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molecules
Article
Analysis of Ginsenoside Content (Panax ginseng)
from Different Regions
Wei Chen 1,2,3 , Prabhu Balan 2,3 and David G Popovich 1,*
1School of Food and Advanced Technology, Massey University, Palmerston North 4442, New Zealand;
W.Chen2@massey.ac.nz
2Riddet Institute, Massey University, Palmerston North 4442, New Zealand; P.Balan@massey.ac.nz
3Alpha-Massey Natural Nutraceutical Research Centre, Massey University,
Palmerston North 4442, New Zealand
*Correspondence: D.G.Popovich@massey.ac.nz; Tel.: +64-63569099
Academic Editor: Vincenzo De Feo
Received: 3 September 2019; Accepted: 25 September 2019; Published: 26 September 2019
Abstract:
Recently Panax ginseng has been grown as a secondary crop under a pine tree canopy in
New Zealand (NZ). The aim of the study is to compare the average content of ginsenosides from
NZ-grown ginseng and its original native locations (China and Korea) grown ginseng. Ten batches of
NZ-grown ginseng were extracted using 70% methanol and analyzed using LC-MS/MS. The average
content of ginsenosides from China and Korea grown ginseng were obtained by collecting data from
30 and 17 publications featuring China and Korea grown ginseng, respectively. The average content
of total ginsenosides in NZ-grown ginseng was 40.06
±
3.21 mg/g (n =14), which showed significantly
(p<0.05) higher concentration than that of China grown ginseng (16.48
±
1.24 mg/g, n =113) and
Korea grown ginseng (21.05
±
1.57 mg/g, n =106). For the individual ginsenosides, except for the
ginsenosides Rb2, Rc, and Rd, ginsenosides Rb1, Re, Rf, and Rg1 from NZ-grown ginseng were 2.22,
2.91, 1.65, and 1.27 times higher than that of ginseng grown in China, respectively. Ginsenosides Re
and Rg1 in NZ-grown ginseng were also 2.14 and 1.63 times higher than ginseng grown in Korea.
From the accumulation of ginsenosides, New Zealand volcanic pumice soil may be more suitable for
ginseng growth than its place of origin.
Keywords: Panax ginseng; ginsenosides; New Zealand; China; Korea
1. Introduction
Panax ginseng, as one of the most important medicinal plant, root was used for first aid, health care,
and the treatment of coma, gastrointestinal disease, and cardiovascular disease in ancient China [
1
].
Pharmacological studies found ginseng possesses diverse bioactive effects, such as anti-aging, anti-stress,
anti-tumor, anti-inflammatory, and anti-diabetes [
2
]. It has a beneficial impact on brain function, liver
function, immune function, and sexual function [
3
]. Since the use of traditional Chinese herbs for
medicinal and dietary purposes is becoming increasingly popular in Western countries, ginseng is
becoming one of the best-selling herbs in the world [4].
Ginsenosides are known as the key active ingredient of ginseng [
2
]. The diversity of ginseng
efficacy is related to the structural variability of ginsenosides, also known as triterpenoid saponins [
5
].
More than a hundred ginsenosides have been reported in Panax ginseng [
6
]. Among them, ginsenosides
Rb1, Rb2, Rc, Rd, Re, Rg1 (chemical structures are shown in Figure 1) are the most abundant and are
usually regarded as the main ginsenosides. These six ginsenosides are normally used to evaluate
ginsenoside abundance and for quality control. The accumulation of ginsenosides in ginseng is variable
and can be influenced by the surrounding environment, including soil fertility, temperature, light, and
Molecules 2019,24, 3491; doi:10.3390/molecules24193491 www.mdpi.com/journal/molecules
Molecules 2019,24, 3491 2 of 11
humidity [
7
]. Even in the same area, the type and amount of ginsenosides are dependent on ginseng
age [
8
], harvest time [
9
], and storage process [
10
]. Since ginseng’s bioactive properties depend largely
on the contents and types of ginsenosides, accurately knowing the amount of ginsenosides is not only
important for the pharmacological evaluation of ginseng products, but also for assessing the quality of
ginseng from different regions.
Molecules 2019, 24, x FOR PEER REVIEW 2 of 12
temperature, light, and humidity [7]. Even in the same area, the type and amount of ginsenosides are
dependent on ginseng age [8], harvest time [9], and storage process [10]. Since ginseng’s bioactive
properties depend largely on the contents and types of ginsenosides, accurately knowing the amount
of ginsenosides is not only important for the pharmacological evaluation of ginseng products, but
also for assessing the quality of ginseng from different regions.
Figure 1. The chemical structures of main ginsenosides. Glc, Arap, Araf, and Rha refer to β-D-
glucopyranosyl, α-L-arabinopyranosyl, α-L-arabinofuranosyl, and α-L-rhamnopranosyl,
respectively.
With the increasing popularity of ginseng around the world, ginseng is also cultivated outside
its place of origin (Northeast China, and Korea). Recently ginseng has been grown in New Zealand
(NZ). NZ has a unique geographical environment, such as the volcanic pumice soil, high-intensity
UV rays, and open-wild environment. NZ-grown ginseng showed abundant ginsenosides in the
underground parts (roots, rootlets) and above ground parts (stem and leaf) based on our previous
study [11]. To compare the average amount of ginsenosides between NZ-grown ginseng and ginseng
grown in China and Korea, we analyzed the amount of ginsenosides in different batches of ginseng
grown in NZ under a pine forest canopy and compared it to published data. Thus, this paper not
only provides the information about the differences of ginsenoside content in ginseng from different
places of origin, but it also provides a reference data for the saponin content from ginseng produced
in different areas. To our knowledge, this is the first article focusing on ginsenoside content in
different regions.
2. Results and Discussion
2.1. The Ginsenoside Contents of NZ-Grown Ginseng
In this study, the amount of 21 ginsenosides in 10 batches of ginseng samples were analyzed
using LC-MS/MS described in our previous method [11]. Briefly, thirteen ginsenosides (Rb1, Rb2,
Rb3, Rc, Rd, Re, Rf, Rg1, Rg2, Rg3, Rh1, Rh2, and F2) were accurately quantified by their own linear
regression equations of standard curves, and some ginsenosides without reference standards, such
as ginsenosides m-Rb1 (m = malonyl), m-Rb2, m-Rb3, m-Rc, m-Rd, m-Re, and m-Rg1, were relatively
quantified by the regression equations of their corresponding neutral ginsenosides. As shown in
Table 1, apart from the individual ginsenoside content, the total ginsenoside amount, the ratio of
protopanaxadiol (PPD)-type to protopanaxatriol (PPT)-type (PPD/PPT) and the ratio of neutral
ginsenoside to malonyl ginsenoside (G/m-G) are also described in this section.
Among those samples, the ginsenoside concentrations were varied. The highest amount (102.69
± 0.91 mg/g) and the lowest amount (38.72 ± 0.15 mg/g) were from the third batch and fifth batch of
samples, respectively. Ginsenosides Rg1, Rb1, m-Rb1, and Re are the four major ginsenosides in most
samples except the fourth and fifth batches of samples, while in the fourth and fifth batches of
samples, the major ginsenosides give way to the ginsenosides m-Rb1, m-Rb2, m-Rc, and Rg1 based
on their concentrations. The high amount of m-Rb1, m-Rb2, and m-Rb3 lead to the higher ratios of
Figure 1.
The chemical structures of main ginsenosides. Glc, Arap, Araf,
and Rha refer to
β
-D-glucopyranosyl,
α
-L-arabinopyranosyl,
α
-L-arabinofuranosyl, and
α-L-rhamnopranosyl, respectively.
With the increasing popularity of ginseng around the world, ginseng is also cultivated outside
its place of origin (Northeast China, and Korea). Recently ginseng has been grown in New Zealand
(NZ). NZ has a unique geographical environment, such as the volcanic pumice soil, high-intensity
UV rays, and open-wild environment. NZ-grown ginseng showed abundant ginsenosides in the
underground parts (roots, rootlets) and above ground parts (stem and leaf) based on our previous
study [
11
]. To compare the average amount of ginsenosides between NZ-grown ginseng and ginseng
grown in China and Korea, we analyzed the amount of ginsenosides in different batches of ginseng
grown in NZ under a pine forest canopy and compared it to published data. Thus, this paper not only
provides the information about the differences of ginsenoside content in ginseng from different places of
origin, but it also provides a reference data for the saponin content from ginseng produced in different
areas. To our knowledge, this is the first article focusing on ginsenoside content in different regions.
2. Results and Discussion
2.1. The Ginsenoside Contents of NZ-Grown Ginseng
In this study, the amount of 21 ginsenosides in 10 batches of ginseng samples were analyzed using
LC-MS/MS described in our previous method [
11
]. Briefly, thirteen ginsenosides (Rb1, Rb2, Rb3, Rc,
Rd, Re, Rf, Rg1, Rg2, Rg3, Rh1, Rh2, and F2) were accurately quantified by their own linear regression
equations of standard curves, and some ginsenosides without reference standards, such as ginsenosides
m-Rb1 (m =malonyl), m-Rb2, m-Rb3, m-Rc, m-Rd, m-Re, and m-Rg1, were relatively quantified by the
regression equations of their corresponding neutral ginsenosides. As shown in Table 1, apart from the
individual ginsenoside content, the total ginsenoside amount, the ratio of protopanaxadiol (PPD)-type
to protopanaxatriol (PPT)-type (PPD/PPT) and the ratio of neutral ginsenoside to malonyl ginsenoside
(G/m-G) are also described in this section.
Molecules 2019,24, 3491 3 of 11
Table 1. The content (mg/g) of ginsenosides in 10 batches of New Zealand (NZ)-grown ginseng samples (mean ±SD).
Compound Ginseng Samples
12345678910
Rg1 9.25 ±0.15 8.49 ±0.00 14.56 ±0.17 6.93 ±0.00 3.22 ±0.02 14.01 ±0.06 15.54 ±0.04 8.17 ±0.30 12.79 ±0.03 9.16 ±0.10
Rf 2.41 ±0.09 2.79 ±0.05 4.01 ±0.09 2.01 ±0.01 1.07 ±0.01 3.13 ±0.00 4.13 ±0.08 2.76 ±0.01 3.05 ±0.08 3.25 ±0.02
Re 4.38 ±0.02 12.27 ±0.05 11.67 ±0.17 5.37 ±0.00 5.41 ±0.04 4.47 ±0.03 8.40 ±0.10 8.04 ±0.10 6.36 ±0.11 10.18 ±0.38
Rg2 0.41 ±0.00 0.89 ±0.00 0.89 ±0.02 0.12 ±0.00 0.40 ±0.00 0.33 ±0.00 0.69 ±0.01 0.67 ±0.00 0.46 ±0.01 0.87 ±0.01
Rh1 0.02 ±0.00 0.01 ±0.00 0.09 ±0.00 # # 0.06 ±0.00 0.11 ±0.00 0.03 ±0.00 0.07 ±0.00 0.05 ±0.00
Rb1 8.26 ±0.14 14.85 ±0.04 19.9 ±0.24 5.95 ±0.01 2.85 ±0.02 9.11 ±0.05 12.60 ±0.04 9.90 ±0.14 12.03 ±0.13 11.58 ±0.09
Rc 4.08 ±0.06 5.73 ±0.11 8.63 ±0.03 3.06 ±0.02 2.16 ±0.03 2.48 ±0.08 4.03 ±0.01 4.00 ±0.04 4.17 ±0.02 5.59 ±0.19
Rb2 3.45 ±0.01 4.57 ±0.00 8.19 ±0.01 2.87 ±0.03 1.80 ±0.01 2.20 ±0.06 3.64 ±0.08 3.61 ±0.01 3.75 ±0.06 5.23 ±0.07
Rb3 0.77 ±0.02 1.06 ±0.01 1.69 ±0.03 0.51 ±0.03 0.36 ±0.03 0.47 ±0.02 0.83 ±0.01 0.80 ±0.05 0.79 ±0.01 1.10 ±0.02
Rd 0.73 ±0.00 0.80 ±0.00 1.74 ±0.02 1.31 ±0.02 0.93 ±0.00 0.78 ±0.01 1.90 ±0.03 0.75 ±0.01 0.78 ±0.00 1.07 ±0.04
Rh2 0.01 ±0.00 0.04 ±0.00 0.06 ±0.00 0.02 ±0.00 0.02 ±0.00 0.01 ±0.00 0.01 ±0.00 0.01 ±0.00 0.01 ±0.00 0.01 ±0.00
F2 0.01 ±0.00 0.02 ±0.00 0.01 ±0.00 0.02 ±0.00 0.03 ±0.00 # # 0.01 ±0.00 0.01 ±0.00 0.01 ±0.00
Rg3 0.01 ±0.00 0.01 ±0.00 0.03 ±0.00 0.01 ±0.00 0.01 ±0.00 0.01 ±0.00 0.02 ±0.00 0.01 ±0.00 0.01 ±0.00 0.02 ±0.00
Ro 3.18 ±0.02 2.09 ±0.01 2.80 ±0.02 3.40 ±0.02 0.57 ±0.01 2.81 ±0.00 2.60 ±0.03 1.08 ±0.00 2.96 ±0.00 1.06 ±0.02
m-Rg1 0.71 ±0.01 0.43 ±0.01 0.41 ±0.00 1.50 ±0.01 0.39 ±0.01 0.92 ±0.01 0.68 ±0.01 0.33 ±0.01 0.50 ±0.01 0.28 ±0.01
m-Re 0.14 ±0.00 0.29 ±0.01 0.14 ±0.00 0.38 ±0.00 0.25 ±0.01 0.07 ±0.00 0.09 ±0.00 0.11 ±0.00 0.08 ±0.00 0.10 ±0.00
m-Rd 1.12 ±0.01 1.25 ±0.02 1.47 ±0.01 3.75 ±0.07 1.91 ±0.01 0.98 ±0.02 2.02 ±0.02 0.88 ±0.01 0.92 ±0.01 1.24 ±0.02
m-Rb1 11.54 ±0.10 13.91 ±0.08 13.16 ±0.12 16.58 ±0.04 6.09 ±0.09 9.67 ±0.05 11.28 ±0.05 8.79 ±0.29 9.85 ±0.11 9.11 ±0.01
m-Rc 5.40 ±0.01 5.21 ±0.01 5.12 ±0.06 9.90 ±0.25 4.66 ±0.05 2.36 ±0.02 3.40 ±0.06 3.46 ±0.05 3.31 ±0.04 4.42 ±0.07
m-Rb2 6.89 ±0.05 5.79 ±0.06 6.96 ±0.07 12.87 ±0.10 5.69 ±0.04 2.69 ±0.00 3.76 ±0.02 4.05 ±0.06 3.98 ±0.01 5.65 ±0.02
m-Rb3 1.26 ±0.04 1.06 ±0.03 1.14 ±0.06 2.32 ±0.02 0.91 ±0.06 0.53 ±0.03 0.74 ±0.01 0.79 ±0.04 0.67 ±0.07 1.01 ±0.01
Total 64.02 ±0.22 81.57 ±0.16
102.69
±
0.91
78.88 ±0.33 38.72 ±0.15 57.08 ±0.18 76.47 ±0.14 58.28 ±0.68 66.57 ±0.25 70.99 ±0.96
PPD/PPT 2.51 ±0.00 2.16 ±0.02 2.14 ±0.01 3.63 ±0.00 2.55 ±0.01 1.36 ±0.02 1.49 ±0.01 1.84 ±0.02 1.73 ±0.01 1.93 ±0.02
G/m-G 1.14 ±0.00 1.71 ±0.00 2.34 ±0.01 0.55 ±0.00 0.84 ±0.00 1.95 ±0.00 2.14 ±0.00 1.92 ±0.01 2.11 ±0.02 2.01 ±0.03
# not quantified. The total ginsenoside amount is the sum of all the quantified ginsenosides. The protopanaxadiol (PPD)-type amount and protopanaxatriol (PPT)-type amount are the sum
of all the quantified PPD-type ginsenosides and PPT-type ginsenosides, respectively. G/m-G is the ratio of neutral ginsenoside amount to malonyl ginsenoside amount; the malonyl
ginsenoside amount is the sum of seven quantified malonyl ginsenosides (m-Re, m-Rg1, m-Rb1, m-Rb2, m-Rb3, m-Rc, and m-Rd), and the neutral ginsenoside amount is the sum of
corresponding neutral ginsenosides (Re, Rg1, Rb1, Rb2, Rb3, Rc, and Rd).
Molecules 2019,24, 3491 4 of 11
Among those samples, the ginsenoside concentrations were varied. The highest amount
(102.69
±
0.91 mg/g) and the lowest amount (38.72
±
0.15 mg/g) were from the third batch and
fifth batch of samples, respectively. Ginsenosides Rg1, Rb1, m-Rb1, and Re are the four major
ginsenosides in most samples except the fourth and fifth batches of samples, while in the fourth and
fifth batches of samples, the major ginsenosides give way to the ginsenosides m-Rb1, m-Rb2, m-Rc, and
Rg1 based on their concentrations. The high amount of m-Rb1, m-Rb2, and m-Rb3 lead to the higher
ratios of PPD/PPT and lower ratios of G/m-G in sample four and five. Both ratios are approximately
two from other samples.
Usually, ginseng refers to the whole ginseng root including the main root body, root hair, and
rhizome. In our previous study, we analyzed ginsenosides from different parts including main root,
fine root, rhizome, stem, and leaf [
11
], it was found that the underground parts, including main root,
fine root, and rhizome, have very similar ginsenoside composition. In this study ginsenosides were
determined from the whole underground part. There is another study reporting ginsenosides analysis
for NZ-grown ginseng [
12
], which only detected seven main ginsenosides in four batches of ginseng
samples. In order to compare with China and Korea grown ginseng, the data from Table 1and Follett’s
publication [12] are used to calculate the average content of ginsenosides of NZ-grown ginseng.
2.2. The Average Content of Ginsenosides in Different Regions
In order to obtain the average content of ginsenosides from China grown ginseng and Korea
grown ginseng, we searched the scientific literature for ginsenosides analysis from ginseng grown in
China and Korea. A total of 524 articles were located, and 151 potentially relevant studies were selected
to full-text review after removing the duplicates (N =230), abstract only (N =13) and screening on
the basis of title and abstract according to the inclusion criteria. After exclusion of 102 articles for
the reasons given in Figure 2, we included 49 articles (article lists are supplied in the Supplementary
Materials). Among these articles, 30 articles were about ginsenosides analysis for China grown ginseng,
17 for Korea grown ginseng, and two for NZ-grown ginseng.
After extracting the data from the inclusion articles, the amount of ginsenosides from 113 batches
of China grown ginseng roots aged from three to 30-years old was used to calculate the average content
of ginsenosides of China grown ginseng. A total of 106 batches of Korea grown ginseng roots with
different ages (one to 10-years old) were analyzed from 17 publications. For NZ-grown ginseng, there
were 14 batches of samples tests, including ten batches of ginseng roots in this study and four from
the literature.
As shown in Figure 3, the average content of total ginsenosides from NZ-grown ginseng
(40.06
±
3.21 mg/g, n =14) is significantly (p<0.05) 1.4 times higher than that of China grown
ginseng (16.48
±
1.24 mg/g, n =113) and 90% higher compared with that of Korea grown ginseng
(21.05
±
1.57 mg/g, n =106). There is no significant difference in the average content of total ginsenosides
for ginseng grown in China and Korea.
The average contents of seven individual ginsenosides are shown in Figure 4, the average
concentrations of ginsenoside Rb1, Re, Rf, and Rg1 from NZ-grown ginseng are significantly (p<0.05)
2.22, 2.91, 1.65, and 1.27 times higher than that of China grown ginseng, respectively. The ginsenosides
Re, Rf, and Rg1 of New Zealand ginseng are 3.14, 1.55, and 2.63 times that of Korean ginseng,
respectively. The average content of PPD type ginsenosides Rb2, Rc, and Rd are not significantly
different among the three growing regions of ginseng.
It is reported that the ratios of PPD to PPT and Rb1 to Rg1 are less than 2.0 and less than 5.0
in Panax ginseng, respectively [
13
]. Thus, we also calculated these ratios of ginsenosides from three
countries (Figure 5). The PPD/PPT ratios of all the NZ-grown ginsengs are less than 2.0, although
the average ratio of PPD/PPT from China grown ginseng is less than 2.0, many of the ratios are more
than 2.0. While, most values of PPD/PPT from Korea grown ginseng are more than 2.0, leading to the
average with >2.0. Although the average ratios of Rb1/Rg1 are less than 5.0 among three countries,
some ginseng samples still have Rb1/Rg1 >5.0. In addition, the ratios of Rg1 to Re is more than 1.0, and
Molecules 2019,24, 3491 5 of 11
the ratio of Rb2 to Rc is more than 0.4 in Panax ginseng [
14
]. From the average level, the average ratios
of Rg1/Re and Rb2/Rc are more than 1.0 and 0.4, respectively, among the three regions’ ginseng samples.
However, neither the value of Rg1/Re stays >1.0 all the time, nor the value of Rb2/Rc shows >0.4 in
all samples.
Molecules 2019, 24, x FOR PEER REVIEW 5 of 12
Usually, ginseng refers to the whole ginseng root including the main root body, root hair, and
rhizome. In our previous study, we analyzed ginsenosides from different parts including main root,
fine root, rhizome, stem, and leaf [11], it was found that the underground parts, including main root,
fine root, and rhizome, have very similar ginsenoside composition. In this study ginsenosides were
determined from the whole underground part. There is another study reporting ginsenosides
analysis for NZ-grown ginseng [12], which only detected seven main ginsenosides in four batches of
ginseng samples. In order to compare with China and Korea grown ginseng, the data from Table 1
and Follett’s publication [12] are used to calculate the average content of ginsenosides of NZ-grown
ginseng.
2.2. The Average Content of Ginsenosides in Different Regions
In order to obtain the average content of ginsenosides from China grown ginseng and Korea
grown ginseng, we searched the scientific literature for ginsenosides analysis from ginseng grown in
China and Korea. A total of 524 articles were located, and 151 potentially relevant studies were
selected to full-text review after removing the duplicates (N = 230), abstract only (N = 13) and
screening on the basis of title and abstract according to the inclusion criteria. After exclusion of 102
articles for the reasons given in Figure 2, we included 49 articles (article lists are supplied in the
Supplementary Materials). Among these articles, 30 articles were about ginsenosides analysis for
China grown ginseng, 17 for Korea grown ginseng, and two for NZ-grown ginseng.
Figure 2. Flow diagram of study search and inclusion criteria.
Figure 2. Flow diagram of study search and inclusion criteria.
Molecules 2019, 24, x FOR PEER REVIEW 6 of 12
After extracting the data from the inclusion articles, the amount of ginsenosides from 113 batches
of China grown ginseng roots aged from three to 30-years old was used to calculate the average
content of ginsenosides of China grown ginseng. A total of 106 batches of Korea grown ginseng roots
with different ages (one to 10-years old) were analyzed from 17 publications. For NZ-grown ginseng,
there were 14 batches of samples tests, including ten batches of ginseng roots in this study and four
from the literature.
As shown in Figure 3, the average content of total ginsenosides from NZ-grown ginseng (40.06
± 3.21 mg/g, n = 14) is significantly (p < 0.05) 1.4 times higher than that of China grown ginseng (16.48
± 1.24 mg/g, n = 113) and 90% higher compared with that of Korea grown ginseng (21.05 ± 1.57 mg/g,
n = 106). There is no significant difference in the average content of total ginsenosides for ginseng
grown in China and Korea.
Figure 3. The average content of total ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean ± SE. Differences were considered significant if p < 0.05. Each dot represents one batch of
ginseng sample test datum. C, K, and NZ-ginseng refers to China (n = 113), Korea (n = 106), and New
Zealand (n = 14) grown ginseng, respectively.
The average contents of seven individual ginsenosides are shown in Figure 4, the average
concentrations of ginsenoside Rb1, Re, Rf, and Rg1 from NZ-grown ginseng are significantly (p < 0.05)
2.22, 2.91, 1.65, and 1.27 times higher than that of China grown ginseng, respectively. The
ginsenosides Re, Rf, and Rg1 of New Zealand ginseng are 3.14, 1.55, and 2.63 times that of Korean
ginseng, respectively. The average content of PPD type ginsenosides Rb2, Rc, and Rd are not
significantly different among the three growing regions of ginseng.
Figure 4. The average content of individual ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean ± SE. * p < 0.05, ** p < 0.01, *** p < 0.001. Differences were considered significant if p < 0.05. C,
K, and NZ-ginseng refers to China (n = 113), Korea (n = 106), and New Zealand (n = 14) grown ginseng,
respectively.
Figure 3.
The average content of total ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean
±
SE. Differences were considered significant if p<0.05. Each dot represents one batch of
ginseng sample test datum. C, K, and NZ-ginseng refers to China (n =113), Korea (n =106), and
New Zealand (n =14) grown ginseng, respectively.
Molecules 2019,24, 3491 6 of 11
Molecules 2019, 24, x FOR PEER REVIEW 6 of 12
After extracting the data from the inclusion articles, the amount of ginsenosides from 113 batches
of China grown ginseng roots aged from three to 30-years old was used to calculate the average
content of ginsenosides of China grown ginseng. A total of 106 batches of Korea grown ginseng roots
with different ages (one to 10-years old) were analyzed from 17 publications. For NZ-grown ginseng,
there were 14 batches of samples tests, including ten batches of ginseng roots in this study and four
from the literature.
As shown in Figure 3, the average content of total ginsenosides from NZ-grown ginseng (40.06
± 3.21 mg/g, n = 14) is significantly (p < 0.05) 1.4 times higher than that of China grown ginseng (16.48
± 1.24 mg/g, n = 113) and 90% higher compared with that of Korea grown ginseng (21.05 ± 1.57 mg/g,
n = 106). There is no significant difference in the average content of total ginsenosides for ginseng
grown in China and Korea.
Figure 3. The average content of total ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean ± SE. Differences were considered significant if p < 0.05. Each dot represents one batch of
ginseng sample test datum. C, K, and NZ-ginseng refers to China (n = 113), Korea (n = 106), and New
Zealand (n = 14) grown ginseng, respectively.
The average contents of seven individual ginsenosides are shown in Figure 4, the average
concentrations of ginsenoside Rb1, Re, Rf, and Rg1 from NZ-grown ginseng are significantly (p < 0.05)
2.22, 2.91, 1.65, and 1.27 times higher than that of China grown ginseng, respectively. The
ginsenosides Re, Rf, and Rg1 of New Zealand ginseng are 3.14, 1.55, and 2.63 times that of Korean
ginseng, respectively. The average content of PPD type ginsenosides Rb2, Rc, and Rd are not
significantly different among the three growing regions of ginseng.
Figure 4. The average content of individual ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean ± SE. * p < 0.05, ** p < 0.01, *** p < 0.001. Differences were considered significant if p < 0.05. C,
K, and NZ-ginseng refers to China (n = 113), Korea (n = 106), and New Zealand (n = 14) grown ginseng,
respectively.
Figure 4.
The average content of individual ginsenosides in the ginseng roots grown in three different
countries. Data were analyzed by one-way ANOVA using Graph pad prism 6 software and expressed
as mean
±
SE. * p<0.05, ** p<0.01, *** p<0.001. Differences were considered significant if p<0.05.
C, K, and NZ-ginseng refers to China (n =113), Korea (n =106), and New Zealand (n =14) grown
ginseng, respectively.
Molecules 2019, 24, x FOR PEER REVIEW 7 of 12
It is reported that the ratios of PPD to PPT and Rb1 to Rg1 are less than 2.0 and less than 5.0 in
Panax ginseng, respectively [13]. Thus, we also calculated these ratios of ginsenosides from three
countries (Figure 5). The PPD/PPT ratios of all the NZ-grown ginsengs are less than 2.0, although the
average ratio of PPD/PPT from China grown ginseng is less than 2.0, many of the ratios are more
than 2.0. While, most values of PPD/PPT from Korea grown ginseng are more than 2.0, leading to the
average with > 2.0. Although the average ratios of Rb1/Rg1 are less than 5.0 among three countries,
some ginseng samples still have Rb1/Rg1 > 5.0. In addition, the ratios of Rg1 to Re is more than 1.0,
and the ratio of Rb2 to Rc is more than 0.4 in Panax ginseng [14]. From the average level, the average
ratios of Rg1/Re and Rb2/Rc are more than 1.0 and 0.4, respectively, among the three regions’ ginseng
samples. However, neither the value of Rg1/Re stays > 1.0 all the time, nor the value of Rb2/Rc shows >
0.4 in all samples.
Figure 5. The PPD/PPT, Rb1/Rg1, Rg1/Re, and Rb1/Rc ratios of ginsenosides in the ginseng roots
grown in three different countries. Data were analyzed by one-way ANOVA using Graph pad prism
6 software and expressed as mean ± SE. Differences were considered significant if p < 0.05. Each dot
represents one batch of ginseng sample test datum. C, K, and NZ-ginseng refers to China (n = 113),
Korea (n = 106), and New Zealand (n = 14) grown ginseng, respectively.
Since the contents of PPT type ginsenosides (Re, Rf and Rg1) in NZ-grown ginseng are
significantly higher than that of Chinese ginseng and Korean ginseng, besides Rb1, the concentrations
of other PPD type ginsenosides (Rb1, Rc and Rd) have no significant difference among three regions’
ginseng, which lead to the lower PPD/PPT ratio in NZ-grown ginseng.
Figure 5.
The PPD/PPT, Rb1/Rg1, Rg1/Re, and Rb1/Rc ratios of ginsenosides in the ginseng roots
grown in three different countries. Data were analyzed by one-way ANOVA using Graph pad prism 6
software and expressed as mean
±
SE. Differences were considered significant if p<0.05. Each dot
represents one batch of ginseng sample test datum. C, K, and NZ-ginseng refers to China (n =113),
Korea (n =106), and New Zealand (n =14) grown ginseng, respectively.
Molecules 2019,24, 3491 7 of 11
Since the contents of PPT type ginsenosides (Re, Rf and Rg1) in NZ-grown ginseng are significantly
higher than that of Chinese ginseng and Korean ginseng, besides Rb1, the concentrations of other PPD
type ginsenosides (Rb1, Rc and Rd) have no significant difference among three regions’ ginseng, which
lead to the lower PPD/PPT ratio in NZ-grown ginseng.
As the two most important sources of ginseng production, the total production by China and
Korea is 72,229 tons, which was approximately 90.2% of the world ginseng production [
15
]. Many
studies have reported the ginsenoside concentrations from China and Korea. However, they mainly
focused on one batch or limited batches of sample analysis [
16
–
18
]. There are few studies concerning
the comparison of ginsenosides between ginseng grown in different countries. We did not know if they
have some differences in the ginsenosides content between China and Korea grown ginseng. In this
study, the average content of ginsenosides from hundreds of batches of ginseng samples represent
the ginsenoside levels of ginseng grown in different regions. We can see there is neither a significant
difference in the content of the total ginsenosides between China grown ginseng and Korea grown
ginseng, nor remarkably differences in the individual ginsenoside contents of Rb2, Rc, Rd, Re, Rf, and
Rg1 in both countries. This may be due to the geographical proximity of Northeast China and South
Korea, and they have a similar growing environment for ginseng.
However, NZ-grown ginseng is grown in the Southern Hemisphere, apart from the similar growth
conditions including the cold winter, temperate summer, and weakly acidic soil to that ginseng’s
natural habitat in Northeast of China and Korea [
19
], there are some different growing characteristics
in New Zealand, including the volcanic pumice soil and high intensity light radiation. A recent study
showed that photosynthetically active radiation, soil, and water potentially had a great impact on
ginsenoside accumulation in ginseng roots [
20
]. The volcanic pumice soil can provide an excellent
environment for root growth because of its unique properties such as dark soil color, unique consistency,
low bulk density, difficult clay dispersion, and high water holding capacity [
21
]. Additionally, during
the Southern Hemisphere summer, NZ receives, on average, 7% more radiation compared to a given
latitude in the Northern Hemisphere summer [
22
]. It was reported that the total ginsenoside content
increased significantly until light transmission rate increased by 20%, but the PPT type ginsenosides
increased larger than PPD type ginsenoside, leading to the ratio of PPD/PPT eventually decreasing [
23
].
So to some extent, we have reason to believe that NZ’s unique geographical environment encourages
elevated ginsenosides (especially PPT type ginsenosides) content compared to ginseng grown in the
Northern Hemisphere with similar latitudes. On the other hand, we need to note the limitation of this
study, there is only 14 batches of NZ-grown ginseng sample data, a bit smaller compared to hundreds
of batches of sample data of Chinese ginseng and Korean ginseng.
3. Materials and Methods
3.1. Analysis of Ginsenosides Content of NZ Grown Ginseng
3.1.1. Ginseng Samples
All the NZ-grown ginseng samples were collected from pine forest around Taupo and Rotorua
(Table 2). The samples were rinsed with water, lyophilized at −68 ◦C and powered.
Table 2. Information of ten batches of ginseng samples.
NO Sample Age NO Sample Age
1 Root, large and hard 13 6 Root, regular 12
2 Root, small and hard 13 7 Root, regular 12
3 Root, small and soft 13 8 Root, regular 12
4
Root, normal size and hard
8 9 Root, regular 12
5 Root, small and hard 8 10 Root, regular 12
Molecules 2019,24, 3491 8 of 11
3.1.2. Standard Samples, Chemicals and Regents
Thirteen reference standards of ginsenosides Rb1, Rb2, Rb3, Rc, Rd, Re, Rf, Rg1, Rg2, Rg3, Rh1,
Rh2, and F2 were purchased from Star Ocean Ginseng Ltd. (Suzhou, Jiangsu, China). The purities of
all reference standards were above 98.0%. HPLC-grade methanol (MeOH) and formic acid (HCOOH)
were purchased from Fisher Chemical (Pittsburg, PA, USA). LC-MS-grade acetonitrile (MeCN) and
water were obtained from Merck (Phillipsburg, NJ, USA). Water (for extraction) was obtained from a
Milli-Q Ultra-pure water system (Millipore, Billerica, MA, USA). Other reagents used in this study
were of analytical grade.
3.1.3. Sample Preparation and HPLC-QTOF-MS/MS Analysis
Ginsenosides were extracted three times from ginseng samples using a Q700 sonicator (Qsonica,
Melville, NY, USA) and analyzed by an Agilent 1290 liquid chromatograph coupled with quadrupole
time-of-flight tandem mass spectrometry (Agilent, MA, USA) according to our previous methods [
11
].
Briefly, 0.7 g dried ginseng root powder was mixed with 10 mL 70% (v/v) aqueous MeOH and extracted
at 20 kHz for 10 min at no more than 40
◦
C. (The extraction was carried out for five cycles, each cycle
contained 2 min ultrasonically extraction at 15% amplitude and 1 min for cooling between extraction).
The supernatant was collected after centrifugation at 4000 rpm for 10 min and the sediment was
extracted twice more. The three extracts were mixed together and filtered through a 0.22-
µ
m filter
before LC/MS analysis.
Thirteen reference standards of ginsenosides Rb1 (0.769 mg/mL), Rb2 (0.846 mg/mL), Rb3
(0.629 mg/mL), Rc (1.077 mg/mL), Rd (0.692 mg/mL), Re (0.923 mg/mL), Rf (1.462 mg/mL), F2
(0.692 mg/mL), Rg1 (1.154 mg/mL), Rg2 (0.615 mg/mL), Rg3 (1.154 mg/mL), Rh1 (1.000 mg/mL), and
Rh2 (1.077 mg/mL) were dissolved in 70% MeOH and then mixed and diluted with 70% MeOH to
obtain a series of mixture standard solutions of different concentrations. The solutions were filtered
through a 0.22- µm syringe filter before LC/MS analysis.
An Agilent 1290 liquid chromatograph (Agilent, MA, USA) equipped with an online degasser, an
auto-sampler, a quaternary pump, and a heated column compartment, and an Agilent 6530 Quadrupole
Time of Flight Mass Spectrometer (Agilent, MA, USA) equipped with an electrospray ionization source
were used for LC/MS analysis. The separation was based on a Zorbax Extend-C18 (2.1
×
100 mm,
3.5
µ
m) column (Agilent, USA) at a temperature of 33
◦
C. The binary gradient elution solvent consisted
of water (A) and acetonitrile (B) (Both A and B containing 0.1% formic acid). The gradient elution
program was as follows: 0–4 min, 80% A; 4–10 min, 80%–70% A; 10–25 min, 70%–67.5% A; 25–27 min,
67.5%–40% A; 27–39 min, 40%–5% A; 39–40 min, 5% A; 40–40.5 min, 5%–80% A. The flow rate was
changed with the gradient: 0–27 min, 0.2 mL/min; 27–40.5 min, 0.25 mL/min. The injected volume
was 1
µ
L. The mass spectrometer data were collected from m/z100–2200 in negative ion model and
nitrogen (>99.998%) was used for nebulizer gas and curtain gas. The gas temperature and flow rate
were 350
◦
C and 10.0 L/min, respectively. The pressure of nebulizer was 37 psi. The voltages of
capillary, fragmentor, and skimmer were 3500 V, 220 V, and 65 V, respectively. The reference masses
in negative ion mode were at m/z121.0509 and 922.0098. The acquisition rates were 4 spectra/s for
MS and 1 spectrum/s for MS/MS. Mass data were analyzed with Agilent MassHunter Workstation
software (version B.06.00; Agilent Technologies, Santa Clara, CA, USA).
3.2. Analysis of Ginsenosides Content from China and Korea Grown Ginseng
Ginsenosides content of China and Korea grown ginseng obtained from publications based on the
following search criteria.
3.2.1. Search Strategy
The following search terms were applied to search the following electronic databases from their
inception to April 2019.
Molecules 2019,24, 3491 9 of 11
The following search terms were used in Web of Science: TITLE: (Content* OR level* OR amount*
OR quantif* OR determinat* OR investigat* OR analy*) AND TOPIC: (Ginsenoside*) AND TITLE:
(“Panax ginseng” OR “Korean ginseng”). Refined by: LANGUAGES: (ENGLISH OR CHINESE) AND
DOCUMENT TYPES: (ARTICLE). Timespan: All years. Databases: WOS, BIOABS, CABI, CCC, FSTA,
KJD, MEDLINE, RSCI, SCIELO. Search language =Auto.
The following search terms were used in the PubMed database: (Ginsenoside [Title] AND content
[Title]) OR (ginsenosides [Title] AND content [Title]) OR (ginsenoside [Title] AND contents [Title])
OR (ginsenosides [Title] AND contents [Title]) OR (ginsenosides [Title] AND investigation [Title]) OR
(ginsenosides [Title] AND quantification [Title]) OR (ginsenosides [Title] AND determination [Title])
NOT rat [Title]).
The following search terms were used in Science Direct: Find articles with these terms “content of
ginsenosides”; Title, abstract, keywords: “ginsenoside, Panax ginseng”; Article type: Research articles.
The following search terms were used in Scopus: TITLE-ABS-KEY (ginsenosides) AND
(LIMIT-TO (ACCESSTYPE (OA))) AND (LIMIT-TO (SUBJAREA, “PHAR”) OR LIMIT-TO (SUBJAREA,
“CHEM”) OR LIMIT-TO (SUBJAREA, “AGRI”)) AND (LIMIT-TO (EXACTKEY- WORD, “Article”) OR
LIMIT-TO (EXACTKEYWORD, “Ginsenoside”) OR LIMIT-TO (EXACTKEYWORD, “Ginsenosides”)
OR LIMIT-TO (EXACTKEYWORD, “Ginseng”)) AND (LIMIT-TO (LANGUAGE, “English”)
OR LIMIT-TO (LANGUAGE, “Chinese”)) AND (LIMIT-TO (SRCTYPE, “j”)) AND (EXCLUDE
(EXACTKEYWORD, “Animals”) OR EXCLUDE (EXACTKEYWORD, “Animal Experiment ”)) AND
(EXCLUDE (EXACTKEYWORD, “Human”)).
3.2.2. Inclusion Criteria
The following inclusion criteria were defined: (a) The literature are experimental articles; (b) the
study measured six common ginsenosides (ginsenosides Rb1, Rb2, Rc, Rd, Re, and Rg1) or seven
common ginsenosides that includes Rf; (c) the above common ginsenosides are extracted from ginseng
root (Panax ginseng); (d) the articles contain the amount of common ginsenosides.
3.2.3. Exclusion Criteria
The following exclusion criteria were defined: (a) Excludes articles about ginsenoside contents in
the animal or human tissue samples, such as plasma, urine, and feces, etc.; (b) excludes articles that
the materials contain other ingredients, such as Chinese herbs formula, commercial ginseng products
(c) excludes articles that ginseng materials did not grow in the forest or farmland, such as cultured
laboratory samples.
3.2.4. Data Extraction
Investigators reviewed the titles, abstracts, and full text of the resulting articles for inclusion. Data
were extracted from each publication meeting the inclusion criteria. The values of ginsenosides (Rb1,
Rb2, Rc, Rd, Re, Rf, and Rg1) content (mean) were collected based on grown locations (China, Korea,
and NZ). When ginsenosides content were reported using bar charts in the literature, the estimated
values were collected using ruler assistance.
3.3. Data Analysis
The level of ginsenosides of NZ-grown ginseng was expressed as mean
±
SD, and the average
contents of ginsenosides of different regions from literature were calculated and expressed as mean
±
SE. One-way ANOVA was used to analyze the difference among groups. A p-value <0.05 was
considered to be statistically significant.
Molecules 2019,24, 3491 10 of 11
4. Conclusions
This is the first article focusing on ginsenoside content in different producing areas. In this study,
the average content of ginsenosides from three regions (China, Korea, and NZ) are described and
compared. There is no significant difference in the average content of total ginsenosides between
China grown ginseng and Korea grown ginseng. NZ-grown ginseng has significantly higher average
content of total ginsenosides than that of above two regions, especially higher concentrations of PPT
type ginsenosides Re, Rf, and Rg1.
Supplementary Materials:
The following are available online at http://www.mdpi.com/1420-3049/24/19/3491/s1,
Inclusion articles lists.
Author Contributions:
W.C. and D.GP. conceived and designed the experiments; W.C. performed the experiments,
analyzed the data, and wrote the original manuscript; P.B. and D.GP. reviewed and edited the manuscript.
Funding: This work was supported by funding from the Alpha-Massey Natural Nutraceutical Research Centre.
Acknowledgments:
The authors thank the Kiwiseng Co. Ltd. for providing the NZ-grown ginseng. We would
like to acknowledge Ceire Hopley for her help in literature searching and analysis and Maggie Zou for her help to
acquire LC-MS/MS data.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
Bai, L.; Gao, J.; Wei, F.; Zhao, J.; Wang, D.; Wei, J. Therapeutic Potential of Ginsenosides as an Adjuvant
Treatment for Diabetes. Front. Pharm. 2018,9, 423. [CrossRef] [PubMed]
2.
Choi, K.T. Botanical characteristics, pharmacological effects and medicinal components of Korean Panax
ginseng C A Meyer. Acta Pharm. Sin. 2008,29, 1109–1118. [CrossRef] [PubMed]
3.
Murthy, H.N.; Dandin, V.S.; Park, S.Y.; Paek, K.Y. Quality, safety and efficacy profiling of ginseng adventitious
roots produced in vitro. Appl. Microbiol. Biotechnol. 2018,102, 7309–7317. [CrossRef] [PubMed]
4.
Chaudhary, S.A.; Gadhvi, K.T.; Chaudhary, A.B. Comprehensive review on world herb trade and most
utilized medicinal plant. Int. J. Appl. Biol. Pharm. Technol. 2010,1, 510–517.
5.
Attele, A.S.; Wu, J.A.; Yuan, C.-S. Ginseng pharmacology: Multiple constituents and multiple actions.
Biochem. Pharmacol. 1999,58, 1685–1693. [CrossRef]
6.
Chen, W.; Balan, P.; Popovich, D.G. Comparison of the ginsenoside composition of Asian ginseng (Panax
ginseng) and American ginseng (Panax quinquefolius L.) and their transformation pathways. In Studies
in Natural Products Chemistry; Rahman, A., Ed.; Elsevier: Amsterdam, The Netherlands, 2019; Volume 63,
in press.
7.
Szakiel, A.; P ˛aczkowski, C.; Henry, M. Influence of environmental abiotic factors on the content of saponins
in plants. Phytochem. Rev. 2011,10, 471–491. [CrossRef]
8.
Shi, W.; Wang, Y.; Li, J.; Zhang, H.; Ding, L. Investigation of ginsenosides in different parts and ages of Panax
ginseng. Food Chem. 2007,102, 664–668. [CrossRef]
9.
Liu, Z.; Wang, C.Z.; Zhu, X.Y.; Wan, J.Y.; Zhang, J.; Li, W.; Ruan, C.C.; Yuan, C.S. Dynamic changes in neutral
and acidic ginsenosides with different cultivation ages and harvest seasons: Identification of chemical
characteristics for panax ginseng quality control. Molecules 2017,22, 734. [CrossRef] [PubMed]
10.
Xu, X.F.; Xu, S.Y.; Zhang, Y.; Zhang, H.; Liu, M.N.; Liu, H.; Gao, Y.; Xue, X.; Xiong, H.; Lin, R.C.; et al.
Chemical comparison of two drying methods of mountain cultivated ginseng by UPLC-QTOF-MS/MS and
multivariate statistical analysis. Molecules 2017,22, 717. [CrossRef] [PubMed]
11. Chen, W.; Balan, P.; Popovich, D.G. Ginsenosides analysis of New Zealand–grown forest Panax ginseng by
LC-QTOF-MS/MS. J. Ginseng Res. 2019, in press. [CrossRef]
12.
Follett, J.M.; Proctor, J.T.; Walton, E.F.; Boldingh, H.L.; McNamare, C.; Douhlas, J.A. Carbohydrate and
Ginsenoside Changes in Ginseng Roots Grown in the Bay of Plenty New Zealand. J. Ginseng Res.
2004,28, 165–172.
13.
Kim, D.H. Chemical Diversity of Panax ginseng, Panax quinquifolium, and Panax notoginseng. J. Ginseng Res.
2012,36, 1–15. [CrossRef] [PubMed]
Molecules 2019,24, 3491 11 of 11
14.
Qi, L.W.; Wang, C.Z.; Yuan, C.S. Ginsenosides from American ginseng: Chemical and pharmacological
diversity. Phytochemistry 2011,72, 689–699. [CrossRef] [PubMed]
15.
Baeg, I.H.; So, S.H. The world ginseng market and the ginseng (Korea). J. Ginseng Res.
2013
,37, 1–7.
[CrossRef] [PubMed]
16.
Zhang, L.; Zhou, Q.L.; Yang, X.W. Determination of the transformation of ginsenosides in Ginseng Radix et
Rhizoma during decoction with water using ultra-fast liquid chromatography coupled with tandem mass
spectrometry. J. Sep. Sci. 2018,41, 1039–1049. [CrossRef] [PubMed]
17.
Wang, H.P.; Zhang, Y.B.; Yang, X.W.; Zhao, D.Q.; Wang, Y.P. Rapid characterization of ginsenosides in the
roots and rhizomes of Panax ginseng by UPLC-DAD-QTOF-MS/MS and simultaneous determination of 19
ginsenosides by HPLC-ESI-MS. J. Ginseng Res. 2016,40, 382–394. [CrossRef] [PubMed]
18.
Lee, G.J.; Shin, B.K.; Yu, Y.H.; Ahn, J.; Kwon, S.W.; Park, J.H. Systematic development of a group quantification
method using evaporative light scattering detector for relative quantification of ginsenosides in ginseng
products. J. Pharm. Biomed. Anal. 2016,128, 158–165. [CrossRef]
19.
Douglas, M.H.; Smallfield, B.M.; Parmenter, G.A.; Burton, L.C.; Heaney, A.J.; Johnstone, P.D. Effect of growing
media on the production of ginseng (Panax ginseng) in Central Otago, New Zealand. N. Z. J. Crop Hortic. Sci.
2000,28, 195–207. [CrossRef]
20.
Zhang, T.; Han, M.; Yang, L.; Han, Z.; Cheng, L.; Sun, Z.; Yang, L. The effects of environmental factors on
ginsenoside biosynthetic enzyme gene expression and saponin abundance. Molecules 2019. [CrossRef]
21.
Nanzyo, M.; Shoji, S.; Dahlgren, R. Chapter 7 Physical Characteristics of Volcanic Ash Soils. In Developments
in Soil Science; Shoji, S., Nanzyo, M., Dahlgren, R., Eds.; Elsevier: Amsterdam, The Netherlands, 1993;
Volume 21, pp. 189–207.
22.
Smallfield, B.M.; Follett, J.M.; Douglas, M.H.; Douglas, J.A.; Parmenter, G.A. Production of Panax. spp. in
New Zealand. Med. Aromat. Plant. 1995,390, 83–91. [CrossRef]
23.
Jang, I.B.; Lee, D.Y.; Yu, J.; Park, H.W.; Mo, H.S.; Park, K.C.; Hyun, D.Y.; Lee, E.H.; Kim, K.H.; Oh, C.S.
Photosynthesis rates, growth, and ginsenoside contents of 2-yr-old Panax ginseng grown at different light
transmission rates in a greenhouse. J. Ginseng Res. 2015,39, 345–353. [CrossRef] [PubMed]
Sample Availability: Samples of the compounds are not available from the authors.
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2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
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