Prime Archives in Plant Sciences

Book Chapter

Antimicrobial Activity and Constituents of Leaf and Pseudo-Stem Essential Oils of Zingiber zerumbet

Le T. Huong1,*, Hoang V. Chinh2, Do. N. Dai3, Olanrewaju I. Eresanya4 and Isiaka A. Ogunwande5,*

1School of Natural Science Education, Vinh University, 182 Le Duan, Vinh City, Nghệ An Province, Vietnam 2Faculty of Natural Science, Hong Duc University, 565 Quang Trung, Đông Vệ, Thanh Hóa City, Thanh Hóa Province, Vietnam 3Faculty of Agriculture, Forestry and Fishery, Nghe An College of Economics, 51-Ly Tu Trong, Vinh City, Nghe An Province, Vietnam 4Department of Chemistry, Faculty of Basic Health Sciences, Eko University of Medicine and Health Sciences, Ijanikin, Nigeria 57, University Area, Aleku, Osogbo, Nigeria

*Corresponding Authors: Isiaka A Ogunwande, 7, University Area, Aleku, Osogbo, Nigeria, Email: [email protected]

Le T. Huong, School of Natural Science Education, Vinh University, 182 Le Duan, Vinh City, Nghệ An Province, Vietnam, Email: [email protected]

Published February 26, 2020

How to cite this book chapter: Le T. Huong, Hoang V. Chinh, Do. N. Dai, Olanrewaju I. Eresanya, Isiaka A. Ogunwande. Antimicrobial Activity and Constituents of Leaf and Pseudo- Stem Essential Oils of Zingiber zerumbet. In: Grace Q Chen, editor. Prime Archives in Plant Sciences. Hyderabad, India: Vide Leaf. 2020.

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© The Author(s) 2020. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Acknowledgments: This research was funded by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number: 106.03-2017.328.

Abstract

This paper reports the chemical constituents and antimicrobial activities of essential oil of the leaf and pseudo-stem of Zingiber zerumbet (L.) Smith. The air-dry samples were subjected to hydrodistillation process using Clevenger-apparatus to obtained essential oils. By using GC and GC/MS, 55 and 25 compounds representing 96.2% and 94.4% of the total oil contents were determined from essential oils of the leaves and pseudo-stem respectively. The main compounds of the leaf oil were -pinene (30.8%), -caryophylene (13.0%) and caryophyllene oxide (12.0%) while zerumbone (64.5%) was the most abundant constituents found in the pseudo-stem oil. The antimicrobial activity (MIC) was determined by microdilution broth susceptibility assay. The results of antimicrobial testing indicated that Z. zerumbet leaf oil exhibited potent antimicrobial action against Aspergillus niger (ATCC 9763) with minimum inhibitory concentration (MIC) of 25 µg/mL. The pseudo-stem oil only displayed antimicrobial activity towards B. subtilis (ATCC 11774) with MIC of 50.0 µg/mL.

Keywords

Zingiber zerumbet; Essential Oil; Monoterpenes; Sesquiterpenes; Antimicrobial Activity

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Introduction

Zingiber zerumbet (L.) Smith is a species in the family of Zingiberacea plants. The plant is edible among ginger species. The volatile and non-volatile extracts have been widely investigated for their chemical constituents and biological activities which they exhibited [1]. Literature information has shown the essential oil derived from Z. zerumbet from all over the world possessed several biological activities such as antimicrobial [1], larvicidal [1], anti-nociceptive [2,3], anti- inflammatory [4], antioxidant [5], antifungal [6] and antimycotoxin [6]. Moreover, Z. zerumbet oils were toxic, thus exhibiting insecticidal actions against insects [7,8]. Essential oils from the rhizomes of Z. zerumbet grown in Vietnam were recently shown to demonstrate both larvicidal and antimicrobial activities [9]. The various biological activities exhibited by extracts and essential oils of Z. zerumbet from other parts of the world have been documented [1]. In recent years, the role of other essential oils as feed supplement and food additives apart from their biological activities, have attracted attention. Some essential oils have been used as feed supplement to ruminant animals because they are stable during feed processing [10]. The potential of dietary essential and aromatic plants to improve the oxidative stability of meat obtained from broilers, hens or turkeys, has been demonstrated [11,12].

The chemical composition of essential oils of Z. zerumbet has been widely studied world over. A survey of literature has shown that zerumbone and its analogues was always the main chemical compound of the essential oil. However, the contents of zerumbone varied from one analysed sample to another in the same region, and from one region to another. The constituents occurring in higher amount in sample of Z. zerumbet rhizome oil analysed from China [8] were zerumbone (40.2%), α- caryophyllene (8.6%) and humulene epoxide II (7.3%). Zerumbone (36.12%) and humulene (10.03%) were reported as main compounds of oil sample from Malaysia [3], while another sample from Malaysia [13] contained zerumbone (60.4%) and humulene epoxide II (20.84%) as significant compounds. Likewise zerumbone (46.37% and 39.09%) and caryophyllene

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(28.01% and 25.81%) were the main constituents obtained from samples analysed in Thailand [5], while the same authors also reported the abundance of zerumbone (11.44%-45.38%) and terpinen-4-ol (25.47%-31.06%) from another oil sample collected from other region of Thailand. A sample of Z. zerumbet oil collected and analyzed also from Thailand [14] contained α- humulene (31.9%) and zerumbone (31.7%) as major constituents. The main constituents of the rhizome oil of Z. zerumbet from India [6] were zerumbone (49.8%) and α- caryophyllene (20.1%). Also, zerumbone (74.82%) constituted the bulk of the oil sample analysed from another location in India [15].

However, low amount or total absence of zerumbone has been reported from some essential oils of Z. Zerumbet around the world. For examples, the main constituents of the root oil of Z. zerumbet from Vietnam [16] were -citral (26.1%), camphene (16.3%) and sabinene (14.6%) while the flower oil contained (E)-nerolidol (34.9%), β-caryophyllene (10.2%), linalool (17.1%). (E)-Nerolidol (21.4%), α-pinene, (10.3%) and β-pinene (31.4%) make up the compositions of the leaf oil of Z. zerumbet from Reunion Island [17]. The contents of zerumbone from sample analyzed in Vietnam [16] and Reunion Island [17] were insignificant.

The aim of the present study was to determine the chemical composition, establish the larvicidal potential and evaluate the antimicrobial activity of essential oil from the rhizome of Z. zerumbet growing in Vietnam. Recently, we have reported the chemical composition and antimicrobial activity of essential oils from plants growing in Vietnam [18,19]. This is part of our extensive research directed towards the characterization of the chemical constituents and biological activities of economically important flora of Vietnam.

Materials and Methods Plants Collection

The leaves and pseudo-stems of Z. zerumbet were collected from Bến En National Park, Thanh Hóa Province, Vietnam, in August

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2018. A voucher specimen, HVC 700, was deposited at the Botany Museum, Vinh University, Vietnam. Plant samples were air-dried prior to extraction.

Hydrodistillation of the Oils

For this experiment, 500 gram each of the air-dried samples was used during separate process. A known weight of samples was separately and carefully introduced into a 5 L flask and distilled water was added until it covers the sample completely. Essential oils were obtained hydrodistillation which was carried out in an all glass Clevenger-type distillation unit designed according to Vietnamese Pharmacopoeia [20] as described in previous studies [18,19]. The distillation time was 3 h and conducted at normal pressure. The volatile oils distilled over water and were collected by running through the tap in the receiver arm of the apparatus into clean and previously weighed sample bottles. The oils were kept under refrigeration (4oC) until the moment of analyses as described in previous studies [18,19].

Gas Chromatography (GC) Analysis

Gas chromatography (GC) analysis was performed on an Agilent Technologies HP 6890 Plus Gas chromatograph equipped with a FID and fitted with HP-5MS column (30 m x 0.25 mm, film thickness 0.25 m, Agilent Technology). The analytical conditions were: carrier gas He (1 mL/min), injector temperature at 250oC, detector temperature 260oC, column temperature programmed from 40oC (2 min hold) to 220oC (10 min hold) at 4oC/min. Samples were injected by splitting and the split ratio was 10:1. The volume of diluted oil in hexane (1: 10) injected was 1.0 L. Inlet pressure was 6.1 kPa. Each analysis was performed in triplicate. The relative amounts of individual components were determined on normalized percentages.

Gas Chromatography (GC) Analysis-Mass Spectrometry (GC/MS) Experiment

An Agilent Technologies HP 6890N Plus Chromatograph fitted with capillary HP-5 MS column (30 m x 0.25 mm, film thickness

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0.25 m) and interfaced with a mass spectrometer HP 5973 MSD was used for this experiment, under the same conditions as those used for gas chromatography analysis as described in previous studies [18,19]. The GC conditions were the same as described above with He (1 mL/min) as carrier gas. The MS conditions were as follows: ionization voltage 70eV; emission current 40 mA; acquisitions scan mass range of 35-350 amu at a sampling rate of 1.0 scan/s.

Identification of the Components of the Oils

The identification of constituents from the GC/MS spectra of Z. zerumbet was performed on the basis of comparison of retention indices (RI) determined with reference to a homologous series of n-alkanes (C4-C40), under identical experimental conditions. In some cases, co-injection with known compounds under the same GC conditions was employed. The mass spectral (MS) fragmentation patterns were checked with those of other essential oils of known composition [21] and with those in the literature as described in other studies [18,19].

Antimicrobial Activity

Eight standardized ATCC strains from laboratory stock cultures were used in the evaluation of the antimicrobial activity of the oils of Z. zerumbet. The Gram negative strains were Escherichia coli (ATCC 25922) and Pseudomonas aeruginosa (ATCC 25923). The Gram positive strains were Bacillus subtilis (ATCC 11774) and Staphylococcus aureus subsp. aureus (ATCC 11632), Aspergillus niger (ATCC 9763) and Fusarium oxysporum (ATCC 48112). Two strains of yeast, Candida albicans (ATCC 10231) and Saccharomyces cerevisiae (ATCC 16404) were also used for the experiment. Testing media included Mueller-Hinton Agar (MHA) used for bacteria and Sabouraud Agar (SA) used for fungi. The Minimum inhibitory concentration (MIC) values were measured by the microdilution broth susceptibility assay [22,23]. For the assays, the essential oil was diluted with DMSO and loaded into the microtiter plate with each of the microbial strains. The plate was then incubated overnight at 37oC. One hundred microlitre of microbial culture

6 www.videleaf.com Prime Archives in Plant Sciences of an approximate inoculums size of 1.0 x 106 CFU/mL was added to all well and incubated at 37oC for 24 h. The last row, containing only the serial dilutions of sample without microorganisms, was used as a negative control. Sterile distilled water and DMSO served as a positive control. The MIC values were determined as the lowest concentration of the test sample that completely inhibits the growth of microorganisms.

Statistical Analysis

Statistical analysis of the differences between mean values obtained for experimental groups were calculated as a mean of standard deviation (SD) of four independent measurements using Microsoft excel program 2003.

Results and Discussion

The essential oil of Z. zerumbet were obtained in yields of 0.31% (±0.01, v/w, leaf) and 0.22% (±0.01, v/w, pseudo-stem), based on a dry weight basis. The colour of the oils was light yellow. As could be seen in Table 1, the compounds including their percentages and retention indices deduced on HP-5MS column were indicated. By using GC/MS, 55 compounds accounting for 96.2% of the oil contents were identified in the leaf oil. The main classes of compound in the leaf oil were monoterpene hydrocarbons (48.0%), sesquiterpene hydrocarbons (21.9%) and oxygenated sesquiterpenes (17.8%). The major constituents of the leaf oil were -pinene (30.8%), -caryophylene (13.0%) and caryophyllene oxide (12.0%). In addition, -pinene (7.8%), phytol (4.4%), -humulene (3.5%), (E)--ocimene (2.3%) and limonene (1.5%) were identified in amount greater than 1%. The abundance of -caryophylene and low content of zerumbone was in agreement from data obtained previously from Vietnam [16] and Reunion Island [17]. From the pseudo-stem oil, 25 constituents representing 94.4% of the volatile contents were identified. The oxygenated sesquiterpenes (82.9%) represent the most abundant class of compound in the oil sample. The compounds occurring in higher quantity includes zerumbone (64.5%), caryophyllene oxide (5.7%) and camphor (5.2%).

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Table 1: Constituents of essential oils from the leaf and pseudo-stem of Z. zerumbet.

Compoundsa RIb Percent composition RIc Leaf Pseudo-stem -Thujene 929 926 0.1 - -Pinene 938 932 7.8 0.1 -Fenchene 952 950 0.1 - Camphene 954 952 0.3 0.6 Sabinene 978 977 2.3 - -Pinene 985 980 30.8 0.4 Myrcene 991 988 0.6 - -3-Carene 1015 1014 1.0 - o-Cymene 1029 1028 0.7 - Limonene 1033 1030 1.5 - -Phellandrene 1034 1032 0.3 - 1,8-Cineole 1036 1034 - 0.7 (Z)--Ocimene 1037 1037 0.2 - (E)--Ocimene 1048 1044 2.3 - Fenchone 1095 1094 - 0.2 Linalool 1102 1100 - 0.9 Nonanal 1104 1102 0.1 - o-Guiacol 1107 1108 0.2 - 4,8-Dimethylnona-1,3,7- 1116 1118 0.1 - triene endo-Fenchol 1122 1122 - 0.1 cis-Sabinol 1149 1150 0.6 - Camphor 1154 1154 - 5.2 Camphene hydrate 1159 1160 - - Pinocarvone 1171 1170 0.3 - Borneol 1176 1177 - 0.9 Terpinen-4-ol 1186 1186 0.1 0.4 -Terpineol 1199 1189 - 0.6 Myrtenal 1205 1210 0.9 - Fenchyl acetate 1226 1228 0.3 - Bornyl acetate 1292 1289 - 0.1 (E)-Anethole 1293 1290 0.4 - Isobornyl acetate 1295 1298 - - Myrtenyl acetate 1331 1335 0.2 - -Terpinyl acetate 1355 1354 - 0.1 -Copaene 1387 1387 0.2 - (E)-Methyl cinnamate 1392 1390 0.6 - cis--Elemene 1402 1400 0.3 - -Gurjunene 1423 1423 0.3 - -Caryophylene 1436 1429 13.0 0.3 trans--Bergamotene 1444 1444 0.5 -

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-Guaiene 1449 1449 0.2 - Geranylacetone 1455 1452 0.5 - (Z)--Farnesene 1458 1458 0.1 - -Humulene 1470 1470 3.5 0.6 9-epi-(E)-Caryophyllene 1477 1475 0.2 - -Zingiberene 1495 1497 0.8 - -Selinene 1502 1505 0.8 0.3 (E,E)--Farnesene 1510 1508 0.2 - -Selinene 1511 1510 0.4 - -Bulnesene 1519 1518 0.1 - -Sesquiphellandrene 1532 1532 0.1 - -Cadinene 1534 1532 0.2 - Elemicine 1559 1560 0.8 - (E)-Nerolidol 1569 1568 0.8 - Spathulenol 1598 1597 0.6 - Caryophyllene oxide 1605 1610 12.0 5.7 Humulene epoxide I 1618 1620 0.2 2.5 Humulene Epoxide II 1630 1632 1.3 2.0 Humulene epoxide III 1651 1652 - - -Eudesmol 1672 1762 0.8 0.6 neo-Intermedeol 1676 1676 0.4 - 14-Hydroxy-9-epi-(E)- 1689 1690 0.2 0.4 caryophyllene -Bicyclofarnesal 1697 1698 0.2 1.4 Zerumbone 1756 1754 0.2 64.5 -Bicyclohomofarnesal 1826 1830 0.6 2.2 6,10,14- 1845 1843 0.5 3.6 Trimethylpentadecan-2- one Phytol 2114 2119 4.4 - Total 96.4 94.3 Monoterpene hydrocarbons 48.0 1.1 Oxygenated monoterpenes 3.9 9.1 Sesquiterpene hydrocarbons 21.9 1.2 Oxygenated sesquiterpenes 17.8 82.9 Diterpenes 4.4 - Non-terpenes 0.4 - aElution order on HP-5MS column; bRetention indices on HP-5MS column; cLiterature retention indices; -not identified

A noteworthy observation was that, zerumbone, the main compound in the present study, was also the main compound of Z. zerumbet reported from other region of the world. However, the quantity of this compound, zerumbone, varied from one geo- graphical location to another. The percentage of zerumbone in

9 www.videleaf.com Prime Archives in Plant Sciences the present study was larger than amounts reported for oils analyzed from India [6], Malaysia [3], Thailand [5,14] and China [8]. However, other analyzed samples from Malaysia [13] and India [15] contain higher amount of zerumbone when compared with this study. This variation in the nature of the chemical constituents may be due to several factors which include nature and age of plant, parts of plant being analysed, handling and harvesting procedure as well the differences in the environmental and climatic conditions between various points of analysis.

Antimicrobial Activity of the Oil

The results obtained from the antimicrobial study on essential oils of Z. zerumbet could be seen in Table 2. The data indicated that the leaf oil sample displayed antibacterial activity and thus inhibitory the growth of A. niger with MIC of 25.0μg/mL. On the other hand, the pseudo-stem oil displayed antimicrobial activity against D. cerues with MIC of 50.0μg/mL. However, the studied leaf and pseudo-stem oils of Z. zerumbet were ineffective towards other microorganisms used in the study.

Table 2: Antimicrobial activity of the leaf and pseudo-stem oils of Z. zerumbet.

Type MIC (g/mL) Microorganisms Pseudo- Leaf stem E. coli (ATCC 25922) Gram- positive - - P. aeruginosa (ATCC 25923) Gram- positive - - B. subtilis (ATCC 11774) Gram- 50.0 ± 0.500 - negative S. aureus subsp. aureus (ATCC Gram- - - 11632) negative A. niger (ATCC 9763) Mould - 25.0 ± 0.000 F. oxysporum (ATCC 48112) Mould - - S. cerevisiae (ATCC 10231) Yeast - - C. albicans (ATCC 16404) Yeast - -

- no activity

The effective antimicrobial action exhibited by Z. zerumbet oils towards A. niger and B. cereus was noteworthy. Z. zerumbet oil was reported previously to displayed antimicrobial action against

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A. flavus and A. ochraceus with MIC values of 160 and 175 ppm [6]. Therefore, it may be postulated that the essential oil of Z. zerumbet oil have good activity against Aspergillus species. In addition, the ineffectiveness of the oil of Z. zerumbet against other microorganism was in agreement with reports from Malaysia in which no activity was shown towards A. niger, C. albicans among others [1]. However, the oils of Z. zerumbet from other regions have shown potency against some other microbes [1] contrary to the activity of the investigated oil sample. For example, sample of Z. zerumbet oil from Indonesia have proved effective against E. coli, P. aeruginosa and Salmonella typhi with MIC of 1.25, 1.25 and 0.625 mg/mL [24]. The potency of Z. zerumbet essential oil as a therapeutic agent against S. aureus, B. cereus, P. aeruginosa and E. coli has been reported [25]. It is well known that there are variations in the toxicity of essential oils against different species of pathogens [18]. This was mainly due to differences in the nature and amount of chemical constituents identified in the oil samples.

The observed antimicrobial activity of the pseudo-stem oil may be attributed to the main compound (zerumbone). The synergistic action of some other minor compounds may also be taken into consideration. It has been reported that zerumbone exhibited a number of biological activities which includes anti- mycological [6], antimicrobial [15] and antifungal [26]. The antimicrobial of several compounds of essential oil of Z. zerumbet have also been reported [1]. The antimicrobial action of leaf oil of Z zerumbet oil may be attributed to terpenes particularly β-caryophyllene, and β-pinene present therein [27]. For example, the antibacterial activity of β-caryophyllene against S. aureus was reported recently [28].

Conclusion

This study showed that most abundant compound of the leaf oil of Z. zerumbet were -pinene, -caryophylene and caryophyllene oxide while zerumbone was found in the pseudo-stem. In addition, the oil displayed antimicrobial action A. niger and B. cereus respectively at reasonable MIC level. In conclusion, the

11 www.videleaf.com Prime Archives in Plant Sciences study revealed the potentials of essential oils of Z. zerumbet from Vietnam as potential antimicrobial agent.

References

1. Yob NJ, Jofrry SM, Affandi MMR, The LK, Salleh MZ, et al. Zingiber zerumbet (L.) Smith: A review of its ethnomedicinal, chemical, and pharmacological uses. Evidence Based Complementary and Alternative Medicine. 2011; 2011: 1-12. 2. Khalid MH, Akhtar MN, Mohamad AS, Perimal EK, Akira A, Israf DA, Lajis N, et al. ulaiman MR. Antinociceptive effect of the essential oil of Zingiber zerumbet in mice: possible mechanisms. Journal of Ethnopharmacology. 2011; 137: 345-351. 3. Sulaiman MR, Mohamad TAST, Mossadeq WMS, Moin S, Yusof M, et al. Antinociceptive activity of the essential oil of Zingiber zerumbet. Planta Medica. 2010; 76: 107-112. 4. Zakaria ZA, Mohamad AS, Ahmad MS, Mokhtar AF, Israf DA, et al. Preliminary analysis of the anti-inflammatory activity of essential oils of Zingiber zerumbet. Biological Research for Nursing. 2011; 13: 425-432. 5. Worakrit W, Kamonchanok D, Nattagan M, Supatsorn C. The effects of soil parameters on efficiency of essential oil from Zingiber zerumbet (L.) Smith in Thailand. International Journal of Agriculture and Biosystem Engineering. 2016; 10: 211-223. 6. Madegowda BH, Parthepan R, Navya PN, Pushpa SM. In- vitro mycological activity of essential oil from Zingiber zerumbet rhizomes. Journal of Essential Oil Research. 2016; 28: 81-88. 7. Duangsamorn S, Fields PG, Angsumarn C. Contact toxicity, feeding reduction, and repellency of essential oils from three plants from the ginger Family (Zingiberaceae) and their major components against Sitophilus zeamais and Tribolium castaneum. Journal of Economic Entomology. 2011; 104: 1445-1454. 8. Yan W, Shan-Shan G, Dong-Ye H, Cheng-Fang W, Jian-Yu W, et al. Contact and repellant activities of Zerumbone and its analogues from the essential oil of Zingiber zerumbet (L.)

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Smith against Lasioderma serricorne. Journal of Oleo Science. 2017; 66: 399-405. 9. Huong LT, Chinh HV, An NTG, Viet NT, Hung HN, et al. Zingiber zerumbetrhizome essential oil: chemical constituents, antimicrobial and larvicidal activities. European Journal of Medicinal Plants. 2019; 30: 1-12. 10. Zhaikai Z, Sai Z, Wang HL, Piao XS. Essential oil and aromatic plants as feed additives in non-ruminant nutrition: a review. Journal of Animal Science and Biotechnology. 2015; 6: 1-12. 11. Marcincak S, Cabadaj RPP, Soltysova L. Antioxidative effect of oregano supplemented to broilers on oxidative stability of pultry meat. Slovakia Veterinary Research. 2008; 45: 61-66. 12. Papageorgiou G, Botsoglou N, Govaris A, Giannenenas I, Iliadis S, et al. Effect of dietary oregano oil and α- tocopheryl acetate supplementation on iron-induced lipid oxidation of turkey breast, thigh, liver and heart. Journal of Animal Physiology and Animal Nutrition. 2003; 87: 324- 335. 13. Restu WM, Halijah I, Nurulhusna AH, Khalijah A. Efficacy of four species of Zingiberaceae extract against vectors of dengue, chikungunya and filariasis. Tropical Biomedicine. 2017; 34: 375-387. 14. Sutthanont N, Wej C, Benjawan T, Anuluck J, Atchariya J, et al. Chemical composition and larvicidal activity of edible plant‐derived essential oils against the pyrethroid‐susceptible and ‐resistant strains of Aedes aegypti (Diptera: Culicidae). Journal of Vector Ecology. 2010; 35: 106-115. 15. Rana VS, Ahluwalia V, Najam AS, Virendra SR. Essential oil composition, antifungal, and seedling growth inhibitory effects of zerumbone from Zingiber zerumbet Smith. Journal of Essential Oil Research. 2017; 29: 320-329. 16. Dai DN, Thang TD, Chau TM, Ogunwande IA. Chemical constituents of the root essential oils of Zingiber rubens Roxb. and Zingiber zerumbet (L.) Smith. American Journal of Plant Science. 2013; 4: 7-10. 17. Chane-Ming J, Vera R, Chalchat JC. Chemical composition of the essential oil from rhizomes, leaves and flowers of Zingiber zerumbet Smith from Reunion Island. Journal of Essential Oil Research. 2003; 15: 202-205.

13 www.videleaf.com Prime Archives in Plant Sciences

18. Huong LT, Viet NT, Sam LN, Giang CN, Hung NH, et al. Antimicrobial activity of essential oil from the rhizomes of Amomum rubidum growing in Vietnam. American Journal of Essential Oil and Natural Products. 2019; 7: 11- 14. 19. Dai DN, Huong LT, Sam LY, Ogunwande IA. Chemical compositions and antimicrobial activity of essential oil from the rhizomes of Curcuma pambrosima Škorničk. & N.S. Lý growing in Vietnam. Natural Products Research. 2019. 20. Vietnamese Pharmacopoeia. Hanoi: Medical Publishing House. 2009. 21. National Institute of Science and Technology. Chemistry Web Book. Data from NIST Standard Reference Database. 2011; 69. 22. Vlietinck AJ. Screening methods for detection and evaluation of biological activity of plant preparation. In: Bohlin L, Brunh G, editors. Bioassay Methods in Natural Product Research and Drug Development. USA: Kluwer academic publishers. 1999; 37-52. 23. Vanden Bergher DA, Vlietinck AJ. Screening methods for antibacterial and antiviral agent from higher plants. In: Dey PM, Harbone JD, editors. Methods in Plant Biochemistry. London: Academic Press. 1991; 47-69. 24. Yusmaniar W, Suprapti TJ. Antibacterial activity of the essential oils of lempuyand wangi (Zingiber aromaticum Val.), lempuyang gajah (Zingiber zerumbet Sm), and lempuyang emprit (Zingiber amaraicans Bl.) on three gram- negative bacteria. Asian Journal of Applied Sciences. 2015; 3: 290-293. 25. Azelan NA, Rosnani H, Awang MA, Abd Malek R, Musa NF, et al. Antibacterial activity of Zingiber officinale and Zingiber zerumbet essential oils extracted by using turbo extractor distillatory. UTNM Journal of Technology. 2015; 77: 43-47. 26. Sidahmed HMA, Hashim NM, Abdulla MA, Ali HM, Mohan S, et al. Antisecretory, gastroprotective, antioxidant and anti- Helicobcter Pylori activity of zerumbone from Zingiber Zerumbet (L.) Smith. PLoS ONE. 2016; 10: e0121060. 27. Swamy MK, Akhtar MS, Sinniah UR. Antimicrobial properties of plant essential oils against human pathogens

14 www.videleaf.com Prime Archives in Plant Sciences

and their mode of action: an updated review. Evidence Based Complementary and Alternative Medicine. 2016: Article ID 3012462, 12 pages. 28. Dahham SS, Tabana YM, Iqbal MA, Ahamed MBK, Ezzat MO, et al. The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna. Molecules. 2015; 20: 11808-11829.

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