Phytochemical profiles and antioxidant capacities of white and red ginseng as affected by marinating media (vinegar, yellow wine, and Chinese liquor)

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1 Received: 29 July 2016 Revised: 17 December 2016 Accepted: 14 February 2017 DOI: /jfpp ORIGINAL ARTICLE Phytochemical profiles and antioxidant capacities of white and red as affected by marinating media (vinegar, yellow wine, and Chinese liquor) X. C. Zhang B. J. Xu Food Science and Technology Program, Beijing Normal University-Hong Kong Baptist University United International College, Zhuhai, Guangdong, , China Correspondence B. J. Xu, 28, Jinfeng Road, Tangjiawan, Zhuhai, Guangdong Province , China. Funding information Beijing Normal University-Hong Kong Baptist University United International College, China; Grant/Award Numbers: UICRG and UICRG Abstract Marinating is popular practice at home and being applied to industrial manufacturing in China. However, knowledge on the effects of steeping media on antioxidant capacity of is limited. Hair root, sliced, powdered, ultrafine ground white and red were marinated with 3.58 and 98 vinegar, yellow wine, and 538 Chinese liquor. Total phenolic content (TPC), total flavonoid content (TFC), DPPH free radical scavenging capacity (DPPH), ferric reducing antioxidant power (FRAP), ABTS free radical scavenging capacity, and total saponin content (TSC) of the steeped liquid were measured with colorimetric methods. Among four marinating media, Chinese liquor is the most favorable medium since most of the indicators showed obvious higher values. It was noticed that TFC and TSC of white hair root steeped liquid by Chinese liquor were extremely higher than others. The results indicate that Chinese liquor is the most desirable medium for steeping. Practical applications Presented information will guide consumers to choose materials and steeping methods to obtain desired health benefit components. The study will also help food manufacturers and alcoholic beverage industry to understand how steeping medium affect the bioactive food components. 1 INTRODUCTION Ginseng (Panax Meyer) is a precious herb for medicinal use in Eastern Asia such as Northeast of China. It is well known that contains various bioactive compounds which have potential health promotion effects, the most famous compounds are ginsenosides which can inhibit tumor growing (Attele, Wu, & Yuan, 1999; Ji et al., 2012; Ma, Xiao, & Liang, 2006). The cultivated (root and rhizome of Panax C. A. Meyer) as a New Food Material has been approved by China Ministry of Health in Five-year-old or younger was permitted to enter into food market on August 29 of 2012 and could be used as a food material in China (Chen, Du, & Xu, 2015). After that root is no longer only used as therapeutic agents but also marketed as dietary supplements or raw materials of health food in China. The phenolic contents and antioxidant capacities of which were used as a food material have been study in our previous study (Chen, Cai, & Xu, 2014). Besides, the antioxidant activity of has been researched for a long time. Ginseng is generally processed in sliced and powdered forms. In recent years, nanotechnology shows its advantages to process both food and medicine. A study pointed that 2.5 times of ginsenosides can be steeped from nanoscale Chinese white than that from microscale Chinese white (Ji et al., 2012). Another research found that more cytotoxic effect against hepatoma cell growth by ultrafine ground red particles (Park, Kim, Youn, & Lee, 2008). Marinating herbs with liquor is a traditional method to process medicinal herbs in China; it is still popular practice in China now. This method is being applied at home and industrial manufacturing. Chinese liquor is generally used to steep herbs for a period to extract the valuable compounds with health promotion effects, such as a study of goji berry conducted by Song and Xu (2013). Ginseng is one of the most popular materials used to process medicinal liquor in China. Chinese liquor and Chinese yellow wine are the steeping media usually used to steep materials according to folk traditions. A study showed that vinegar-processed reduced more insulin resistance J Food Process Preserv. 2018;42:e wileyonlinelibrary.com/journal/jfpp VC 2017 Wiley Periodicals, Inc. 1of7

2 2 of 7 ZHANG AND XU induced by a high-fat diet in ICR mice than nonprocessed root (Yun, Ko, Lee, & Chung, 2007). Since the information on the effects of steeping media on antioxidant capacity of is limited. The objectives of this study were to investigate how phenolic profiles and antioxidant capacity were influenced by different steeping media in six forms of commonly consumed products, and to figure out how the antioxidant properties are altered by the steeping media. In this investigation, sliced white, powered white, white hair root, ultrafine ground white, powdered red and ultrafine ground red samples were prepared. The 3.58 vinegar, 98 vinegar, 538 Chinese liquor, and yellow wine were selected to be the steeping media. Total phenolic content (TPC), total flavonoid content (TFC), DPPH free radical scavenging capacity (DPPH), ferric reducing antioxidant capacity (FRAP), ABTS free radical scavenging capacity, and total saponin content (TSC) are used as indicators to determine the antioxidant capacity of materials in this study. This study will provide a base to further researches about processing. 2.2 Chemicals and reagents (1)-Catechin and soyasaponin Ba was purchased from Sigma-Aldrich Co. (St. Louis, MO). Folin-Ciocalteu reagent, DPPH, ABTS, Trolox and TPTZ were supplied from Shanghai Yuanye Biotechnology Co., Ltd (Shanghai, China). Gallic acid, sodium nitrite, ferrous sulfate, potassium persulfate, sodium hydroxide, vanillin, and aluminum chloride hexahydrate (AlCl 3 6H 2 O) were purchased from Tianjin Damao Chemical Reagent Co., Ltd (Tianjin, China). Sulfuric acid, hydrochloric acid, glacial acetic acid, absolute ethanol, and methanol were obtained from Tianjin Baishi Chemical Reagent Co., Ltd. (Tianjin, China). Sodium carbonate was purchased from Tianjin Fucheng Chemical Reagent Co., Ltd. sodium acetate trihydrate was purchased from Guangzhou Chemical Reagent Co., Ltd (Guangzhou, China) and ferric chloride hexahydrate (FeCl 3 6H 2 O) was purchased from Sinopharm Chemical Reagent Co., Ltd vinegar (Meiweixian Co., Guangdong, China), 98 vinegar (Meiweixian Co., Guangdong, China), yellow wine (Jiashan Co., Zhejiang, China), and 538 Chinese liquor (Tuxing Co., Beijing, China) were media used for marinating, all of these media are food grade. 2 MATERIALS AND METHODS 2.1 Ginseng materials Both white and red samples were provided by Prof. Yinan Zheng in Jilin Agricultural University, Changchun, China. The white and red products were originally purchased from DaQin Supermarket in DunHua, Jilin Province, the products were made from fresh (five-year, harvested in 2008) which were cultivated in Fusong County, Baishan City, Jilin Province of China. After trimming the hair root of white, the white samples were divided into a few portions for further processing. The white samples were processed into the sliced white, powdered white, and ultrafine ground white. The red samples were processed into powdered red, ultrafine ground red. The red has no hair root and the red also cannot be sliced due to the hard and crisp texture. The sliced white, powdered white, hair root of white, ultrafine ground white, powdered red, ultrafine ground red were used to carry out this study. 2.3 Marinating of materials Ginseng materials were marinated by soaking for seven days with four steeping media. First, every sample was weighed in 5 g in a 50 ml centrifuge tube in duplicates, and then 45 ml different steeping media were added in the tubes respectively, and the materials were steeped for seven days. At last, the materials were separated from the solvent with filter paper; the filtrates were used as samples to carry out the determinations. To subtract the background absorbance of marinating media, the respective marinating medium was used as the blank for the following colorimetric assays. The whole experimental design is elucidated in Figure Determination of total phenolic content (TPC) Total phenolic content in extracts were determined using a colorimetric method with Folin Ciocalteu assay (Singleton & Lamuela- Raventos, 1999), phenolic compounds were oxidized and formed a blue color which can be absorbed at 765 nm by an UV visible spectrophotometer. A calibration curve of gallic acid was established with a linearity range of lg/ml (R 2 >.999). The results of samples FIGURE 1 Experimental design of marination study

3 ZHANG AND XU 3 of 7 were expressed as mg gallic acid equivalents (GAE) per gram materials. 2.5 Determination of total flavonoid content (TFC) Total flavonoid content in s was determined by a modified aluminum chloride colorimetric method which described in our previous studies (Xu & Chang, 2007; Xu, Yuan, & Chang, 2007). The results were expressed as catechin equivalents (mg CAE/g) with a catechin calibration curve with a linearity range of lg/ml (R 2 >.999). 2.6 Determination of free radical DPPH scavenging capacity DDPH free radical scavenging capacity was measured by a modified colorimetric method which decolorized the purple color of DPPH and provide a strong absorption at 517 nm by the spectrophotometer (Chen & Ho, 1995; Xu & Chang, 2007). The DPPH results were described by Trolox equivalents (lmol TE/g) by using a calibration curve of Trolox with a linearity range of 20 to 750 lm (R 2 >.999). 2.7 Determination of ferric reducing antioxidant power (FRAP) FRAP was examined by a colorimetric assay described by Benzie and Strain (1999) and Xu and Chang (2007), in which the reduced ferric cations formed a navy blue color which can be absorbed at 593 nm. The FRAP values were expressed as Fe 21 equivalents (mmol Fe 21 /100 g) using a calibration curve of Fe 21 with a linearity range of mm (R 2 >.999). 2.8 ABTS free radical scavenging assay (ABTS) ABTS values were measured by a method described by Miller, Rice- Evans, Davis, Copinathan, and Milner, (1993) and Re et al. (1999), a blue color was formed which can be absorbed at 734 nm by spectrophotometer. The results were expressed as Trolox equivalents (lmol TE/g) using a calibration curve of Trolox with a linearity range of 20 1,000 lm (R 2 >.999). 2.9 Determination of total saponin content (TSC) TSC was determined by vanillin-sulfuric acid colorimetric method which described by Hiai, Oura, and Nakajima (1976). It is a color reaction between saponin content and vanillin. The TSC results were expressed as soyasaponin Ba equivalents (mg SBa E/g) using a calibration curve of soyasaponin Ba with a linearity range of 250 5,000 lg SBa/mL (R 2 >.999) Statistical analysis The results were expressed as mean 6 standard deviation (n 5 6). Analysis of variation was performed by Microsoft Office Excel Significant difference analysis was conducted by SPSS 19.0, significant levels were defined using p.05. TABLE 1 Effects of different marinating media on phytochemical profiles of TPC TFC TSC (mg GAE/g) (lg CAE/g) (mg SBaE/g) Sliced white 3.58 Vinegar b b b 98 Vinegar b a c Yellow Wine a c a Chinese liquor b d d Powdered white 3.58 Vinegar b a a 98 Vinegar b a b Yellow wine a b a Chinese liquor b c c White hair root 3.58 Vinegar b a a 98 Vinegar bc a a Yellow wine a a a Chinese liquor c b a white 3.58 Vinegar b a ab 98 Vinegar ab a a Yellow wine a b a Chinese liquor b c b Powdered red 3.58 Vinegar b a a 98 Vinegar c b a Yellow wine a c a Chinese liquor d d b red 3.58 Vinegar b a a 98 Vinegar c b a Yellow wine a c a Chinese liquor c d b Results are expressed as mean 6 standard deviation of two replicates. Phytochemical contents marked by the same later are not significantly (p.05) difference. 3 RESULTS AND DISCUSSION 3.1 Phenolic contents of marinated liquor Natural phenolics utilize their antioxidant activities to exert their health promotion effects (Fang, Yang, & Wu, 2002). Phenolic compounds are naturally existed in s, which were steeped by several steeping media. TPC values in marinated liquor are presented in Table 1. There are different TPCs from different steeping media for the same sample. Different TPCs are exhibited among different samples steeped by the same extraction solvent. The results indicate that TPC was slightly higher in the ultrafine ground white but was comparable with others. The TPCs from the sliced white marinated by different steeping media ranged from 0.94 to 1.52 mg GAE/g. It was mg GAE/g for the powdered white,

4 4 of 7 ZHANG AND XU mg GAE/g for the hair root of white, mg GAE/g for the ultrafine ground white, mg GAE/g for the powdered red, and mg GAE/g for the ultrafine ground red, respectively. The results showed that TPCs in the steeping liquid from the sliced white, the powdered white, the hair root of white, the ultrafine ground white, the powdered red, and the ultrafine ground red were less affected by steeping media since there were slight differences between the larger variation and the smaller variation for one sample. Also, the TPCs were less influenced by varieties and processed forms stated before. Flavonoid from plants has health promotion function due to their antioxidant activity (Andarwulan, Batari, Sandrasari, Bolling, & Wijava, 2010). Flavonoids are naturally existed in, which were steeped by four different steeping media and determined by colorimetric methods. TFCs from the sliced white, the powdered white, the hair root of white, the ultrafine ground white, the powdered red, and the ultrafine ground red are shown in Table 1. The TFC for the sliced white steeped by different steeping media ranged from to lg CAE/g, to lg CAE/g for the powdered white, to lg CAE/g for the hair root of white, to lg CAE/g for the ultrafine ground white, to lg CAE/g for the powdered red, and to lg CAE/g for the ultrafine ground red. The data indicate that flavonoid contents are significantly different in varieties and the processed forms. red has the highest value; the sliced white and the powdered white are comparable for the lowest TFC. The data also show that TFCs are strongly influenced by steeping media since large difference between the larger variation and the smaller variation for the same sample. Chinese liquor is the best steeping medium to extract TFC from suggested by data from Table 2, the results of other three steeping media are much lower than Chinese liquor. 3.2 Total saponin content (TSC) of marinated liquor TSC is another indicator to measure the usefulness of products by different marinating media where saponins are evidenced in traditional medicine preparations for oral administrations (Xu & Chang, 2009). The TSC results of liquors are presented in Table 1. The TSC for the sliced white steeped by different steeping media ranged from to mg SBa/g, to mg SBa/g for the powdered white, to mg SBa/g for the hair root of white, to mg SBa/g for the ultrafine ground white, to mg SBa/g for the powdered red, and to mg SBa/g for the ultrafine ground red. The results show that TSC are significantly different in different processed forms. Hair root of white has the highest value; the ultrafine ground red has relative higher TSC than others. white and the powdered red have the comparably lowest TSC. The data also indicate that TSC of TABLE 2 Effects of different marinating media on antioxidant activity of liquor DPPH FRAP ABTS (lmol TE/g) (mmol Fe 21 E/100g) (lmol TE/g) Sliced white 3.58 Vinegar a b b 98 Vinegar bc a a Yellow wine ab NA c Chinese liquor c c d Powdered white 3.58 Vinegar a b c 98 Vinegar b a a Yellow wine b NA b Chinese liquor c c c White hair root 3.58 Vinegar a b b 98 Vinegar ab c a Yellow wine b a NA Chinese liquor c d c white 3.58 Vinegar b b c 98 Vinegar a a a Yellow wine ab NA NA Chinese liquor c b b Powdered red 3.58 Vinegar a b c 98 Vinegar b c a Yellow wine c a NA Chinese liquor d d b red 3.58 Vinegar ab b b 98 Vinegar b c b Yellow wine a a NA Chinese liquor c d a Results are expressed as mean 6 standard deviation of two replicates. Values marked by the same later are not significantly (p.05) difference. s are strongly affected by four marinating media since large differences between the larger variation and the smaller variation for the same sample. Among them, hair root of white and ultrafine ground red marinated by Chinese liquor showed extremely high TSC value ( mg SBa/g). 3.3 Antioxidant capacities of marinated liquor A method used to determine the antioxidant capacity is to utilize the stable 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical which will be decolorized when it combines with the hydrogen from a free radical scavenging antioxidant (Xu & Chang, 2007). The antioxidant capacity of liquor is examined by scavenging activity of DPPH. The results are presented in Table 2. The DPPH values of the sliced white

5 ZHANG AND XU 5 of 7 ranged from 0.88 to 1.24 lmol TE/g, 0.58 to 0.99 lmol TE/g for the powdered white, 0.39 to 2.28 lmol TE/g for hair root of white, 0.69 to 1.20 lmol TE/g for the ultrafine ground white, 0.81 to 2.01 lmol TE/g for the powdered red, and 0.87 to 2.00 lmol TE/g for the ultrafine ground red. The data indicate that there are no significant differences between different forms of products. DPPH value of the powdered white is relatively lower than others. It showed that DPPH values were not significantly influenced by steeping medium due to the slight differences between the larger variation and the smaller variation for one extract, but it is the same for all samples that the lager variation of one extract examined was from Chinese liquor. Chinese liquor can dissolve more antioxidant compounds from, or it can promote the scavenging capacity of antioxidant compounds. FRAP assay is a direct method to determine the antioxidants of samples directly using antioxidants as reductants in a redox-linked colorimetric reaction to reduce ferric ions to ferrous ions (Benzie & Strain, 1999). The more ferric ions reduced, the more intense the blue color formed, which means the more antioxidants contained. The antioxidant capacity of samples in the experiment is determined by FRAP assay by spectrophotometer at 378C, the values are presented in Table 2. The variety and processed forms showed influences on FRAP values of marinated liquor. The FRAP values of the sliced white ranged from 0.28 to 0.43 mmol Fe 21 equivalents/100 g, 0.22 to 0.38 mmol Fe 21 equivalents/100 g for the powdered white, 0.56 to 1.19 mmol Fe 21 equivalents/100 g for the hair root of white, 0.26 to 0.42 for the ultrafine ground white, 0.12 to 0.85 mmol Fe 21 equivalents/100 g for the powdered red, 0.17 to 0.91 mmol Fe 21 equivalents/100 g for the ultrafine ground red. The highest FRAP value is from the hair root of white, the values of two forms of red are relative higher, and other three are comparably lower. ABTS method is used to measure the antioxidant capacities of foods by reduction of oxygen species and the blue color formed can be absorbed at 734 nm by spectrophotometer (Huang, Ou, & Prior, 2005). The results are presented in Table 2. The ABTS values are influenced by both varieties and steeping media. The sliced white ranged from 1.67 to 2.94 lmol TE/g, 1.17 to 2.21 lmol TE/g for the powdered white, 3.66 to 5.77 lmol TE/g for the hair root of white, 1.20 to 2.59 lmol TE/g for the ultrafine ground white, 2.66 to 4.02 lmol TE/g for the powdered red, 2.83 to 3.90 lmol TE/g for the ultrafine ground red. These data indicate that hair root of white has relatively higher ABTS values than others, others are comparably lower. 3.4 Significant differences by marinating media TPC from samples are presented in Table 3 in groups of four steeping media. It is obvious that TPC values steeped by yellow wine were relative lower than other three steeping media. Values of 3.58 vinegar, 98 vinegar, and Chinese liquor were comparable, but a few varies in varieties and processed forms of. The results suggest that yellow wine is not suitable to steep phenolic compounds from s. TFC values of six samples are significantly influenced by steeping media listed in Table 3. The yields of TFC by steeping media were in a descending order: Chinese liquor > Yellow wine > 98 vinegar > 3.58 vinegar. Among these four steeping media, TFC values from Chinese liquor extracts were very high, which were times of the values from other steeping media. Especially the extract of white hair root, the TFC value was up to lg CAE/g. The data indicate that Chinese liquor contributes the highest flavonoid compounds extraction, the contribution of yellow wine is moderate, and two vinegar media suppress the extraction of flavonoid content from s. The DPPH values of extracts were also affected by steeping media. The highest DPPH values were contributed by Chinese liquor. The values of 98 vinegar and yellow wine extracts were comparably lower than Chinese liquor but higher than 3.58 vinegar from sliced, powdered, hair root of white and powdered red. The lowest DPPH values obtained by 3.58 vinegar extracts of the sliced, powdered, hair root of white and the powdered red. The results suggest that Chinese liquor is the best medium to extract more antioxidants for Chinese medicinal liquor, and 3.58 vinegar is the most undesirable medium among four steeping media. The FRAP values were significantly affected by steeping media. The FRAP values in yellow wine steeped sliced white, powdered white, ultrafine ground white were not detected. For other varieties and forms, their yellow wine extracts showed much lower FRAP values than other steeping media among one sample. Besides, Chinese liquor showed the highest FRAP for all samples, the values are around two times of values of 3.58 vinegar extracts. The values from two vinegars (3.58 and 98) were comparably lower than Chinese liquor. These results suggest that Chinese liquor provide the highest yields of among four steeping media for extracting FRAP from s, and yellow wine is not a good medium for FRAP extraction. Different steeping media affected the results of ABTS significantly since the relative large differences between the larger variation and the smaller variation among one sample steeped by four steeping media. The larger variations of all white extracts were from Chinese liquor, especially for white hair root, its Chinese liquor extract was up to 5.77 lmol TE/g, which was the highest ABTS value among all treatments. The 3.58 vinegar extracts were the second highest for white samples. For red samples, 3.58 vinegar extracts possessed the highest ABTS values. The results also suggest that Chinese liquor is desirable for total antioxidants marinating from s, while yellow wine is not a favorable medium of s for antioxidant steeping, since no ABTS had been detected in the yellow wine steeped liquid of white hair root, ultrafine ground white, powdered red, and ultrafine ground red. The TSC results of the liquors are presented in Table 3 in groups of four media. The values were influenced by steeping media in a descending order: Chinese liquor > 98 vinegar > 3.58 vinegar > yellow

6 6 of 7 ZHANG AND XU TABLE 3 Significant difference analyses for the different forms among the same marinating media TPC TFC DPPH FRAP ABTS TSC (mg GAE/g) (lg CAE/g) (lmol TE/g) (mmol Fe 21 E/100g) (lmol TE/g) (mg SBaE/g) 3.58 Vinegar Sliced white a b bc b b e Powdered white b a a a a c White hair root a bc d e d f white c c bc c c d Powdered red a d b bc d a red a e d d d b 98 Vinegar Sliced white c a d a b d Powdered white ab b b a a b White hair root a c e c d c white bc c a a a b Powdered red ab d c b c a red c e b b e b Yellow wine Sliced white b b b NA e Powdered white a b a NA d White hair root a a d c NA f white c c a NA NA c Powdered red b d c a NA a red ab e a b NA b Chinese liquor Sliced white c b b a d c Powdered white ab a a a a a White hair root a e d d e f white b ab ab a b d Powdered red ab c c b d b red c d c c c e Results are expressed as mean 6 standard deviation of two replicates. Values marked by the same later are not significantly (p.05) difference. wine for sliced, powdered, ultrafine ground white, powdered, ultrafine ground red. All the highest TSC values are contributed by Chinese liquor extracts, especially in the hair root of white which is up to mg SBa/g. The results suggest that Chinese liquor is the best for saponin steeping, while yellow wine suppresses the extraction which is an undesirable medium. The results of s in Table 3 are grouped by four different marinating media, all data indicate that Chinese liquor is the most favorable marinating media for steeping, and yellow wine is the most undesirable one. The differences in compositions of two marinating media are considered as the main reason why their results are significantly different. Chinese liquor used in this study is 538, it contains 53% ethanol. The ethanol content of yellow wine is 14%, which is much lower than the Chinese liquor. Ethanol is a favorable solvent with a strong penetrating and diffusion ability; it is commonly used in extraction work. Chinese liquor with higher ethanol content is more easily to steep chemicals than yellow wine. In addition, yellow wine has higher polysaccharides content than Chinese liquor. Polysaccharides in yellow wine may suppress the antioxidant substances dissolving out from s. Both of two kinds of vinegars have no big contribution for steeping according to comparably low values in Table 3. The phenolics and antioxidants of 98 vinegar are relative higher than that of 3.58 vinegar. These data indicate marinating media with higher acidity may not help some certain chemicals dissolving out from s. 4 CONCLUSION The results clearly showed that significant differences in antioxidant properties, phenolic and saponin profiles of s marinated by different media. The most desirable solvent was Chinese liquor for TFC, DPPH, FRAP, and TSC. Chinese liquor and vinegar were relative favorable for ABTS extraction. Yellow wine is the most undesirable medium for TPC, DPPH, FRAP, ABTS, and TSC. Two forms of red materials showed significant higher TFC than white s. More researches are needed to figure out how the antioxidants from s contribute to health promotion effects. ACKNOWLEDGMENTS This research was jointly supported by two research grants (UICRG and UICRG ) from Beijing Normal University- Hong Kong Baptist University United International College, China.

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