Accepted Manuscript

Structure, physicochemical properties and adsorption function of insoluble di-

etary fiber from ginseng residue: a potential functional ingredient

Mei Hua, Jiaxi Lu, DiQu, Chang Liu, Lei Zhang, Shanshan Li, Jianbo Chen,
Yinshi Sun

PII: S0308-8146(19)30182-7
DOI: https://doi.org/10.1016/j.foodchem.2019.01.114
Reference: FOCH 24209

To appear in: Food Chemistry

Received Date: 8 August 2018

Revised Date: 10 January 2019
Accepted Date: 22 January 2019

Please cite this article as: Hua, M., Lu, J., DiQu, Liu, C., Zhang, L., Li, S., Chen, J., Sun, Y., Structure,
physicochemical properties and adsorption function of insoluble dietary fiber from ginseng residue: a potential
functional ingredient, Food Chemistry (2019), doi: https://doi.org/10.1016/j.foodchem.2019.01.114

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 Structure, physicochemical properties and adsorption function of insoluble dietary fiber from

ginseng residue: a potential functional ingredient

Mei Huaa, Jiaxi Lub, DiQu a, Chang Liua, Lei Zhanga, Shanshan Lia, Jianbo Chen a, Yinshi Suna,*

a
Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, 130112

Changchun, Jilin, China

b
Institute of Chemical technology, The Hague University of Applied Science, The Hague 2521 EN,

Netherlands

⁎
Corresponding author :

Work address: Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural

Sciences, 130112 Changchun, Jilin, China.

E-mail address: sunyinshi2015@163.com

Phone number: +0086 17790062198

Author E-mail address: huam149@nenu.edu.cn (M.Hua); lujiaxi1019@outlook.com (J.X.Lu);

15143162826@163.com(D.Qu); liuchang@caas.cn(C.Liu); leizhang0102@163.com (L.Zhang);

lishanshan@caas.cn (S.S.Li); chenjianbo00882@126.com (J.B.Chen)

1
Abstract

The insoluble dietary fiber from ginseng residue (ginseng-IDF) was extracted using the AOAC

(Association of Official Analytical Chemists) method with content of 68.61%. Ginseng-IDF had a

polysaccharide content of 18.87%, uronic acid content of 7.85%, protein content of 6.52%, and had

ideal water-holding capacity (17.66 g/g), swelling ability (15.05 mL/g), and oil-holding capacity (1.78

g/g). Scanning electron microscope, fourier transform infrared spectroscopy, and X-ray diffraction

analyses suggested that ginseng-IDF had the typical structures of hydrolysis fiber, polysaccharide

functional groups, and crystal structure of cellulose. Different fiber components give ginseng-IDF a

specified range of pyrolysis temperature, and it is suitable for application in food processing lower than

300 ℃. In addition, ginseng-IDF exhibited notable glucose and sodium cholate adsorption, significantly

improved nitrite adsorption at pH 2.0 and cholesterol adsorption at pH 7.0. The above results show that

ginseng-IDF could be used as an ideal functional ingredient in food processing.

Keywords: Ginseng residues; Insoluble dietary fiber; Composition; Structure; Physicochemical

properties; Adsorption function

2
1. Introduction

Modern dietary habits have resulted in a serious lack of nutrients obtained from food, especially

the "seventh nutrient"-dietary fiber (DF). Dietary fiber is a kind of non-starch polysaccharide

carbohydrate that mainly comes from the cell wall of plants. DF cannot be digested by human intestinal

digestive enzymes, and is only absorbed by the large intestine, but it has important physiological

functions in the body (Alba et al., 2018). Depending on its solubility, dietary fiber can be divided into

water-soluble dietary fiber (SDF) and water-insoluble dietary fiber (IDF). SDF usually includes pectin,

oligosaccharides, and soluble hemicelluloses. IDF usually includes cellulose, insoluble hemicelluloses,

and lignin (Alba et al., 2018). IDF plays a critical role in digestive processes, including promoting

intestinal peristalsis, increasing fecal volume, and adsorbing and quickly eliminating grease, heavy

metals, and other toxic substances (Makki, Deehan, Walter, & Bäckhed, 2018). In fact, it is necessary

to consume 50%–75% IDF in daily meals to achieve the best activity of dietary fiber. Therefore, the

role of insoluble dietary fiber in human health should not be ignored (Alba et al., 2018).

Fruits, vegetables, and grains are the traditional sources of dietary fiber, while the modern dietary

habits in western countries have resulted in an insufficient intake of dietary fiber. Therefore, the United

States, Japan, and other countries have developed a variety of methods for the artificial extraction or

synthesis of dietary fiber carbohydrates (Makki, Deehan, Walter, & Bäckhed, 2018). Represented by

Chinese food, the eastern diet emphasizes health and balance. Medicinal foods have a long history in

the eastern diet. Residues of edible medicinal plants contain a small amount of medicinally active

ingredients and a large number of oligosaccharides, cellulose, and hemicellulose components, making

them a valuable source of dietary fiber (Li et al., 2015).

Panax ginseng, which usually refers to the root of the Panax genus, has long been widely used as

a nourishing and strengthening medicine in Eastern Asia, North America, and Europe (Zhang et al.,

2018). The raw materials of ginseng are widely used in food, health care products, cosmetics, and in

other industries, resulting in large quantities of residue. These residues are discarded as industrial waste

without optimal utilization (Chen & Lee, 2018). Some research of ginseng has focused on the efficacy

of its main active components, as digestible starch-polysaccharide and ginsenoside. However, very few

reports have focused on the indigestible non-starch polysaccharides in ginseng residues (Yu et al.,

2017). Studies have shown that ginseng residues are rich in dietary fiber, proteins, mineral elements

3
and other nutrients (Yu et al., 2017). In regard to total dietary fiber, IDF accounts for a major

proportion, and exhibits different chemical composition and functional properties when compared with

SDF, such as the adsorption to the oil, cholesterol and toxic metal ions (Zheng et al., 2018). These

results suggest that, to obtain ginseng dietary fiber with health-promoting function, it is necessary to

conduct an in-depth study of its main component—ginseng-IDF.

The aim of this study was to elucidate the application value of insoluble dietary fiber of ginseng

(ginseng-IDF) as a functional food ingredient. To this end, ginseng-IDF was extracted using the AOAC

(Association of Official Analytical Chemists) method. To our knowledge, this is the first systematic

study on the composition, structure, physicochemical properties and adsorption function of

ginseng-IDF. This study provides the necessary information for the research on the quality and

properties of ginseng-IDF. In addition, the present study can also lead to the further research on its

application value in human health and nutrition.

2. Materials and methods

2.1. Materials

2-(N-Morpholino) ethanesulfonic acid (MES) and 1,1,1-tris(hydroxymethyl)-methanamin (Tris)

were purchased from Sigma-Aldrich Co. (Shanghai, China). In addition, thermostable α-amylase,

protease from Bacillus licheniformis, amyloglucosidase solution from Aspergillus niger, and all the

monosaccharide standards were purchased from Sigma-Aldrich Co. (Shanghai, China). Ginseng

residue was prepared in our laboratory after boiled extraction of ginseng polysaccharides. All other

reagents used were of analytical grade.

2.2. Preparation of ginseng-IDF

2.2.1. Pretreatment of ginseng residue

Ginseng residue was washed twice with 70% and 85% ethanol and distilled water, to remove

water-soluble oligosaccharide and inorganic salts. The residue was dried at 60 ℃ for 24 h and filtered

through a 60-mesh sieve, then packaged in a self-sealing bag and stored at -20 °C until further analysis.

4
2.2.2. Extraction of the ginseng-IDF

Extraction of the ginseng-IDF was carried out following the AOAC method 991.43 (AOAC,

2002). Briefly, 50 g of ginseng residue was treated with 2.5 mL thermostable α-amylase in 1.5 L

(solid/liquid ratio of 1:30) of MES-Tris buffer (pH 8.2) using a magnetic stirrer (300 rpm) at 100 ℃ for

30 min. Upon cooling of the reactant to 60 ℃, 5.0 mL protease was added and the mixture was

incubated with continuous agitation for 60 min. Next, the pH of the reactant was adjusted to 4.5 using 3

M acetic acid, and 10.0 ml amyloglucosidase was added at 60 ℃ for 60 min with the same stirring

speed. After the enzymatic hydrolysis, the reaction mixture was centrifuged at 8000 ×g for 20 min.

Solid residue was then washed twice with distilled water and 95% ethanol. Precipitate was dried at 60

℃, crushed through a 60-mesh standard sieve, and collected as ginseng-IDF. The soluble dietary fiber

(ginseng-SDF) and total dietary fiber (ginseng-TDF) were extracted and calculated according to the

AOAC method 991.43 too.

2.3. Component analysis of ginseng-IDF

Oven-drying method (120 °C) was used to determine the moisture content of the ginseng-IDF

(Mokhtar, Swailam, & Embaby, 2018). Protein (N × 6.25), fat and ash content of the ginseng-IDF were

measured following the AOAC method (AOAC 978.04, AOAC 996.06, AOAC 930.05). Total sugar

and uronic acid content of the ginseng-IDF was measured by the phenol-sulfuric acid method (Dubois

et al., 1956) and the m-hydroxydiphenyl method (Blumenkrantz & Asboe-Hansen, 1973), respectively.

Cellulose, hemicellulose, and lignin contents of the ginseng-IDF were measured by the method of Xu

et al. (2012).

Monosaccharide composition analysis was performed by HPLC (High Performance Liquid

Chromatography) using Thermo Scientific Hypersil ODS-2 (C18) (4.6×250 mm) connected to a

Shimadzu HPLC system (Essentia LC-16 pump and SPD-M20A UV-VIS detector) following the

method of Zhang et al. (2017) after hydrolysed the sample with 4 M trifluoroacetic acid at 120 ℃ for 2

h (Alba et al., 2018). The detection conditions were: 84% A and 16% B at 35 ℃ for 40 min, and a flow

rate of 1 ml/min, at a detection wavelength of 245 nm.

Amino acid composition was measured by the method of Mokhtar et al. (2018), and detected

5
using the L-8900 automatic amino acid analyzer (Hitachi High-Technologies Corporation, Tokyo,

Japan) equipped with a 4.6 mm (ID) × 60 mm ion-exchange column. An external standard was used to

calculate the concentration of each amino acid.

Mineral element composition was measured by the method of Zhang et al. (2017) using a flame

atomic absorption spectrophotometer (Analytik Jena, ZEEnit 700, Jena, Germany), except for Se, As,

and Hg, which were detected using a multichannel atomic fluorescence spectrometer (PGENERAL,

PF6-3, Beijing, China). For trace element measurements, 0.5 g of dried sample was dissolved in acid

mixture comprising 5 mL of 37% HCl and 10 mL of 63% HNO3, diluted to 100 mL using distilled

water.

2.4. Structure and thermal analysis

The microscopic appearance of ginseng residue and ginseng-IDF were observed using XL-30

ESEM FEG Scanning Electron Microscope (SEM) (FEI CompanyTM, OR, USA) after spraying with

gold-palladium alloy (Cressington Scientific Instruments Ltd, Watford, UK). The scanning images

were captured at accelerating voltages of 5 kV and 10 kV, and photographed at magnifications of 200 ×

(scale bar 100 μm) to 3427 × (scale bar 10 μm).

Fourier transform infrared spectroscopy (FT-IR) analyses of ginseng-IDF were performed using a

VERTEX 70 FT-IR spectrometer (Bruker Optics Inc., Ettlingen, Germany). The sample table was

mixed with KBr powder (1:100, w/w), and the spectra was read over the range of 4000–500 cm−1 with

a resolution of 2 cm−1.

X-ray diffractometry (XRD) patterns of ginseng-IDF were recorded using an X-ray diffractometer

(D8 ADVANCE, Bruker AXS GmbH Co., Karlsruhe, Germany) equipped with theta-compensating slits

and Cu-Kα radiation source (λ=1.542 Å), running at 40 mA and 40 kV. Diffraction angle (2θ) was

adjusted from 5° to 70°, at a rate of 2°/min. The crystallinity index (CI, %) was calculated by MDI Jade

6.5 software using the following equation (Segal, 1959):

CI = [(I002 − Iam) / I002] × 100

In this equation, CI expresses the relative degree of crystallinity, I002 is the intensity of the 002

6
lattice diffraction at 2θ = 22.8°, and Iam is the intensity of diffraction at 2θ = 18°–19°. I002 represents

both crystalline and amorphous regions, while Iam represents only the amorphous part.

Thermal gravity (TG) analysis and differential thermal gravity (DTG) techniques were used to

complete the thermal analysis of ginseng-IDF. The TG/DTG was performed using a thermogravimetric

analyzer (Pyris Diamond TGA/DTG, PerkinElmer, USA) in a nitrogen atmosphere over a range of

50–600 ℃, with a rate of 10 ℃/min.

2.5. Physicochemical properties of ginseng-IDF

Bulk density (BD) was measured by the method of Qi et al. (2015), calculated as follows:

BD (g/mL) = weight of the sample (g) / volume of the sample (mL)

Water-holding capacity (WHC) was measured by the method of Zhang et al. (2017). Initial dry

weight of the sample was recorded as W1, the treated weight of IDF residue was recorded as W2. The

WHC was then calculated as follows:

WHC (g/g) = (W2 - W1) / W1

Solubility in water (SOL) was measured as the percentage of weight difference before and after

the water dissolved of sample.

Oil-holding capacity (OHC) was measured by the method of Zhang et al. (2017) with appropriate

modifications. Briefly, 0.5 g of the sample (M1) was vigorously mixed with 5 mL of peanut oil,

incubated at 25 ℃ for 24 h, and centrifuged at 4000 ×g for 10 min. The oil supernatant was then

discarded and the weight of the residue was recorded as M2. The OHC was calculated as follows:

OHC (g/g) = (M2 − M1) / M1

Swelling ability (SA) was measured by the method of Gouw et al. (2017) with appropriate

modifications. Briefly, 0.5 g of sample was mixed vigorously with 20 mL of distilled water at 25 ℃ for

7
24 h to swell fully for swelling volume detection. The SA was calculated as follows:

SA (mL/g) = swelling volume of the sample (mL) / weight of the sample (g)

2.6. Adsorption capacity of ginseng-IDF

2.6.1. Glucose-adsorption capacity (GAC)

GAC was measured according to the method of Benítez et al. (2017) by mixing 1 g of

ginseng-IDF with 100 mL of glucose solution (0.05-0.5 mg/mL) at 37 ℃ for 6 h. DNS colorimetric

method was used to determine the glucose content in supernatant.

2.6.2. Nitrite-adsorption capacity (NAC)

NAC was measured according to the method of Luo et al. (2017) by mixing 1 g of ginseng-IDF

with 25 mL of sodium nitrite solution (100 μmol/L) , then adjusted to pH 2.0 or pH 7.0 (simulating the

pH conditions in the stomach and small intestine, respectively) and incubated at 37℃ for 120 min.

Nitrite content was determined by N-(1-Naphthyl) ethylenediamine dihydrochloride/sulfanilic acid

reagent at 538 nm on a UV-2000 ultraviolet spectrophotometer (Unico, Shanghai, China).

2.6.3. Cholesterol-adsorption capacity (CAC)

CAC was measured according to the method of Luo et al. (2017) by mixing 1 g of ginseng-IDF

with 30 mL of diluted yolk solution (a fresh egg yolk diluted by 9 volume of distilled water and

homogenized), then adjusted to pH 2.0 or pH 7. 0 and incubated at 37 °C for 180 min. Absorbance of

the supernatant was measured at 550 nm.

2.6.4. Bile acid-adsorption capacity (BAC)

BAC was measured according to the method of Luo et al. (2017) by mixing 1 g of ginseng-IDF

with 30 mL of sodium cholate (1-3 mg/mL, pH 7.0) and incubated at 37 °C for 120 min. Absorbance of

the supernatant was determined at 620 nm.

The adsorption quantities of GAC, NAC, CAC, and BAC were calculated as per 1 g IDF:

8
 Adsorption quantity (μg/g or mg/g) = the original content − the remaining content at different

adsorption times

The adsorption rate of GAC, NAC, CAC, and BAC were calculated as:

Adsorption rate = (1–the content at different adsorption times / the original content) × 100

2.7. Statistical analyses

All experiments were repeated three times, and the data are expressed as mean values ± standard

deviations (SD). Statistical analyses and preparation of the figures were carried out in GraphPad Prism

6.0 software (GraphPad Software Inc., USA).

3. Results and discussion

3.1. Chemical composition and physicochemical properties

As shown in Table 1, ginseng-IDF was the major component of ginseng residue, accounting for

approximately 69% of its content. Within the IDF, the content of cellulose was higher than 70%.

Ginseng-IDF had a polysaccharide content of 18.87%, a uronic acid content of 7.85%, and a protein

content of 6.52%, which reflected its rich nutritional value. The extremely low fat content (1.87%) also

suggested its potential application as a low-calorie food ingredient (Zheng et al., 2018). We compared

the differences in the nutritional composition of ginseng-IDF with other dietary fibers from fruits,

cereals and coffee in Supplemental Table 1. The nutritional advantages of ginseng-IDF were also

confirmed. Besides, ginseng-SDF and ginseng-TDF contents in ginseng residue were 7.47% and

54.11%, respectively (data unpublished). The monosaccharide composition of ginseng-SDF included

nine compositions: galactose, glucose, xylose, mannose, fucose, D-glucosamine, galacturonic acid,

rhamnose and glucuronic acid (data unpublished).

In addition to its nutritional value, ginseng-IDF also had ideal physicochemical properties. As

shown in Table 1, ginseng-IDF had a BD index of 0.58 g/mL, reaching the level of ordinary cellulose

9
(0.50 g/mL, Benítez et al., 2017). Ginseng-IDF had a good WHC of 17.66 g/g, which was close to the

levels of corn stover (17.7 g/g) and sugarcane bagasse (17.3 g/g, Yadav, Kale, Hicks, & Hanah, 2017),

and much higher than that of bamboo shoot shell IDF (2.83 g/g, Luo et al., 2017). The SA index of

ginseng-IDF (15.05 mL/g) was much higher than that of bamboo shoot shell IDF (4.01 mL/g, Luo et

al., 2017) and rice bran IDF (5.24-7.54 g/g, Zhao et al., 2018). Ginseng-IDF had a low SOL index of

5.67%, which was in line with its high content of cellulose. The OHC level of ginseng-IDF (1.78 g/g)

was close to that of superfine rice bran IDF (1.72 g/g, Zhao et al., 2018), but better than that of lotus

node IDF (0.61-1.50 g/g, Hussain et al., 2018). Some studies have indicated that the effect on the

hydration and adsorption properties of IDF depended on the processing and structural characteristics of

the cellulose material (Zhao et al., 2018). This may help explain why ginseng-IDF with the

enzymolysis processing could match the OHC level of superfine rice bran IDF.

The amino acid and mineral element content analyses (Table 2) showed that ginseng-IDF contains

abundant amino acids and various mineral elements needed by the human body. Nine essential amino

acids and eight non-essential amino acids were detected in ginseng-IDF. Among the essential amino

acids, leucine, arginine, and lysine had the highest contents of over 0.35 g per 100 g. The essential

amino acid content of ginseng-IDF was nearly 50% of the total amino acid content, which was much

higher than that of papaya peel SDF (Zhang et al., 2017). The above results indicated that the nutritive

content of ginseng-IDF is higher than that of some fruits SDF. Mineral elements are another important

nutritional component of ginseng-IDF. Fourteen mineral elements were detected in ginseng-IDF with a

total content (TM) of 2.57 × 104 mg/kg (Table 2). Ca accounted for 80% of this value, which was found

in much higher levels in ginseng-IDF than in ginseng-SDF (data unpublished), which indicated that a

high amount of calcium may be retained in insoluble dietary fiber during processing. In addition,

ginseng-IDF also contained high levels of Zn (71.72 mg/kg) and Se (0.24 mg/kg), suggesting that

ginseng-IDF could be a trace element supplement with the potential roles of an antioxidant and a

nephroprotective agent (Soussi, Gargouri, & El Feki, 2018; Zhu et al., 2017).

3.2. Monosaccharide composition

The composition of seven monosaccharides in ginseng-IDF is shown in Table 2. Neutral

monosaccharides, including glucose (Glc, 28.64%), xylose (Xyl, 21.01%), galactose (Gal, 20.95%),

10
fucose (Fuc, 15.79%), and mannose (Man, 4.61%), were found to be the primary component of

ginseng-IDF. In addition, ginseng-IDF contained a small amount of acidic monosaccharide:

galacturonic acid (GalUA, 6.08%) and trace amounts of D-glucosamine (GlcN, 2.91%), which was

lower than the amount in papaya peel SDF (Zhang et al., 2017). Ginseng-IDF showed a different

monosaccharide composition compared to the dietary fiber from fruit pomace (Alba et al., 2018; Zhang

et al., 2017) and agricultural by-products (Yadav, Kale, Hicks, & Hanah, 2017; Zhu et al., 2018), which

are characterized mainly by the absence of arabinose and rhamnose, and the presence of fucose. The

total content of neutral monosaccharide in ginseng-IDF was over 90%. This result further confirmed

the conclusion that glucose oligosaccharides and cellulose were the major components of ginseng-IDF.

The detection of xylose, glucose, and mannose suggested the possible presence of xyloglucans, xylans,

and galactomannans, which all belong to the hemicellulose component (Qi et al., 2015).

3.3. Structure analysis

3.3.1 SEM

The micromorphologies of ginseng residue and ginseng-IDF are shown in Fig. 1. The surface of

ginseng-IDF showed a more loosely packed microstructure with more cracks compared to that of the

ginseng residue (Fig. 1a and Fig. 1c). The likely reason for this is that large amounts of water-soluble

substances were lost from the ginseng residue in the boiling process, and resulting that part of the

structure of the ginseng fiber had been destroyed. For that reason, some irregular fragments and small

clumps were observed (Fig. 1b). After the extraction treatment, ginseng-IDF showed a relatively

regular loose structure with cavities (Fig. 1d). The extraction treatment led to a looser structure with

increased specific surface area of ginseng-IDF, which improved its water, oil, heavy metal, and salt ion

absorption capacities (Zhu et al., 2018). On the whole, the microstructures of ginseng-IDF and ginseng

residues showed no substantial differences and were still dominated by insoluble cellulose.

3.3.2. FT-IR and XRD analyses

Polysaccharide functional groups of ginseng-IDF were revealed by FT-IR spectrum analysis (Fig.

2a). The FT-IR spectrum of ginseng-IDF was similar to that of blackcurrant IDF (Alba et al., 2018) and

okara IDF (Ullah et al., 2017), which have typical functional groups of soluble pectin and insoluble

11
cellulose. As shown in Fig. 2a, a strong absorption at 3419 cm-1, mainly of the native cellulose, was

attributed to the O-H group stretching by molecular hydrogen bonding of uronic acids (Alba et al.,

2018; Zhang et al., 2015). The notable absorption at 2926 cm-1 resulted from the C-H stretching of

-CH3 or =CH2, representing the typical structure of cellulose polysaccharide compounds (Yan, Ye, &

Chen, 2015). The minor peak at 1741 cm-1 was mainly due to acetyl group or ester carbonyl (C=O)

group stretching of hemicellulose (Alba et al., 2018). The notable peak at 1626 cm-1 was mostly

attributed to the esterified and ionized carboxyl groups of GalUA (Pappas et al., 2004). The weak peak

at 1516 cm-1, along with the minor peak at 1427 cm-1, was a result of the aliphatic or aromatic C-H

group vibration of lignin (Alba et al., 2018). The weak peak at 1319 cm-1 was mainly from the typical

cellulose structure (Zhang et al., 2015). The weak peak at 1242 cm-1 was assigned to the O-H or C-O

group vibration of hemicellulose (Bian et al., 2012). Peaks at 900-1200 cm-1, including the absorption

at 1056 cm-1, originated from the acyl-oxygen (CO–OR) stretching vibration of hemicelluloses and the

C–O stretching vibration of the guaiacyl unit of lignin (Chen, Luo, Qin, & Tong, 2014). The above

results clearly showed that ginseng-IDF had the typical functional groups of cellulose polysaccharides,

including pectin, cellulose, hemicellulose, and lignin, which is consistent with its composition shown in

Table 1.

X-ray diffractometry was used to determine the structure and the type of cellulose crystals in

ginseng-IDF. As shown in Fig. 2b, ginseng-IDF had a cellulose I crystal structure with two obvious

diffraction peaks of 2θ = 15.02° and 21.08°, which suggested the presence of a crystalline cellulose

region. This profile was similar to that of okara IDF and rice bran IDF, in which the amorphous portion

of cellulose was partly destroyed (Ullah et al., 2017; Qi et al., 2015). Irregular weak peaks at 2θ = 9.4

and from 24.3° to 38.1° in Fig. 2b could be attributed to the denaturation of cellulose during the

ginseng-IDF extraction process under conditions of acidic/alkaline solution and enzyme hydrolysis (Ma

& Mu, 2016). The relative crystallinity of ginseng-IDF was 34.24%, which was close to the 36.60%

crystallinity index of okara IDF (Ullah et al., 2017).

3.4. Thermal analysis

Thermogravimetric (TG) and differential thermogravimetric (DTG) analyses (Fig. 3) were carried

out to evaluate the thermal behaviours of ginseng-IDF, to quantify the thermal effect generated during

12
the processing, and to further confirm its thermal stability. The TG curve profile of ginseng-IDF had

three mass loss phases at 50–200 ℃, 200–400 ℃, and 400–600 ℃ with different degradation rates (in

black), which was similar to the thermal behaviour of rice bran IDF (Qi et al., 2015). In the first

pyrolytic range of 50–200 ℃, evaporation occurred at 120 ℃ and yielded a mass loss of less than 1.0%,

which can be interpreted as the evaporation of absorbed water from the surface of the sample. In the

second pyrolytic range of 200–400 ℃, ginseng-IDF demonstrated different weightlessness rates. As a

result, an obvious peak appeared in the DTG curve (in red). Ginseng-IDF had a rapid weightlessness

rate, beginning at 259.53 ℃, and a maximum weightlessness rate of 6.72%/min was observed at 333.33

℃, with a maximum weightlessness of 2.49 mg (61.91%). Notably, the weightlessness of ginseng-IDF

can be attributed to the pyrolytic decomposition of soluble pectin and hemicellulose polysaccharides,

which can also be seen as the pre-carbonization process of cellulose in ginseng-IDF (Zhang et al.,

2017). In addition, less soluble components of ginseng-IDF, such as protein and pectin, contribute to its

higher pyrolytic decomposition temperature (Julie Chandra, George, & Narayanankutty, 2016). After

heating to the third pyrolytic range of 400–600 ℃, a slow weightlessness of 0.22 mg (5.43%) residual

weight could be observed. Ginseng-IDF had a lower rate of weightlessness beginning at 476.72 ℃, a

maximum weightlessness rate of 3.07%/min at 511.51 ℃ and a maximum weightlessness of 1.08 mg

(26.76%). The second peak in the DTG curve can be attributed to the decomposition of cellulose and

lignin in ginseng-IDF (Alvarez & Vázquez, 2004). The above results suggested that ginseng-IDF was

suitable for applications in food processing lower than 300 ℃.

The network of lignin in the plant cell wall is composed of ester and ether linkages with

hemicellulose, and the cellulose is usually embedded in the cell wall to form complex fiber-polymers.

The amorphous structure of lignin has great pyrolysis resistance to thermal processes and reduces the

thermal accessibility of cellulose. Generally, the thermal stability order of the three fiber is: lignin >

cellulose > hemicellulose (Yang, Zeng, & Zhang, 2010). With regard to the pyrolysis mechanism of

cellulose, the most commonly accepted response path is as follows. First, cellulose produces activated

cellulose with a low degree of polymerization through complex reactions such as dehydration,

condensation and depolymerization. Then, the active cellulose is further decomposed into intermediate

products by dehydration and aromatization, producing char and small gases, or by dehydration of side

functional groups and condensation, resulting in mainly levoglucosan, all of which decompose into the

final products of gases, bio-oil, and char (Demirba, 2000).

13
 To improve the pyrolysis selectivity and conversion efficiency of cellulose, some physical,

chemical and biological pretreatment methods have been widely used in the pyrolysis process. Before

pyrolysis, biomass materials are pretreated to destroy the complex structure or the corresponding

components of lignocellulose, and to reduce the structural resistance to pyrolysis. The pH conditions

and enzyme treatment in the extraction of ginseng dietary fiber can reduce the protection of lignin in

the cellulose-associated hemicellulose mixture, aggravate the decomposition of hemicellulose, worsen

the thermal stability of cellulose and hemicellulose, and enhance the accessibility of cellulose and

hemicellulose to pyrolysis (Demirba, 2000).

3.5. Adsorption function analysis

The in vitro adsorption function of ginseng-IDF was further investigated with glucose, sodium

nitrite, cholesterol, and sodium cholate (Fig. 4). The adsorption of ginseng-IDF increased with

increasing glucose concentration, and the adsorption rate remained at 80%-89% for 6 h (Fig. 4a). This

adsorption trend was consistent with that of the onion by-product IDF reported by Benitez et al. (2017),

suggesting that ginseng-IDF may have application value in blood glucose control. The nitrite

adsorption of ginseng-IDF was determined at pH 2.0 and 7.0 to simulate the gastric and intestinal

environment in vitro (Fig. 4b). The results showed that ginseng-IDF exhibited significantly better

adsorption capacity at pH 2.0 than at pH 7.0, which was similar to the results observed in FMBDF

(foxtail millet bran dietary fiber, Zhu et al., 2018) and DCCDF (defatted coconut cake-IDF, Zheng et

al., 2018). Over time, the nitrite adsorption of ginseng-IDF at pH 2.0 increased gradually from 79.83

μg/g to 254.38 μg/g, with the highest adsorption ratio of 73.73% occurring at 2 h. In contrast, the

adsorption at pH 7.0 was saturated (93.76 μg/g, 54.35%) at 1 h, then began a slow descent, and ended

with a final adsorption capacity of 57.47 μg/g and adsorption ratio of 33.31%. The nitrite adsorption of

ginseng-IDF was noticeably higher than that of DCCDF (Zheng et al., 2018) and FMBDF (Zhu et al.,

2018) within a short duration (2 h). The great adsorption capacity of ginseng-IDF at pH 2.0 may be due

to the chemisorption mechanism. Dietary fiber is rich in uronic acid, amino acids, phenolic acids and

other active groups. Among these active groups, phenolic acid groups are the main contributors to

nitrite adsorption. In acidic conditions, NO2- can combine with H+ to produce HNO2. HNO2 then forms

a lot of nitrogen-oxygen compounds, including the strong electron-affinity compound N2O3, which can

14
bind to the negatively charged oxygen atoms of phenolic acid groups in the dietary fiber and cause

adsorption (Honikel, 2008).

Over 90% of bile acids in the human body exist in the form of binding substances, such as sodium

cholate. DF can effectively absorb sodium cholate and other lipid substances in the intestinal tract, and

help eliminate these substances, acting as a lipid scavenger (Devi et al., 2014). In addition, when the

sodium cholate content decreases, the body automatically converts cholesterol into sodium cholate for

supplementation, thereby promoting the consumption of cholesterol. Therefore, the adsorption capacity

of DF for cholesterol and cholate is often used as an evaluation index for the adsorption of lipophilic

substances (Zhu et al., 2018). As shown in Fig. 4c, ginseng-IDF exhibited a clear adsorption affinity for

cholesterol in vitro, with the highest adsorption capacity of 49.69 mg/g (84.56%) at pH 7.0 after 30

min, which then slowly decreased to 36.30 mg/g (61.79%) over 3 h. In contrast, the cholesterol

adsorption of ginseng-IDF at pH 2.0 was saturated (20.48 mg/g, 18.41%) after 1 h, followed by a slow

increase and ended with a final adsorption value of 22.17 mg/g and 19.92%. In general, ginseng-IDF

exhibited significantly better cholesterol adsorption at pH 7.0 than at pH 2.0, which is similar to the

behaviour of FMBDF (Zhu et al., 2018), but different from that of DCCDF (Zheng et al., 2018), and

much better than the apple peel and wheat grain (Zhang, Huang, & Ou, 2011). The above results

indicated that adsorption pH has a marked influence on the adsorption effect of DF. Ginseng-IDF was

more effective for cholesterol adsorption in the intestinal environment than in the stomach

environment, and the optimal adsorption time was 1-2 h (Zhu et al., 2018; Zhang, Huang, & Ou, 2011).

As shown in Fig. 4d, ginseng-IDF exhibited improved adsorption for sodium cholate in vitro with an

increasing concentration (1-3 mg/mL), similar to the behaviour of FMBDF (Zhu et al., 2018).

Ginseng-IDF had the highest adsorption capacities of 9.91 mg/g (16.51%), 21.86 mg/g (18.22%), and

60.50 mg/g (33.61%) for 1, 2, and 3 mg/mL, respectively. All the highest adsorption values were

reached after 1 h, and tended to be stable over 2 h. Feng et al. (2017) reported that the original SDF of

black bean coats exhibited little bile acid binding capacity, and modified SDF with 1 M Ca2+ exhibited

an adsorption value of 6 mg/g. From the viewpoint of Feng et al. (2017), a high calcium concentration

would lead to a more open gel structure suitable for cholate adsorption, and the corresponding

rheological properties would also change. This view may be used to support the result that ginseng-IDF

containing large amounts of Ca2+ (Table 2) exhibits significant adsorption capacity of sodium cholate.

15
4. Conclusion

The edible medicinal plant ginseng is rich in polysaccharide carbohydrates, and can be used as a

valuable source of functional dietary fiber. In this study, ginseng-IDF, the insoluble dietary fiber of

ginseng residue, was extracted and studied systematically for the first time. The results suggested that

ginseng residue was an ideal material for insoluble dietary fiber recovery. High polysaccharide, uronic

acid, protein and mineral element contents of ginseng-IDF suggested its potential nutritional value. The

ideal WHC, SA, and OHC index of ginseng-IDF suggested its application potential in food processing.

SEM, FT-IR, and XRD analyses suggested that ginseng-IDF had the typical structure of hydrolysis

fiber, polysaccharide functional groups, and crystal structure of cellulose. Thermal analysis suggested

that different fiber components give ginseng-IDF a specified range of pyrolytic temperatures, and the

extraction method was helpful to improve the pyrolytic accessibility of the cellulose in ginseng-IDF.

Ginseng-IDF is suitable for applications in food processing lower than 300 ℃. In addition, ginseng-IDF

exhibited notable glucose and sodium cholate adsorption, and significantly improved nitrite adsorption

at pH 2.0 and cholesterol adsorption at pH 7.0, which are levels equal to or higher than those of the

insoluble dietary fiber of grain. The above results showed that ginseng-IDF has high nutritional value,

ideal physiological activity and adsorption function, making it a potential functional ingredient in the

food industry.

Acknowledgements

This work was supported by the Scientific and Technologic Foundation of Jilin Province (grant

numbers 20191102052YY, 20160520048JH and 201603078YY).

Conflict of interest

The authors have no interest conflicts to declare.

Appendix

16
Supplemental Table 1

Nutritional components of ginseng-IDF, fruits, and other insoluble dietary fiber materials.

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Figure captions

Fig. 1. Microstructure of ginseng residue (a,b) and ginseng-IDF (c,d).

Fig. 2. Fourier transform infrared spectroscopy (FT-IR, a) and X-ray diffraction (XRD, b) spectra of

20
 ginseng-IDF. 2θ represents diffraction angle, the relative crystallinity was calculated by MDI Jade 6.5.

Fig. 3. Thermal analysis of ginseng-IDF. TG and DTG curve of ginseng-IDF are marked in black and

red, respectively. The sample quantity was 4.026 mg. The initial pyrolysis temperature was 53.84 ℃,

and the final pyrolysis temperature was 600.00 ℃. Onset Y, residual mass at the beginning of

weightlessness. Onset X, temperature at the beginning of weightlessness. Peak, temperature at the

maximum weightlessness rate. Area, area of weightlessness peak which is proportional to the weight

loss.

Fig. 4. The in vitro adsorption of ginseng-IDF for glucose (a), sodium nitrite (b), cholesterol (c), and

sodium cholate (d). (a) the adsorbing quantity and adsorption rate of ginseng-IDF for different glucose

concentrations (0.05-0.5 mg/mL); (b,c) the adsorbing quantity and adsorption rate of ginseng-IDF for

sodium nitrite and cholesterol at pH 2.0 and pH 7.0; (d) the adsorbing quantity and adsorption rate of

ginseng-IDF for different sodium cholate concentrations (1-3 mg/mL). Data are expressed as mean ±

standard deviation (SD).

Table 1

Chemical composition and physicochemical properties of ginseng-IDF.

Component Percentage (%) Physicochemical properties Percentage (%)

Moisture 5.85 ± 0.40 Bulk density (g/ml d.w.) 0.58 ± 0.01

Protein 6.52 ± 0.09 Water-holding capacity (WHC, g/g) 17.66 ± 0.10

Fat 1.87 ± 0.11 Oil--holding capacity (OHC, g/g) 1.78 ± 0.04

21
Ash 8.11 ± 0.15 Swelling ability (SA, ml/g) 15.05 ± 0.36

Total sugar 18.87 ± 0.49 Solubility in water (SOL, %) 5.67 ± 0.49

Uronic acid 7.85 ± 0.45

Insoluble dietary fiber (IDF) a 68.61 ± 1.46

cellulose 72.30 ± 0.29

hemicellulose 13.74 ± 0.37

lignin 4.35 ± 0.08

Data are pressented as mean values ± SD (n=3). Results were expressed as %, g/g or ml/g dry mater

(d.w.). a. Content percentage from the ginseng residue, and all the other data were were measured with

IDF as sample.

Table 2

Amino acid, mineral elements and monosaccharide composition of ginseng-IDF.

Ginseng-IDF

Amino acid composition (g/100g dry weight) Mineral elements (mg/kg dry weight)

EAAs Ca 2.06×104 ± 14

Threonine 0.3176 Na 1.50×103 ± 9.64

Valine 0.3009 Mg 1.71×103 ± 7.77

Methionine 0.0352 K 794.90 ± 1.56

Isoleucine 0.2798 Fe 712.56 ± 4.54

Leucine 0.4290 Mn 231.27 ± 2.60

Phenylalanine 0.3115 Cu 24.64 ± 0.54

Lysine 0.3647 Zn 71.72 ± 0.41

Histidine 0.1722 As 0.0019 ± 0.0002

Arginine 0.3778 Se 0.24 ± 0.02

NEAAs Cr 5.58 ± 0.04

Serine 0.3149 Cd 0.40 ± 0.05

Glutamic acid 0.5622 Pb 2.32 ± 0.03

Glycine 0.3273 Hg 0.03 ± 0.0026

22
 Alanine 0.3222 TMs 2.57×104

Cysteine 0.0297 Monosaccharide composition (mol %)

Aspartic acid 0.6877 Man 4.61 ± 0.04

Tyrosine 0.2008 GlcN 2.91 ± 0.02

Proline 0.3942 GalUA 6.08 ± 0.06

TAAs 5.4279 Glc 28.64 ± 0.17

EAAs/TAAs (%) 47.69 Gal 20.95 ± 0.20

Xyl 21.01 ± 0.47

Fuc 15.79 ± 0.02

EAAs: essential amino acids; NEAAs: non-essential amino acids; TAAs: total amino acids; TMs: total

minerals. Man: mannose; GlcN: D-Glucosamine; GalUA: galacturonic acid; Glc: glucose; Gal:

galactose; Xyl: xylose; Fuc: fucose. Data are pressented as mean values ± SD (n=3).

Highlights

• Ginseng residue was rich in dietary fiber, especially the ginseng-IDF.

• Ginseng-IDF was rich in nutrition and chemical composition.

• Ginseng-IDF presented good physicochemical properties and adsorption function.

• Ginseng-IDF could be served as a promising functional food ingredient.

Conflict of interest

The authors have no interest conflicts to declare.

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