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Abstract

Objective: The comparison of chemical composition and antimicrobial activity of Dalbergia odorifera essential oils, obtained by hydrodistillation and supercritical carbon dioxide extraction methods. Methods: Their compositions and antimicrobial activity were investigated using gas chromatography-mass spectrometry (GC-MS) and microdilution methods, respectively. Results: Hydro-distilled essential oil (HD-EO) consisted of 8 components, accounting for 98.67%, whereas supercritical carbon dioxide extracted essential oil (SC-EO) consisted of 13 components, accounting for 87.90%. The significant differences between the compositions of these essential oils were nerolidol oxide Ⅰ (23.69% for HD-EO and 16.10% for SC-EO), nerolidol oxide Ⅱ (43.40% for HD-EO and 34.52% for SC-EO), and nerolidol oxide Ⅲ (3.61% for HD-EO and 7.27% for SC-EO). S. epidermidis and S. pneumoniae were more sensitive to HD-EO than to SC-EO. Moreover, HD-EO possessed anti-B. cereus and anti-S. dysenteriae activities, with minimal inhibitory concentration (MIC) values of 13.6 mg/mL. SC-EO exhibited anti-C. albicans activity with an MIC value of 2.9 mg/mL. Moreover, the essential oils were tested but found inactive against E. aerogenes, E. faecalis, K. pneumonia, P. vulgaris, S. typhi, S. typhimurium, or V. parahaemolyticus. Conclusion: These results support for the rational utilization and further development of D. odorifera essential oils.

Keywords

essential oil antimicrobial activity nerolidol oxide

Introduction

Infectious and foodborne diseases resulting from pathogens threaten public health and safety worldwide,¹ and they result in considerable economic losses.² At present, the clinical application of conventional antibiotics is limited because of adverse neurological effects,³ ototoxicity, nephrotoxicity,⁴ allergic reactions,⁵ and multidrug-resistant pathogens.⁶ Essential oils from aromatic plants possess a broad spectrum of antimicrobial activities and further medicinal properties.^7,8 Moreover, essential oils from plants have few side effects and are safe for the environment.⁹

Dalbergia odorifera T.Chen from Dalbergia genus is a medical aromatic plant that is widely distributed in Southeast and South Asia. The heartwood of this plant, known as “Jiangxiang”, is recorded in the Chinese Pharmacopoeia because of its ability to treat blood disorders, ischaemia, swelling, necrosis, and rheumatic pain.¹⁰ To date, the chemical profile of essential oils from its heartwood has revealed 31 terpenes, 5 aldehydes, 3 phenols, 3 ketones, 3 alcohols, 3 esters and 4 other components.^11,12 This plant has a broad spectrum of biological activities such as myocardial protective,¹³ antithrombotic, and analgesic activities.¹⁴ In addition, antimicrobial activities against Staphylococcus aureus, methicillin-resistant S. aureus, Pseudomonas aeruginosa, and Bacillus subtilis, have been reported.¹⁵

Supercritical carbon dioxide extraction is a novel effective approach for extracting the essential oils because of its high selectivity, low extraction temperature, short possessing time, and benign environment.¹⁶ It has been reported that D. odorifera essential oil extracted by supercritical carbon dioxide can reach a higher yield than that extracted by the hydrodistillation method.¹⁷ However, comparisons of chemical compositions and antimicrobial activities of the essential oils obtained by supercritical carbon dioxide extraction and hydrodistillation methods are scarce.

Therefore, the present study investigated the chemical composition of D.odorifera essential oils obtained by hydrodistillation and supercritical carbon dioxide extraction methods by gas chromatography-mass spectrometry (GC-MS) and evaluated their antimicrobial activities against microorganisms by the microdilution method for the rational utilization and further development of these essential oils.

Materials and Methods

Plant Material

The heartwood of D. odorifera were purchased from Chinese Herbal Medicine Market, Yulin, Guangxi, China in September 2022, and identified by Dr. Yuekui Liao, at Guangxi University of Chinese Medicine. A voucher specimen (No. 20220902) was deposited at Key Laboratory of Modern Preparation of Traditional Chinese Medicine, Ministry of Education, Jiangxi University of Chinese Medicine, Nanchang, China.

Chemicals and Reagents

Anhydrous sodium sulphate was analytical grade purchased from Xilong Scientific Co., Ltd., Guangdong, China. n-Alkanes (C₇-C₄₀, 1 × 10³ mg/L) standard was purchased from o2si smart solutions Company, South Carolina, USA. β-Cedrene (98%) was purchased from Wuhan Zbsci Co., Ltd., Wuhan, China. trans-Nerolidol (98%) was obtained from Chengdu Must Bio-technology Co., Ltd., Chengdu, China. (2Z,6E)-Farnesol (90%) was obtained from Guangzhou Kemeng Biotechnology Co., Ltd., Guangzhou, China. (E,E)-Farnesol (98%) was purchased from Sichuan Vicki Biotechnology Co., Ltd., Sichuan, China. Nerolidol oxide Ⅰ∼Ⅲ successfully were prepared in our laboratory. Ceftazidime, fluconazole and glycerol were purchased from Sigma-Aldrich in Missouri, USA.

Extraction of Essential Oils

The heartwood of D. odorifera were smashed mechanically into small granules before extraction. The granular samples (400.0 g) were placed in a clean 5 L round-bottomed flask and purified water (2.0 L) were subjected to steam distillation for 4 h and conducted at normal pressure in a Clevenger-type apparatus. The collected essential oil (1.84 mL, ρ = 0.92 g/mL, 0.46% v/w) was dried over anhydrous sodium sulfate to remove the remaining water and stored in a sealed glass bottle at 4 °C until further analysis.

The granular samples (257.7 g) were subjected to supercritical fluid extraction using supercritical CO₂ as the solvent with a HA220-50-06 supercritical CO₂ extraction apparatus (Nantong Hua’ an Supercritical Extraction Co., Ltd., Nantong, China). The samples were placed in an extraction axe (1.0 L) and heated at 40 °C by water heating bath system. The separators including Ⅰ and Ⅱ reached at different temperature by water heating bath systems. The parameters were set at 50 °C for separator Ⅰ and the room temperature for separator Ⅱ. Then, the cooling bath system reached temperature at 8 °C to prevent overheating and precool the liquid CO₂, improving CO₂ isolated from essential oil. The CO₂ intake valve and compressor were turned on for pressuring the system to desired operating conditions. The pressure of extractor and separator Ⅰ were set at 20 MPa and 6.5 MPa, respectively. The extraction time was 3 h since there was not significantly increasing essential oil with longer extraction time. The essential oil (4.63 mL, ρ = 0.93 g/mL, 1.80% v/w) was collected from the separators and stored at 4 °C until further analysis. The essential oil yields were determined by the following equation: Yield (mL/100 g) = V_EO/m × 100, where V_EO is the volume of the extracted essential oil (mL) and m is the weight of the granular sample (g).

Gas Chromatography-Mass Spectrometry (GC-MS)

The GC-MS analysis of the essential oils was carried out on an Agilent 7890B-5977A Gas chromatography-mass spectrometer with a HP-5MS capillary column (30 m × 250 μm, film thickness 0.25 μm). The column temperature was started at 60 °C for 2 min, climbed to 115 °C at a rate of 10 °C/min kept for 2 min, increased to 135 °C at a rate of 1 °C/min held for 2 min, then increased to 280 °C at a rate of 10 °C/min and remained for 5 min. The injection temperature was set at 250 °C. The temperatures of detector and transfer line were 280 °C. Helium as the carrier gas was at a flow rate of 1 mL/min with the split rate 50:1. The injection volume was 1 μL. The mass spectrometer parameters were as follows: ionization energy was 70 eV, the temperature of ionization source was 230 °C, and the mass range 35 to 500 m/z.

The identification of the essential oils components was based on the comparison of calculated retention indices (RI) with RI reported in NIST Chemistry WebBook and literature,^17-23 computer matching of the mass spectra with NIST20 database as well. The calculated RI was relative to homologous series of n-alkanes C₇-C₄₀ under the same experimental condition of the essential oils. Moreover, the structural isomers displayed similar mass spectrum with major fragments. Some standard pure components, such as β-cedrene, trans-nerolidol, (2Z,6E)-farnesol, (E,E)-farnesol, were also used for identification.

Antimicrobial Activity

The microbial strains were purchased from the American Type Culture Collection (ATCC) and National Center for Medical Culture Collections (CMCC). The antimicrobial activities of essential oils of D. odorifera were assessed against four Gram-positive bacteria including Bacillus cereus (ATCC 1778), Enterococcus faecalis (ATCC 29212), Staphylococcus epidermidis (CMCC 26069), Streptococcus pneumoniae (CMCC 31001), seven Gram-negative bacteria including Enterobacter aerogenes (ATCC 13048), Klebsiella pneumonia (CMCC 46117), Proteus vulgaris (CMCC 49027), Salmonella typhi (CMCC 50071), Salmonella typhimurium (ATCC 14028), Shigella dysenteriae (CMCC 51105), Vibrio parahaemolyticus (ATCC 17802), and one fungus Candida albicans (ATCC 10231). Overnight broth cultures were prepared for each strain above and the concentration were adjusted to 0.5 McFarland standard turbidity by PBS buffered solution.

According to the Clinical Laboratory and Standards Institute (CLSI) guideline, the antimicrobial activities of D. odorifera essential oils were determined by microdilution assay. The EOs were dissolved in dimethyl sulfoxide (DMSO) and then assessed in a concentration range from 0.01 to 0.25 mL/mL by a series of doubling dilution in sterile 96 well trays using LB broth (Guangdong Huankai Biotechnology Co., Ltd, Shaoguan, China). 100 μL LB broth medium and 10 μL suspension of the microorganisms were added in the 96 well trays containing a desired range of the diluted EOs. Inoculated trays were incubated at 37 °C for 24 h. The optical density (OD) values of the incubation time at 0 and 24 h were measured using a microplate manager at 600 nm. Then MIC was recorded as the lowest concentration of the EOs restricting growth of OD at 24 h. Ceftazidime (1 mg/mL) and Fluconazole (1 mg/mL) were used as positive controls for bacteria and fungus separately. Meanwhile glycerol was a negative control. All assays were performed in triplicate and performed in a biological safety cabinet.

Statistical Analysis

All data were statistically processed using SPSS Statistics soft ware (version 21.0 for windows, SPSS Inc.). The results are presented as the mean value ± standard deviation.

Results

Chemical Composition of Essential Oils

The GC/MS analysis (Supplemental Figures S1-S8) provided information on the chemical composition of HD-EO and SC-EO, the results of which are presented in Table 1.

Table 1.

Chemical Composition from Essential Oils of Dalbergia odorifera Extracted by Hydrodistillation and Supercritical Carbon Dioxide.

No.	Component	Formula	RI_a	RI_b	Area (%)		Identification	Reference
No.	Component	Formula	RI_a	RI_b	HD-EO	SC-EO	Identification	Reference
1	β-Cedrene	C₁₅H₂₄	1417	1419	0.05	nt	MS,RI,CO-ST	¹⁸
2	Cabreuva oxide D	C₁₅H₂₄O	1474	1479	0.09	nt	MS,RI	¹⁸
3	2-[5-(1-Hydroxyethyl)- 5-methyl-tetrahydrofuran- 2-yl]propan-1-ol	C₁₀H₂₀O₃	1537	−	nt	0.23	MS	−
4	Lilac alcohol epoxide	C₁₀H₁₈O₃	1550	−	0.25	0.32	MS	−
5	Nerolidol oxide Ⅰ	C₁₅H₂₆O₂	1558	−	23.69	16.10	MS	^19,20
6	trans-Nerolidol	C₁₅H₂₆O	1564	1561	26.58	25.13	MS,RI,CO-ST	¹⁸
7	Nerolidol oxide Ⅱ	C₁₅H₂₆O₂	1576	−	43.40	34.52	MS	^19,20
8	Nerolidol oxide Ⅲ	C₁₅H₂₆O₂	1631	−	3.61	7.27	MS	^19,20
9	Nerolidol oxide Ⅳ	C₁₅H₂₆O₂	1634	−	1.00	2.06	MS	^19,20
10	Humulol	C₁₅H₂₆O	1648	1618	nt	0.19	MS,RI	²¹
11	cis-Nerolidyl acetate	C₁₇H₂₈O₂	1658	1676	nt	0.99	MS,RI	¹⁸
12	(2Z,6E)-Farnesol	C₁₅H₂₆O	1732	1722	nt	0.32	MS,RI,CO-ST	¹⁸
13	(E,E)-Farnesol	C₁₅H₂₆O	1741	1742	nt	0.68	MS,RI,CO-ST	¹⁸
14	Nerolidol formate	C₁₆H₂₆O₂	1751	1752	nt	0.04	MS,RI	²²
15	(2E,6Z)-Farnesol	C₁₅H₂₆O	1755	1746	nt	0.05	MS,RI	²³
		Total (%)				98.67	87.90
		Oxygenated monoterpenes (%)				0.25	0.55
		Hydrocarbon sesquiterpenes (%)				0.05	nt
		Oxygenated sesquiterpenes (%)				98.37	87.35

RI_a: retention index calculated according to a series of n-alkanes (C₇-C₄₀) on a HP-5MS capillary column; RI_b: retention index from literature;

HD-EO: essential oil extracted by hydrodistillation; SC-EO: essential oil extracted by supercritical carbon dioxide; nt: not detect; MS: identification by computer matching of the mass spectra with NIST20 database; CO-ST: co-injection/comparison to RI and MS of standards.

The extraction yield of the colourless essential oil obtained by the hydrodistillation method was approximately 0.46 ± 0.01 mL/100 g. Eight components accounting for 98.67% of HD-EO were identified, including 6 oxygenated sesquiterpenes (98.37%), 1 oxygenated monoterpene (0.25%), and 1 hydrocarbon sesquiterpene (0.05%) (Figure 1 and Table 1). Among them, nerolidol oxide Ⅱ (43.40%), trans-nerolidol (26.58%), nerolidol oxide Ⅰ (23.69%), nerolidol oxide Ⅲ (3.61%), and nerolidol oxide Ⅳ (1.00%) were the top five components with relatively high contents in the essential oil. In addition, the extraction yield of the clear claret red essential oil obtained by supercritical carbon dioxide extraction was approximately 1.80 ± 0.01 mL/100 g. Thirteen components accounting for 87.90% of SC-EO were identified, including 11 oxygenated sesquiterpenes (87.35%) and 2 oxygenated monoterpenes (0.55%). Among them, five major components with relatively high contents in the essential oil were nerolidol oxide Ⅱ (34.52%), trans-nerolidol (25.13%), nerolidol oxide Ⅰ (16.10%), nerolidol oxide Ⅲ (7.27%), and nerolidol oxide Ⅳ (2.06%) (Figures 1 and 2).

Figure 1.

Total ion chromatogram (TIC) of essential oils from Dalbergia odorifera extracted by hydrodistillation and supercritical carbon dioxide: (A) is TIC of HD-EO; (B) is TIC of SC-EO. Number of peaks were indicated in Table 1.

Figure 2.

Chemical structures of major compositions from essential oils of Dalbergia odorifera.

Antimicrobial Activity

In the present study, S. epidermidis and S. pneumoniae were more sensitive to HD-EO than to SC-EO. Compared with SC-EO, HD-EO exhibited stronger anti-S. pneumoniae activity, with an MIC value of 3.4 mg/mL. However, HD-EO inhibited the growth of B. cereus and S. dysenteriae with the same MIC value of 13.6 mg/mL, whereas SC-EO not. In contrast, SC-EO inhibited the growth of C. albicans, with an MIC of 2.9 mg/mL, but HD-EO not. In addition, neither HD-EO nor SC-EO showed antimicrobial activity against E. aerogenes, E. faecalis, K. pneumonia, P. vulgaris, S. typhi, S. typhimurium, or V. parahaemolyticus (Table 2).

Table 2.

Antimicrobial Activity of Essential Oils of Dalbergia odorifera Extracted by Different Methods, Ceftazidime and Fluconazole.

Type of micro-organisms	Name of micro-organisms	MICs of EOs		MICs of antibiotics
Type of micro-organisms	Name of micro-organisms	HD-EO	SC-EO	Ceftazidime	Fluconazole
Bacteria strain	Streptococcus pneumoniae	3.4	7.3	1.0	nt
	Staphylococcus epidermidis	13.6	14.5	1.0	nt
	Shigella dysenteriae	13.6	nt	0.1	nt
	Bacillus cereus	13.6	nt	1.0	nt
	Enterobacter aerogene	nt	nt	0.5	nt
	Enterococcus faecalis	nt	nt	0.16	nt
	Klebsiella pneumonia	nt	nt	0.5	nt
	Proteus vulgaris	nt	nt	0.5	nt
	Salmonella typhi	nt	nt	0.5	nt
	Salmonella typhimurium	nt	nt	0.25	nt
	Vibrio parahaemolyticus	nt	nt	0.5	nt
Fungus	Candida albicans	nt	2.9	nt	125.0

HD-EO: essential oil of D. odorifera extracted by hydrodistillation; SC-EO: essential oil of D. odorifera extracted by supercritical carbon dioxide; MIC: minimal inhibitory concentration; nt: not tested; Values given as mg/mL for the essential oils and as μg/mL for antibiotics.

Discussion

In our study, the yield of SC-EO was approximately 4 times greater than that of HD-EO. The colours of the samples were significantly different. The extraction yields of these two oils were similar to those reported previously.¹⁷ Moreover, the major components, including trans-nerolidol and nerolidol oxides, in SC-EO and HD-EO were also similarly reported by Nan et al²⁴ and Zhao et al²⁵ Compared with those in SC-EO, the relative contents of nerolidol oxide Ⅱ, trans-nerolidol, and nerolidol oxide Ⅰ in HD-EO were significantly greater, whereas those of nerolidol oxide Ⅲ and nerolidol oxide Ⅳ were lower. Moreover, some components, such as humulol, cabreuva oxide D, and nerolidol formate, were also discovered in D. odorifera essential oils for the first time. Up to now, the identification of the structural isomers, such as nerolidol oxide I∼Ⅳ, still remains challenging because of the limitations of corresponding records in the database. What is more, the chemical compositions of these two essential oils should be also investigated by gas chromatography with a flame ionization detector (GC-FID) in future research.

Previous reports have reported, the significant antibacterial activities of HD-EO for Streptococcus mutans, Salmonella enteritidis, B. subtilis,²⁶ and methicillin-resistant S. aureus.²⁷ The present findings may be associated with the difference in the relative contents of trans-nerolidol and nerolidol oxides, as the major components. trans-Nerolidol is also a prominent component of the essential oils from Magydaris tomentosa flowers (35.4%).²⁸ In the present study, the antimicrobial activities of these essential oils against S. epidermidis were strongly correlated with the content of trans-nerolidol. Therefore, it indirectly supported that HD-EO had greater potential against S. epidermidis than SC-EO. Moreover, to the best of our knowledge, nerolidol oxides have rarely been reported to kill these microbes in previous reports.

Conclusion

In this study, these essential oils, extracted using hydrodistillation and supercritical carbon dioxide extraction methods, showed significantly different chemical composition and antimicrobial activity. These findings provide data to support for the rational utilization and further development of D. odorifera essential oil.

Supplemental Material

sj-docx-1-npx-10.1177_1934578X251313966 - Supplemental material for Comparison of Chemical Composition and Antimicrobial Activity of Dalbergia odorifera Essential Oils Obtained by Hydrodistillation and Supercritical Carbon Dioxide Extraction Methods

Supplemental material, sj-docx-1-npx-10.1177_1934578X251313966 for Comparison of Chemical Composition and Antimicrobial Activity of Dalbergia odorifera Essential Oils Obtained by Hydrodistillation and Supercritical Carbon Dioxide Extraction Methods by YingYi Wang, GuangQiang Ma, XiaoYing Huang, XiaoMan Li and Feng Shao in Natural Product Communications

Footnotes

Acknowledgments

The authors would like to thank Dr. Yuekui Liao (Guangxi University of Chinese Medicine) for her identifying plant material and support.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethical Approval

Ethical Approval is not applicable for this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Ganpo Juncai-Training Program for Academic and Technical Leaders in Major Disciplines of Jiangxi Province (Leading Talents-Academic Category), China (Grant no. 20243BCE51019), National Natural Science Foundation of China (Grant no. 82160733), Natural Science Foundation of Jiangxi Province, China (Grant no.20232BAB206180), Science and Technology Project of Jiangxi Provincial Administration of Traditional Chinese Medicine (Grant no.2023B1324).

ORCID iD

Feng Shao

Statement of Human and Animal Rights

This article does not contain any studies with human or animal subjects.

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There are no human subjects in this article and informed consent is not applicable.

Supplemental Material

Supplemental material for this article is available online.

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