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BY 4.0 license Open Access Published by De Gruyter Open Access November 11, 2022

Study on essential oil, antioxidant activity, anti-human prostate cancer effects, and induction of apoptosis by Equisetum arvense

  • Hongyong Gu EMAIL logo , Ting Yi , Pengxiu Lin and Jin Hu
From the journal Open Chemistry

Abstract

In this study, we have reported the chemical composition of Equisetum arvense essential oil and the anti-cancer activity of the plant against the prostate cancer cell line. The essential oil was obtained using the hydro-distillation assay. The chemical composition was identified using the gas chromatographic methods including gas chromatography/flame ionization detector and gas chromatography/mass spectrometry. The antioxidant activity of the essential oil and extract was evaluated using classical methods. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay was run to evaluate the cytotoxic effect of the essential oil and extract on the prostate cancer cell line of lymph node carcinoma of the prostate. The induction apoptosis of the extract was analyzed by a flow cytometer. Thymol acetate (14.7%), trans-carveol (12.5%), thymol (11.8%), and δ-elemene (9.4%) were identified as the main compounds for the essential oil. The extract scavenged the free radical of 2,2-diphenyl-1-picrylhydrazyl with a half maximal inhibitory concentration (IC50) of 15.2 ± 1.4 μg/mL for the plant extract. In the MTT assay, the IC50 of the extract and essential oil were 25.2 ± 0.3 and 218.9 ± 10.7 μg/mL after 72 h. The highest apoptosis was 31.6% for the plant extract. The obtained results of the present study revealed that E. arvense can be introduced as a potent agent to prevent the growth of prostate tumors.

List of abbreviations

AsA

ascorbic acid

BHT

butylhydroxytoluene

DPPH

2,2-diphenyl-1-picrylhydrazyl

EDTA

ethylenediaminetetraacetic acid

FIC

ferrous ion chelating ability

GC/FID

gas chromatography/flame ionization detector

GC/MS

gas chromatography/mass spectrometry

IC50

half maximal inhibitory concentration

LNCaP

lymph node carcinoma of the prostate

MTT

3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

RSA

radical scavenging activity

TPC

total phenolic content

TFC

total flavonoid content

TOC

α-tocopherol

1 Introduction

Prostate cancer is the most common cancer in men. If it is early detected, the survival rate is high [1,2]. Surgery, chemotherapy, or secondary hormonal therapy, which depends on tumor aggressiveness, are usual ways to treat prostate cancer [3,4,5]. Herbal medicine is an alternative to cure diseases due to the minimal side effects [4]. In recent years, there is an increasing interest in diets rich in some ingredients such as lycopene, vitamin C, vitamin K, and polyphenols to improve the survival of patients with prostate cancer due to their ability reported in the literature [6].

Equisetum arvense, known as horsetail, belongs to Equisetaceae family [7]. E. arvense is a perennial plant. It grows naturally in light sandy soils [8]. In folkloral medicine, E. arvense has been used for urinary and prostatic problems, managing enuresis, managing irritable symptoms of the urinary system [9]; treatment of digestive disorders and kidney/bladder stones, analgesic, hemostatic, astringent [10]; skin, hair, and nail remedies [11]; wounds, metabolic or hormonal edema, rheumatism, and chilblains [12].

The stem extract of E. arvense showed sedative and anticonvulsant properties [13]. The extract showed analgesic and anti-inflammatory effects [14]. The prepared herbal tea of E. aruense is known as a diuretic agent in folk medicine of different cultures [15]. Various uses have been reported for E. arvense. The plant showed antitumoral, antimicrobial, anticonvulsant, and antidiabetic activity [16]. The plant is an effective agent to treat tuberculosis, ulcers, and bleeding [17].

E. arvense is rich in polyphenolic compounds such as flavonoids, tannins, sterols, and saponins [18]. Epicatechin, quercetin, catechin, leutolin, and apigenin are the abundant flavonoids, and vanillic acid, caffeic acid, ferulic acid, and coumaric acid are the predominant phenolic compounds [19,20,21]. Oh et al. reported the isolation of phenolic compounds onitin and onitin-9-O-glucoside and of flavonoids luteolin, kaempferol-3-O-glucoside, and quercetin-3-O-glucoside from E. arvense [22]. Calcium, potassium, phosphate, iron, manganese, silicic acid, and silicates are abundant minerals in the plant [23,24].

In the present study, the chemical composition of E. arvense essential oil was analyzed using chromatography methods as well as the antioxidant activity of the plant essential oil and extract. Furthermore, as mentioned earlier, E. arvense is known as an herbal remedy for prostate problems in some traditional medicine around the world; this is a study examining on the anti-cancer activity of the plant volatile oil and extract using 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay on lymph node carcinoma of the prostate (LNCap) cell line as a standard human prostate cancer cell line.

2 Material and methods

2.1 Chemicals

The chemicals with analytical grades were used in this research: 2,2-diphenyl-1-picrylhydrazyl (DPPH), ferrozine, and α-tocopherol (Sigma, USA); Na2SO4, ascorbic acid (AsA) (Merck, Germany); saturated hydrocarbon homologous series (C8–C20 and C21–C40) (Fluka, USA); ferrous sulfate heptahydrate (BD, UK).

2.2 Collection of plant material

The aerial parts of E. arvense were purchased from a medicinal plant store. The plant was identified by Mrs. Yudi Miao with voucher number 20-11-328.

2.3 Isolation of E. arvense essential oil

A 100 g plant sample was put in a Clevenger-type apparatus for 4 h. The hydrodistillation was repeated five times. The obtained essential oil was dried over anhydrous sodium sulfate (Merck) and stored in tightly closed vials at −18°C in the dark before biological and analytical assays.

2.3.1 Gas chromatography/flame ionization detector analysis

2.3.1.1 GC/FID analysis

The essential oil was subjected to GC/FID analysis using a Hewlett-Packard 5890 GC instrument equipped with a DB-5 capillary column (30 m × 0.25 mm i.d.; film thickness, 0.1 mm; from J.W. Scientific, USA). Helium was the carrier gas (1.0 mL/min). The injector and detector temperature was 250°C. The initial temperature was maintained at 40°C for 2 min, then raised at 3°C/min to 240°C, and held for 10 min. The split ratio was 1:20. Hydrogen was applied as fuel in the detector. A homologous series of saturated hydrocarbons (C8 to C40) were subjected to the instrument with the same conditions. Quantification was done by an external standard method using calibration curves generated by running GC analysis of representative compounds.

2.3.1.2 Gas chromatography/mass spectrometry analysis

For the GC-MS analysis of the essential oil, an Agilent GC/MS system (7890A equipped with an Agilent 5975C mass detector) was selected. The sample was injected into an HP-5 capillary column (30 m × 0.32 mm i.d.; 0.25 mm film thickness from J.W. Scientific). All parameters were the same as GC/FID conditions. A 70 eV was the ionization voltage, and the scan mass range was 50–600 amu for the mass detector.

2.3.1.3 Component identification

The identity of the chemical constituents of the volatile oil was established using the GC retention indices Kovats indices, the retention time, and mass spectral fragmentation patterns with those of the known compounds from the literature data [25] and the standard database of NIST (National Institute of Standards and Technology) [26]. Furthermore, structural assignment confirmation was also made by co-injection of available authentic pure samples. Quantification was done by an external standard method using calibration curves generated by running GC analysis of representative compounds.

2.4 Preparation of E. arvense extract

To obtain the hydroalcoholic extract of E. aevense, 50 g of the aerial parts of the plant was ground and macerated in the solvent for 72 h. The solvent consisted of 70% of ethanol and 30% of water. Then, the solvent was evaporated using a Buchi evaporator (50°C). Finally, the crude extract was put in a freeze-dryer for 48 h. The powder was kept in a dark-and-cold place before biological investigations.

2.4.1 Antioxidant activity evaluation assays

The classical assays including total phenolic content (TPC), total flavonoid content (TFC), radical scavenging activity (RSA), and ferrous ion chelating ability (FIC) were carried out to study the antioxidant activity of E. aevense extract and essential oil [27,28].

2.5 TPC

First, a mixture that included 0.5 mL of a methanolic solution of E. aevense extract (100 µg/mL), Folin-Ciocalteu Reagent (0.5 mL, 10% in distilled water), and H2O (2 mL) was prepared. After 5 min, 2 mL of sodium carbonate (5%) was added and shaken. Then, the optical density of the mixture was recorded at 760 nm using a Shimadzu instrument (UV-2400) after 2 h. The TPC was reported as mg GAE/g extract, which means mg of gallic acid equivalent per gram of extract. All measurements were carried out in triplicates.

2.5.1 TFC

A 1.5 mL of E. aevense extract (200 µg/mL) was added to AlCl3 in methanol (1 mL, 2%) and kept for 40 min. Then, the optical density was read at 415 nm. The TFC was reported as milligram RE/gram extract, that is, the milligram of rutin equivalent per gram of dried extract. The analyses were run three times.

2.5.2 RSA

A 0.5 mL of E. aevense extract or essential oil at different concentrations was poured into 0.5 mL of DPPH (1 × 10−3 M) and shaken. After 2 h, the absorbance was read at 517 nm. α-Tocopherol (Toc) and butylated hydroxytoluene (BHT) were the selected positive controls for this assay. All measurements were run three times. The RSA% was obtained by the following equation:

RSA % = ( A c A s ) A c × 100 ,

where A c and A s are the control absorbance (DPPH solution) and the sample, respectively.

2.5.3 FIC

Ferrozine (100 µL, 5 × 10−3 M) was pipetted to a mixture of FeSO4 (50 µL, 2 × 10−3 M) and 1 mL of E. aevense extract or essential oil at different concentrations. After 10 min. the absorbance was read at 562 nm. Ethylenediaminetetraacetic acid (EDTA) and AsA were chosen as the positive control for this assay. All measurements were run three times. The FIC was calculated using the following equation:

Inhibition % = ( A c A s ) A c × 100 ,

where A c and A s are the absorbance of the control (FeSO4 and ferrozine) and the sample, respectively.

2.5.4 MTT assay

In this research, we used LNCaP cell lines to evaluate the anti-human prostate cancer and cytotoxicity effects of E. arvense extract and essential oil. The assay was run according to previous studies with some modifications [29,30]. The cell line was cultured (1 × 104 cells/well) in a 96-well microplate and incubated at 37°C, CO2 5% for 24 h. Next, the plant extract or essential oil at different concentrations was added to the wells and incubated for 24, 48, and 72 h. After that, 20 µL of MTT (3-[4,5-dimethylthiazole-2-yl]-2,5-diphenyltetrazolium bromide) with a concentration of 5 mg/mL in PBS was added and incubated at 37°C for 4 h. Finally, the absorbance of the dissolved formazan crystals in DMSO (dimethyl sulfoxide) was read at 570 nm and 630 by a plate reader (Thermo Lab systems, Franklin, MA USA). The half maximal inhibitory concentration (IC50), which showed the concentration of E. arvense extract or essential oil for 50% mortality rate, was measured through Prism software. All treatments run three times. For this assay, DMSO and docetaxel (0.1 µM) were used as the negative and positive controls, respectively.

2.5.5 Flow cytometric analysis

The apoptosis was screened by propidium iodide (PI) staining of small DNA fragments followed by flow cytometry according to a previous study [30]. Briefly, LNCaP cells (1.5 × 105 cells) were cultured in FBS (10%) and then incubated overnight at 37°C under CO2 (5%). Then, it was treated with the calculated IC50 value of the extract for 24, 48, and 72 h. After that, the cells were taken up and put in an incubator for 24 h with 700 μL of 50 mg/mL PI. After that, a Becton Dickinson flow cytometer was used. A total of 10,000 events were attained with FACS. A flow Jo-V10 software was used to analyze the data.

2.6 Qualitative measurement

The obtained findings were analyzed using SPSS (version 20) software using one-way ANOVA, followed by Duncan's posthoc test (P ≤ 0.01).

3 Results and discussion

3.1 The essential oil composition

The obtained volatile oil was colorless with an average of 0.21 ± 0.03% (W/W) yield. Twenty compounds were identified in the essential oil comprising eight oxygenated monoterpenes (33.4%), four sesquiterpene hydrocarbons (29.1%), two phenolic compounds (26.5%), two oxygenated hydrocarbons (6.0%), and one monoterpene hydrocarbon (0.6%). These represented 95.6% of all oil components. Table 1 shows the chemical composition of E. aevense essential oil. The phenolic compounds of thymol acetate (14.7%) and oxygenated monoterpene of trans-carveol (12.5%) were the main components of the essential oil, followed by thymol (11.8%) and δ-elemene (9.4%).

Table 1

Chemical composition of the essential oil of the aerial parts of Equisetum arvense

No Compoundsa RT RI (Lit.)b RI (Obsd.)c Area (%) Id. Meth.d
1 1,8 Cineole 7.16 1,026 1,024 1.6 RI, MS
2 γ-Terpinene 7.94 1,054 1,053 0.6 RI, MS
3 Heptyl acetate 9.7 1,112 1,110 0.4 RI, MS
4 Octyl formate 10.2 1,127 1,122 5.6 RI, MS
5 iso-3-Thujanol 10.7 1,130 1,134 2.3 RI, MS
6 γ-Terpineol 13.1 1,199 1,196 7.9 RI, MS
7 trans-Carveol 13.9 1,216 1,215 12.5 RI, MS
8 E-Ocimenone 14.8 1,235 1,236 0.7 RI, MS
9 Geraniol 15.5 1,249 1,252 0.9 RI, MS
10 Geranial 15.7 1,264 1,267 0.4 RI, MS
11 Methyl nerolate 16.7 1,280 1,279 1.6 RI, MS
12 Thymol 17.3 1,289 1,291 11.8 RI, MS
13 Azulene 17.6 1,298 1,297 6.8 RI, MS
14 δ-Terpinyl acetate 18.5 1,316 1,318 1.7 RI, MS
15 δ-Elemene 19.4 1,335 1,338 9.4 RI, MS
16 α-Cubebene 19.7 1,345 1,344 4.8 RI, MS
17 Thymol acetate 19.8 1,349 1,348 14.7 RI, MS
18 (E)-Caryophyllene 22.8 1,417 1,415 5.7 RI, MS
19 4,8β-Epoxy-caryophyllane 23.4 1,423 1,427 2.4 RI, MS
20 trans-Carvyl propanoate 29.13 1,454 1,459 3.8 RI, MS
I Oxygenated monoterpenes (OM) 33.4
II Sesquiterpene hydrocarbons (SH) 26.7
III Phenolic compounds (Ph) 26.5
IV Oxygenated hydrocarbons (OH) 6.0
V Oxygenated sesquiterpene (OS) 2.4
VI Monoterpene hydrocarbons (MH) 0.6

aOxygenated monoterpenes, Nos. 2, 5–11, 14, 20; Sesquiterpene hydrocarbons, Nos. 13, 15,16, 18, 19; Phenolic compounds, Nos. 12 and 17; Oxygenated hydrocarbons, Nos. 3 and 4; Oxygenated sesquiterpene, Nos. 19; Monoterpene hydrocarbons, No. 2.

bRI (Lit.): Retention indices from literatures (Adams [25]).

cRI (Obsd.) Retention indices (I) on DB-5.

dIdentify method.

In a previous study, the essential oil of E. aevense from Europe was dominated by hexahydrofarnesyl acetone, cis-geranyl acetone, and trans-β-damascenone [31]. Fons et al. have evaluated the volatile organic compounds of different Equisetum species using GC/MS analysis. According to their reports, E. arvense was rich in 3-hydroxy-7,8-epoxy-β-ionol, (E,E)-pseudoionone, and 3-oxo-α-ionol; E. palustre var. americana was dominated by 1-octen-3-ol, (E)-2-hexenoic acid, and (E)-2-hexenal; 3-hydroxy-7,8-epoxy-β-ionol, 3-hydroxy-α-ionone, and 4-vinylguaiacol were the main component of E. telmateia; (E)-2-heptenal, (E)-and (Z)-ferulic acid isomers were the main compounds for E. hyemale; E. ramosissimum was rich in 4-vinylguaiacol, (E)- and (Z)-ferulic acid; on the other hand, 3-hydroxy-β-ionone, 3-hydroxy-7,8-epoxy-β-ionol (15.5%), and homovanillic acid were identified in E. scirpioides [32]. The essential oil of E. diffusum was dominated by phytol, hexacosane, and cis-cadin-4-ene-7-ol [33]. The difference in the chemical composition of Equisetum plants can be due to the method applied to the isolation of the essential oils, the seasonal variation, drying period, altitudes, environmental circumstances, climatic conditions, and geographical location of the plant [34,35].

3.2 Antioxidant activity

The results of the antioxidant activity of E.aevense extract and essential oil are presented in Table 2. A 389.0 ± 6.4 mg GAE/g for TPC and 57.6 ± 3.8 mg RE/g for TFC of E.aevense were recorded. According to our findings, the extract was more potent in the selected antioxidant assays compared to the essential oil. The extract scavenged DPPH with IC50 of 15.2 ± 1.4 μg/mL. The extract showed more activity than BHT and TOC. Furthermore, the IC50 of 112.7 ± 3.4 μg/mL was calculated for E.aevense extract using FIC assay. The extract was more active than AsA and less than EDTA. For the essential oil, 952.7 ± 15.2 and 1282.7 ± 12.7 μg/mL were calculated for the IC50 using RSA and FIC assays, respectively.

Table 2

TPC, TFC, DPPH RSA, and FIC of Equisetum arvense extract and essential oil

TPC mg GAE/g extract TFC (mg RE/g extract) RSA IC50 (μg/mL) FIC IC50 (μg/mL)
Extract 389.0 ± 6.4 57.6 ± 3.8 15.2 ± 1.4 112.7 ± 3.4
Essential oil 952.2 ± 15.2 1,282.7 ± 12.7
BHT 18.3 ± 1.1
TOC 32.4 ± 0.9
EDTA 56.2 ± 1.8
AsA 1371.2 ± 8.7

Values are presented as means ± SD (n = 3).

Previous studies have reported the ability of E. arvense extract to scavenge DPPH [9,19]. E. arvense from different locations in Romania was rich in polyphenols and flavonoids with a high ability to scavenge the free radical of DPPH [36], whereas 30% of RSA has been reported for E. hyemal [37]. A 0.675 mg/mL gallic acid equivalent has been reported for the hydroalcoholic extract of E. ramosissimum [38]. The extract of E. ramosissimum also scavenged the free radical of DPPH [39].

3.3 Cytotoxicity effect of E. arvense on LNCaP cell line

Figures 1 and 2 present the results of the MTT assay of E. arvense extract and essential oil against the human prostate cancer cell line (LNCaP cell line). In most studies on the evaluation of anti-prostate cancer activity, the MTT assay is run on the LNCaP cell line because it is known as the standard cell line. The cell line is androgen-responsive and derived from human prostate cancer with metastatic to bone. According to the results, the viability of the prostate cell line is reduced dose-dependently in the presence of the plant extract and essential oil. Furthermore, the cell viability depends on the treatment time. The IC50 of the plant extract was 43.2 ± 1.7, 29.3 ± 1.6, and 25.2 ± 1.3 μg/mL after treatment for 24, 48, and 72 h, respectively. The plant extract had higher activity than the essential oil with IC50 of 382.2 ± 13.6, 285.3 ± 5.7, and 218.9 ± 10.7 μg/mL for 24, 48, and 72 h treatment, respectively. In a comparison with previous studies on the anti-prostate cancer activity of the plant extract, E. arvense extract exhibited more activity against than Boswellia serrata extract [40], Scaphechinus mirabilis extract [41], and Corni fructus extract [42]. However, the anticancer activity of E. arvense extract was less than that of Linum usitatissimum extract against LNCaP cell line [30].

Figure 1 
                  Effect of Equisetum arvense extract on the viability of LNCaP cells. The viability percentage was measured using MTT assay. LNCaP cells were treated with different concentrations of the extract for 24, 48, and 72 h.
Figure 1

Effect of Equisetum arvense extract on the viability of LNCaP cells. The viability percentage was measured using MTT assay. LNCaP cells were treated with different concentrations of the extract for 24, 48, and 72 h.

Figure 2 
                  Effect of Equisetum arvense essential oil on the viability of LNCaP cells. The viability percentage was measured using MTT assay. LNCaP cells were treated with different concentrations of the extract for 24, 48, and 72 h.
Figure 2

Effect of Equisetum arvense essential oil on the viability of LNCaP cells. The viability percentage was measured using MTT assay. LNCaP cells were treated with different concentrations of the extract for 24, 48, and 72 h.

The diets, which are enriched in phenolic compounds, play a considerable role in preventing and treating prostate cancer [43,44]. According to our results, the extract of E. arvense presented a considerable cytotoxic effect on the LNCaP cell line. According to the previous reports, the presence of secondary metabolites such as polyphenols and flavonoids is the major reason for the ability of E. arvense extract to prevent the prostate cancer cell line. Among the phenolic and flavonoids reported for the extract of E. arvense, quercetin, luteolin, vanillic acid, caffeic acid, and ferulic acid reported as having considerable potential against different cancer cell lines [45,46,47]. Furthermore, the synergistic effect of polyphenols with chemotropic drugs is known as an effective strategy to treat cancer diseases [48,49].

A few studies have reported the anti-cancer activity of the plants from the Equisetum genus. In reported research, E. arvense exhibited a cytotoxic effect against the human leukemic cell line [50]. The ethanolic extract of E. arvense showed a cytotoxic effect on the human pancreatic carcinoma cell line [51]. The plant extract is also active against cervical, breast, and colorectal cell lines [12]. E. ramosissimum showed anticancer activity against three human melanoma cancer cell lines [39].

3.4 Detection of apoptosis by flow cytometry

Apoptosis and necrosis are known as the two main types of cell death. Apoptosis is programmed cell death. Apoptosis happens in two ways including (1) extrinsic pathway that is started by death receptor–ligand stimulation systems and (2) intrinsic pathway that takes place by DNA damage [3,6]. Figures 3 and 4 exhibit the flow cytometric analysis and the percentage for apoptosis by the extract of E. arvense. The prostate cancer cells were treated with E. arvense extract with concentrations of 25.0, 30.0, and 40.0 μg/mL, which were close to the obtained IC50 from the MTT assay. The results showed that the treated cells with E. arvense extract increased the apoptosis percentage considerably compared to the control. The highest result was calculated for the concentration of 40.0 μg/mL after 72 h with 31.6% apoptosis, while the minimum apoptosis (16.4%) was obtained for 25.0 μg/mL after 24 h.

Figure 3 
                  Flow cytometric evaluation of induced apoptosis using Propidium iodide staining by Equisetum arvense extract in LNCaP cells at different times and concentrations. a1–4 after 24 h; b1–4 after 48 h; and c1–4 after 72 h (the vertical axial shows Histogram details, and the horizontal axial shows FL2-H subset).
Figure 3

Flow cytometric evaluation of induced apoptosis using Propidium iodide staining by Equisetum arvense extract in LNCaP cells at different times and concentrations. a1–4 after 24 h; b1–4 after 48 h; and c1–4 after 72 h (the vertical axial shows Histogram details, and the horizontal axial shows FL2-H subset).

Figure 4 
                  PI-staining induced apoptosis on LNCaP cells. LNCaP cells were treated with different concentrations of Equisetum arvense extract for 24, 48, and 72 h.
Figure 4

PI-staining induced apoptosis on LNCaP cells. LNCaP cells were treated with different concentrations of Equisetum arvense extract for 24, 48, and 72 h.

4 Conclusions

The results of the present study revealed that thymol acetate, trans-carveol, thymol, and δ-element were the major components of E. arvense essential oil. The plant extract showed higher antioxidant activity than the essential oil and even the positive controls. The extract scavenged the free radical of DPPH with an IC50 of 15.2 ± 1.4 μg/mL. In the MTT assay, the plant extract prevented the growth of LNCaP as the selected prostate cancer cell line more than the plant essential oil with an IC50 of 25.2 ± 1.3 μg/mL after 72 h. The plant extract induced a 31.6% apoptosis in the cell line. According to the obtained results from the study, E. arvense extract can be used as herbal medicine for prostate cancer; however, further research especially in vivo evaluation should be carried out to evaluate the therapeutic potential of E. arvense against prostate cancer.

  1. Funding information: There is no external funding.

  2. Author contributions: Writing–original draft preparation, Hongyong Gu; data curation and software, Ting Yi; conceptualization and methodology, Pengxiu Lin; formal analysis, writing–review and editing, Jin Hu.

  3. Conflict of interest: The authors declare no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2022-06-15
Revised: 2022-08-08
Accepted: 2022-08-21
Published Online: 2022-11-11

© 2022 Hongyong Gu et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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