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Journal of the East Asian Society of Dietary Life - Vol. 33 , No. 5
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Journal of the East Asian Society of Dietary Life - Vol. 33, No. 5, pp. 415-421
Abbreviation: J East Asian Soc Diet Life
ISSN: 1225-6781 (Print) 2288-8802 (Online)
Print publication date 31 Oct 2023
Received 15 Sep 2023 Revised 20 Oct 2023 Accepted 23 Oct 2023
DOI: https://doi.org/10.17495/easdl.2023.10.33.5.415

Changes of Ginsenoside Compositions in Cultivated Wild Ginseng with Different Steaming Temperatures and Time
Gyo-Nam Kim†
Professor, Dept. of Pharmaceutical Engineering, Kyungnam University, Changwon 51767, Republic of Korea

Correspondence to : †Gyo-Nam Kim, Tel: +82-55-249-6330, Fax: +82-505-999-2104, E-mail: gnkim@kyungnam.ac.kr

Abstract

This study was conducted to investigate changes in the ginsenoside compositions of cultivated wild ginseng caused by steaming at different temperatures (95, 117, 126, and 132℃) and times (10, 30, 50, 70, 90, 110, and 130 min). On increasing steaming temperatures from 95 to 132℃, levels of protopanaxadiol (PPD) ginsenosides Rg3, Rk1, and Rg5 increased from 0.69, 1.11, and 1.79 mg/g to 4.08, 5.16, and 8.98 mg/g, respectively, whereas levels of protopanaxatriol (PPT) ginsenosides Re, Rf, Rg6, F4, Rk3, and Rh4 increased from 2.04, 0.79, 0.53, 0.77, 0.53, and 0.52 mg/g to 2.44, 2.50, 1.83, 2.74, 1.39, and 1.72 mg/g, respectively. Furthermore, amounts of total PPD ginsenosides and total ginsenosides increased on increasing temperature, and total PPT ginsenoside amounts peaked at 126℃. In addition, when the steaming time was increased from 10 to 70 min, amounts of PPD ginsenosides Rg3, Rk1, and Rg5 increased 2.06, 1.90, and 1.89-fold, respectively, and amounts of PPT ginsenosides Rf, Rg6, F4, Rk3, and Rh4 increased 1.22, 1.44, 1.66, 1.61, and 1.95-fold, respectively. However, levels of total PPT ginsenosides and total ginsenosides peaked at a steaming time of 10 min.

Keywords: cultivated wild ginseng, ginsenosides, steaming temperature, steaming time
INTRODUCTION

Panax ginseng C.A. Meyer (Araliaceae) is commonly known as Korean ginseng. It is one of the most widely used tonic to enhance immune response and consequently improve health and longevity for over 2000 years in Oriental countries (Patel S & Rauf A 2017). Mountain wild ginseng is found in the natural environment of mountainous regions, whereas cultivated wild ginseng is grown in forests and mountains to mimic mountain wild ginseng. However, mountain wild ginseng is considered superior to regular cultivated ginseng as it contains higher amounts of certain ginsenosides. Furthermore, ginsenoside levels have been found to be consistently lower in more intensively cultivated crops, although their growth is consistently higher (Lim W et al 2005). Generally, cultivated ginseng is systematically cultivated on land and harvested after 4—6 years of cultivation, whereas cultivated wild ginseng grows in the wild or deep in mountains, making it difficult to harvest. Their different growth environments can lead to differences in several functional compounds and pharmacological effects (Yu GJ et al 2015). It has been reported that cultivated wild ginseng is more effective than cultivated ginseng in terms of efficacy. Its ginsenoside content is also higher than that of cultivated ginseng. Cultivated wild ginseng is also known to be effective against cancer, hypotension, oxidants, hepatotoxicity, and lipid weakening (Kim YJ & Son DY 2012). To date, nearly two hundred ginsenosides have been isolated and identified from various tissues of ginseng plants (Chen W et al 2019). Based on chemical structures of aglycones moieties, ginsenosides are mainly divided into protopanaxadiol (PPD) type ginsenosides (such as Rb1, Rb2, Rc, Rd, Rg3, and so on) and protopanaxatriol (PPT) type ginsenosides (such as Rg1, Re, Rg2, Rh1, and so on).

Heat treatment is the most widely used method for preserving and extending the shelf-life of food products and nutritional supplements. This treatment can improve biological activity and ginsenoside content of ginseng. However, some naturally occurring nutrients can be lost during thermal processing because most bioactive compounds are relatively unstable to heat (Banga JR et al 2003; Awuah GB et al 2007). Thermally processed foods, especially fruits and vegetables, show increased biological activities compared with fresh foods owing to the chemical changes that occur during heat treatment (Ryley J & Kajda P 1994). Especially, steaming is known to induce a structural change in ginsenoside and enhance biological activities of ginseng (Yang SJ et al 2006; Kim KY et al 2007). These steaming procedures can transform major ginsenosides including Rb1, Rb2, Rc, Rd, Re, and Rg1 into minor ginsenosides including Rg3, Rk1, Rg5, and F2. Characteristic compounds in red and black ginseng have potential biological activities including anticancer, antidiabetic, neuroprotective, and anti-inflammatory activities (Chen J et al 2008; Kang KS et al 2008; Sun BS et al 2009; Yayeh T et al 2012; Kim JH et al 2016). Therefore, the objective of this study was to investigate changes in ginsenoside compositions of cultivated wild ginseng induced by steaming processing at different steaming temperatures and time.

MATERIALS AND METHODS
1. Materials

Five-year-old cultivated wild ginseng roots was collected on August 5, 2019 in the experimental field of Jinsaengbio Farm Association Co., Hamyang-gun, Gyeongnam, South Korea. Standards of ginsenosides Rb1, Rg1, Re, Rf, Rh1, Rc, Rb2, Rd, Rg6, F4, Rk3, Rh4, Rg3, Rk1, and Rg5 were purchased from Ambo Institute (Daejeon, Korea). Acetonitrile and high-performance liquid chromatography (HPLC) grade water were purchased from J.T. Baker (Phillipsburg, NJ, USA). A solid-phase extraction (SPE) column (Agilent, Bond Elut Plexa Cartridge 6 mL/200 mg, CA, USA) was used to purify and concentrate samples. All other chemicals used were of analytical grade.

2. Sample Preparation

Main roots of cultivated wild ginseng were washed with tap water to remove soil and other debris. Raw cultivated wild ginseng was then dried at 40℃ in a forced convection oven (LID-1904S, L'equip Co., Korea) or 6 hrs until the final moisture content was less than 30%. Dried cultivated wild ginseng was then steamed at 95℃ for 1.5 h using an autoclave (HK-AC60, Hankuk S&I Co., Korea). After cooling to room temperature, the autoclaved cultivated wild ginseng was dried again at 60℃ for 3 hrs in a forced convection drying oven. After secondary drying, autoclaved cultivated wild ginseng was steamed for 30 minutes at 95℃ (0 kfg/cm2), 117℃ (1.0 kfg/cm2), 126℃ (1.5 kfg/cm2), or 132℃ (2.0 kfg/cm2) using an autoclave and then dried at 60℃ for 3 hours to prepare cultivated wild ginseng samples with different steaming temperatures. To prepare cultivated wild ginseng samples with different steaming time, cultivated wild ginseng was first dried in the same way and then steamed for 10 to 130 minutes under the condition of 132℃ using an autoclave and then dried at 60℃ for 3 hrs.

3. Analysis of Ginsenosides
1) Extraction

Steamed cultivated wild ginseng was dried at 50℃. Dried cultivated wild ginseng was ground to 20—30 mesh and refluxed with 10 volumes (v/w) of hot water at 80℃ for 3 h. After reflux, the extract was filtered twice and concentrated at 55℃. The concentrate was then freeze-dried and stored at —75℃ until used.

2) SPE Column Purification

SPE was performed using a Varian Vac Elute SPS 24 vacuum manifold (Varian Inc., Walnut Grove, CA, USA). The SPE cartridge (Agilent, Bond Elut Plexa Cartridge 6 mL/200 mg, CA, USA) was conditioned with 6 mL of methanol and 6 mL of water before introducing sample solution. A 1.0 mL aliquot of the sample solution was introduced into the SPE cartridge at a flow rate of 0.1 mL/min. A washing step was then performed with 1.0 mL of ultra-pure water at the same flow rate. Retained analytes were eluted with 1.0 mL of methanol at a flow rate of 0.08 mL/min. The eluate solution was filtered through a 0.22 μm filter prior to analysis.

3) Determination of Ginsenosides by HPLC

Ginsenosides were determined using the method described by Dong H et al (2011) with slight modifications. Analyses were performed using an Agilent 1260 liquid chromatograph (Hewlett Packard, Wilmington, NC, USA) equipped with a quaternary gradient pump and multiple wavelength detector operating at 203 nm. Samples were separated on a Zorbax Eclipse XDB-C18 column (4.6 mm × 150 mm, 5 μm; Agilent Technologies, Inc. CA, USA) at 35℃ with a sample injection volume of 10 μL. The mobile phase consisted of a gradient of water (A) and acetonitrile (B). The following gradient was used: 20% B (0 min), 20% (0—10 min), 32% (10—40 min), 50% (40—55 min), 65% (55—70 min), 90% (70—82 min), and 80% (82—90 min). Data analysis was performed using a Chemstation software (Hewlett Packard). The flow rate of the mobile phase was set at 0.9 mL/min. Stock solutions of ginsenosides Rb1, Rg1, Re, Rf, Rh1, Rc, Rb2, Rd, Rg6, F4, Rk3, Rh4, Rg3, Rk1, and Rg5 were prepared in methanol. A series of standard operating solutions of different concentrations were obtained by diluting standard stock solutions.

4. Statistical Analysis

Experimental data were subjected to analysis of variance (ANOVA). Significant differences between mean values as determined from measurements carried out in five replicate tests (i.e., p<0.05) were obtained by Duncan’s multiple-range test using statistical analysis software (SPSS 20.0, IBM Inc., NY, USA).

RESULTS AND DISCUSSION
1. Changes of Ginsenosides in Cultivated Wild Ginseng Induced by Steaming Processing at Different Steaming Temperatures

Changes in ginsenoside compositions of cultivated wild ginseng induced by steaming processing at different steaming temperatures are shown in Table 1. Ginsenoside compositions varied significantly with steaming temperature. With increasing temperature, levels of PPD ginsenosides Rc, Rb2, and Rd decreased from 3.88, 4.10, and 3.12 mg/g to 1.78, 1.57, and 2.63 mg/g, respectively. In contrast, levels of ginsenosides Rg3, Rk1, and Rg5 increased from 0.69, 1.11, and 1.79 mg/g to 4.08, 5.16, and 8.98 mg/g, respectively, with increasing temperature. However, ginsenoside Rb1 was not detected at any steaming temperature. The level of ginsenoside Rg5 was the highest at 8.98 mg/g when the steaming temperature was 132℃. It increased with increasing steaming temperature. On the other hand, levels of PPT ginsenosides Rg1 and Rh1 only decreased from 4.01 and 7.39 mg/g to 1.28 and 5.86 mg/g, respectively, with increasing temperature. In contrast, levels of ginsenosides Re, Rf, Rg6, F4, Rk3, and Rh4 increased from 2.04, 0.79, 0.53, 0.77, 0.53, and 0.52 mg/g to 2.44, 2.50, 1.83, 2.74, 1.39, and 1.72 mg/g, respectively, with increasing temperature. Although ginsenoside Rh1 was decreased with increasing temperature, among PPT ginsenosides, ginsenoside Rh1 showed the highest content at 5.86 mg/g when the steaming temperature was 132℃. Moreover, amounts of total PPD ginsenosides and total ginsenosides were increased with increasing temperature. Levels of total PPD ginsenosides and total ginsenosides were 24.20 and 43.94 mg/g at 132℃, respectively. However, the amount of total PPT ginsenosides was the highest with a content of 21.30 mg/g at 126℃. This result was consistent with results of Wang D et al (2012) & Xiong Y et al (2019). Changes of chemical composition and content can be extrapolated from chemical structure. Under a steaming condition, the sugar chain at C-20 of ginsenosides Rb1 and Rd could be easily and selectively eliminated to produce ginsenoside 20(S)/(R)-Rg3 and ginsenoside Rg3 at C-20 could be dehydrated to yield ginsenosides Rg5 and Rk1 (Huang X et al 2019). Ginsenosides Rg1 and Re are likely to first lose a glycosyl moiety at C-20 and subsequently its terminal sugar unit at C-6 to form ginsenosides Rg2 and/or Rh1. Ginsenoside Rh1 is further converted to Rk3 and Rh4 through dehydration at C-20 (Sun S et al 2011). Additionally, Kim WY et al (2000) have reported the structural change in ginsenosides during red ginseng manufacturing with decreased levels of ginsenosides Rb1, Rb2, Rc, Rd, and Rg1 but increased levels of ginsenosides Rf, Rg3, and Rg5 after steaming.

Table 1. 
Contents of ginsenosides in cultivated wild ginseng induced by steaming processing at different steaming temperatures
Ginsenosides
(mg/g)		 Steaming temperature and pressure, ℃ (kfg/cm2)
95 (0) 117 (1) 126 (1.5) 132 (2)
20(S)-protopanaxadiol (PPD) groups
Rb1 -1) - - -
Rc 3.88±0.31b 6.09±0.30a 3.16±0.04c 1.78±0.07d
Rb2 4.10±0.51a 2.71±0.06b 2.66±0.06b 1.57±0.08c
Rd 3.12±0.04a 2.93±0.25ab 2.77±0.16bc 2.63±0.17c
Rg3 0.69±0.05d 1.80±0.04c 3.08±0.04b 4.08±0.13a
Rk1 1.11±0.17d 2.52±0.07c 3.80±0.12b 5.16±0.09a
Rg5 1.79±0.07d 4.52±0.24c 6.85±0.36b 8.98±0.18a
20(S)-protopanaxadiol (PPD) groups
Rg1 4.01±0.14a 3.98±0.02a 2.19±0.05b 1.28±0.07c
Re 2.04±0.06b 2.58±0.08a 2.50±0.03a 2.44±0.18a
Rf 0.79±0.02d 1.05±0.03c 2.26±0.04b 2.50±0.07a
Rh1 7.39±0.29b 8.71±0.49a 7.82±0.12b 5.86±0.33c
Rg6 0.53±0.29d 1.20±0.01c 1.48±0.01b 1.83±0.04a
F4 0.77±0.10d 1.72±0.02c 2.22±0.03b 2.74±0.03a
Rk3 0.53±0.02d 0.84±0.01c 1.26±0.01b 1.39±0.02a
Rh4 0.52±0.03d 0.93±0.01c 1.57±0.02b 1.72±0.03a
Total PPD 14.70±0.85d 20.57±0.69c 22.32±0.59b 24.20±0.49a
Total PPT 16.55±0.19c 21.03±0.50a 21.30±0.27a 19.74±0.63b
Total content 31.25±0.94c 41.60±1.17b 43.62±0.82a 43.94±0.93a
PPD/PPT ratio 0.89±0.05d 0.98±0.01c 1.05±0.02b 1.23±0.04a
Values are presented as mean±S.D. (n=5).
a—d Different superscripts within a row indicate significant differences at p<0.05.
1) Not detected (limit of detection: 0.1 mg/g).

2. Changes of Ginsenosides in Cultivated Wild Ginseng Induced by Steaming Processing with Different Steaming Time

Changes in ginsenoside compositions of cultivated wild ginseng induced by steaming processing at different steaming time are shown in Table 2. Among PPD ginsenosides, ginsenoside Rb1 was not detected with any steaming time. Levels of ginsenosides Rc, Rb2, and RD were decreased when the steaming time was increased. Ginsenosides Rc and Rb2 were not detected after 50 min of steaming. Ginsenoside Rd was not detected after 90 min of steaming. In contrast, levels of ginsenosides Rg3, Rk1, and Rg5 were increased until steaming time of 70 min. They were then decreased thereafter. At 70 min of steaming time, levels of ginsenosides Rg3, Rk1, and Rg5 were 6.22, 7.81, and 14.12 mg/g, respectively. In particular, levels of ginsenosides Rg3, Rk1, and Rg5 were increased by 2.06, 1.90, and 1.89 folds, respectively, after 70 min of steaming compared to those after 10 min of steaming. For PPT ginsenosides, levels of ginsenosides Rg1 and Re were decreased when steaming time was increased, whereas Rh1 level was decreased, increased, and then decreased again. In contrast, levels of ginsenosides Rf, Rg6, F4, Rk3, and Rh4 were increased until the steaming time was 70 min. They were then decreased thereafter. After 70 min of steaming, levels of ginsenosides Rf, Rg6, F4, Rk3, and Rh4 were 2.66, 2.41, 3.92, 2.05, and 2.97 mg/g, respectively. The level of total PPD ginsenosides was 29.01 mg/g after 70 min of steaming, while levels of total PPT ginsenosides and total ginsenosides were 25.68 and 53.19 mg/g after 10 min of steaming. Moreover, levels of ginsenosides Rf, Rg6, F4, Rk3, and Rh4 were increased by 1.22, 1.44, 1.66, 1.61, and 1.95 folds, respectively, after 70 min of steaming compared to those after 10 min of steaming. Results of this study are consistent with those of Wang CZ et al (2004). They reported that levels of ginsenosides Rg1, Re, Rb1, Rc, Rb2, Rb3, and Rd appeared to decrease after steaming, whereas those of ginsenosides Rg3 were increased after steaming. An increase in saponin content of steamed ginseng might be explained by pyrolysis of malonyl ginsenoside, producing aglycones of diol-series saponins (Ryu GH 2007). In addition, Park IH et al (2002) have isolated three new dammarane glycosides (ginsenosides Rk1, Rk2, and Rk3) from heat-processed ginseng. Chen W et al (2020) have investigated ginsenoside changes in black ginseng leaf products and suggested that polar PPD-type ginsenosides (Rb1, Rb2, Rc, Rd, etc.) are more likely to be converted to ginsenosides Rk1 and Rg5 by dehydration from Rg3 and to ginsenosides Rk2 and Rh3 through losing an H2O from Rh2 than to be completely degraded to aglycones PPD during a heat process. Furthermore, the levels of total PPD ginsenosides and total PPT ginsenosides were decreased after 90 min of steaming. Xie YY et al (2012) reported that the concentration of polar ginsenosides such as Rb1, Rb2, Rb3, Rd, Re, Rg1, and Rf decreases, while that of non-polar ginsenosides such as ginsenosides Rg3, Rh2, compound K, Rh3, Rh4, Rk1, Rk2, Rk3, and Rg5 increases during steaming. Therefore, the reduction in PPD and PPT ginsenoside content after a heating time of 90 minutes may be attributed to the conversion of polar ginsenosides to non-polar ginsenosides and transformation to unmeasured ginsenosides occurred.

Table 2. 
Contents of ginsenosides in cultivated wild ginseng induced by steaming processing after different steaming time
Ginsenosides
(mg/g)		 Steaming time (min) at 132℃ (2.0 kfg/cm2)
10 30 50 70 90 110 130
20(S)-protopanaxadiol (PPD) groups
Rb1 -1) - - - - - -
Rc 5.47±0.11a 2.03±0.07b 0.81±0.06c - - - -
Rb2 4.03±0.16a 1.11±0.05b 0.74±0.09c - - - -
Rd 3.39±0.14a 1.81±0.11b 1.43±0.15c 0.86±0.05d 0.70±0.06e - -
Rg3 3.02±0.04e 4.86±0.09c 5.36±0.11b 6.22±0.32a 4.83±0.40c 3.99±0.05d 4.58±0.04c
Rk1 4.12±0.04g 5.89±0.09e 6.92±0.12b 7.81±0.09a 6.68±0.05c 5.76±0.06f 6.38±0.04d
Rg5 7.48±0.07e 10.59±0.18d 12.43±0.22b 14.12±0.19a 12.32±0.11bc 10.65±0.10d 12.13±0.10c
20(S)-protopanaxatriol (PPT) groups
Rg1 3.53±0.05a 1.44±0.06c - 1.80±0.08b 1.03±0.05d 0.93±0.06e 0.87±0.02e
Re 3.09±0.03a 2.60±0.15b 1.97±0.08c 1.97±0.04c 1.48±0.02d 1.20±0.06e 1.19±0.06e
Rf 2.18±0.05b 1.78±0.14c 1.20±0.04e 2.66±0.09a 1.82±0.06c 1.39±0.07d 1.29±0.06de
Rh1 10.06±0.23a 4.11±0.18b 0.80±0.04f 3.22±0.12c 2.86±0.14d 2.34±0.20e 2.71±0.12d
Rg6 1.67±0.02d 2.17±0.03b 2.40±0.04a 2.41±0.03a 1.97±0.02c 1.61±0.01e 1.53±0.01f
F4 2.36±0.04f 3.42±0.05c 3.72±0.06b 3.92±0.05a 3.01±0.02d 2.57±0.01e 2.37±0.01f
Rk3 1.27±0.01f 1.42±0.02e 1.55±0.02d 2.05±0.03a 1.82±0.01b 1.41±0.01e 1.70±0.01c
Rh4 1.52±0.01f 1.76±0.02e 2.06±0.03d 2.97±0.03a 2.84±0.02b 2.12±0.02c 2.87±0.02b
Total PPD 27.51±0.18b 26.29±0.44c 27.69±0.52b 29.01±0.57a 24.53±0.54d 20.40±0.19f 23.08±0.17e
Total PPT 25.68±0.32a 18.69±0.21c 13.69±0.18f 21.00±0.21b 16.83±0.26d 13.55±0.30f 14.51±0.21e
Total content 53.19±0.47a 44.98±0.38c 41.38±0.69d 50.01±0.59b 41.36±0.80d 33.95±0.40f 37.59±0.26e
PPD/PPT ratio 1.07±0.01f 1.40±0.03e 2.02±0.02a 1.38±0.03e 1.46±0.01d 1.51±0.03c 1.59±0.03b
Values are presented as mean±S.D.(n=5).
a—g Different superscripts within a row indicate significant differences at p<0.05.
1) Not detected (limit of detection: 0.1 mg/g).

SUMMARY AND CONCLUSIONS

In conclusion, results of this study indicated that steaming process had a positive influence on changes of ginsenoside compositions in cultivated wild ginseng. With increases of steaming temperature and steaming time, levels of PPD ginsenosides (Rg3, Rk1, and Rg5), PPT ginsenosides (Re, Rf, Rg6, F4, Rk3, and Rh4), total PPD ginsenosides, and total ginsenosides were increased until a heating time of 70 minutes. Amounts of PPD ginsenosides (Rg3, Rk1, and Rg5), PPT ginsenosides (Rf, Rg6, F4, Rk3, and Rh4), and total PPD ginsenosides were the higher after 70 min of steaming than those after 10 min of steaming. However, levels of total PPT ginsenosides and total ginsenosides were higher after 10 min of steaming. As a result, it was concluded that the most effective steaming temperature and time for cultivated wild ginseng is a heating temperature of 132℃ (2.0 kfg/cm2) for 70 minutes, during which the highest ginsenoside content was achieved. Results of the present study suggest that the steaming process could be used to develop value-added cultivated wild ginseng products and red ginseng.

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