteria fermentation. Durian aril is fermented after being left at room temperature for a few days and turns sour and watery. In Malaysia, underutilised durian aril is fermented (spontaneous and uncontrolled) to a product known as Tempoyak [66]. Tempoyak is widely used as seasoning in cooking. According to Leisner et al. (2001) lactic acid bacteria (LAB) are the predominant microorganisms in Tempoyak [67]. The LAB microorganisms were identified as Lactobacillus plantarum. However, other species including Lactobacillus fersantum, Lactobacillus corynebacterium, Lactobacillus brevis, Lactobacillus mali, Lactobacillus fermentum, Lactobacillus durianis, Lactobacillus casei, Lactobacillus collinoides, Lactobacillus paracasei and Lactobacillus fructivorans were also reported in Tempoyak [67][68][69][70]. Khalil et al. (2018) and Ahmad et al. (2018) recently demonstrated the potential of Tempoyak as a source of probiotics. The study by Khalil et al. (2018) isolated seven Lactobacillus strains that belonged to five different species of the genus Lactobacillus, including one Lactobacillus fermentum (DUR18), three Lactobacillus plantarum (DUR2, DUR5, DUR8), one Lactobacillus reutri (DUR12), one Lactobacillus crispatus (DUR4), and one Lactobacillus pentosus (DUR20) from Tempoyak. These strains were able to produce exopolysaccharide (EPS) and had great potency to withstand the extreme conditions, either at low pH 3.0, in 0.3% bile salts or in in vitro model of gastrointestinal conditions [69]. EPS has the prebiotic potential to positively affect the gastrointestinal (GIT) microbiome and may reduce cholesterol [70]. Ahmad et al. (2018) isolated Lactobacillus plantarum from Tempoyak and showed good probiotic properties including acid and bile salt tolerance, antioxidative, antiproliferative effects, and remarkable adhesion on colon adenocarcinoma cell line (HT-29 cell lines) [71].

Conclusions
Durian is rich in macronutrients (sugars and fat) and micronutrients (potassium), dietary fibre, and volatile compounds. Durian is an energy-dense fruit due to high sugar and fat content and, hence, might contribute to daily energy intake and increase postprandial blood glucose. Durian is also rich in bioactive polyphenols and hence possessed strong in vitro antioxidant capacity. However, the bioactivity of these polyphenols in animal or human studies is still scarce and needs further investigation. The major volatile compounds have been identified in the Malaysian, Thai, and Indonesian durian varieties as esters (ethyl propanoate, methyl-2-methylbutanoate, propyl propanoate), sulphurs (diethyl disulphide, diethyl trisulphide and ethanethiol), thioacetals (1-(methylthio)-propane), thioesters (1-(methylthio)-ethane), thiolanes (3,5-dimethyl-1,2,4-trithiolane isomers), and alcohol (ethanol). Both in vitro and in vivo animal studies showed that durian possessed anti-hyperglycaemic, anti-atherosclerotic, anti-proliferative, and probiotic effects. Durian is rich in bioactive compounds, and hence can be used as an active ingredient for the development of functional foods. Further human interventional studies are warranted to explore the health benefits of functional foods prepared with durian.