This paper was written with the aim to give comparison of the commercially available B. serrata essential oil and hydrodistilled from resin that is also commercially available on the Serbian market. In that order, GC/MS analysis was performed, chemical components identified and quantified and obtained results served as the basis for interpreting the findings from the antimicrobial and antioxidant tests. The essential oil from frankincense resin was isolated by Clevenger’s distillation. In the essential oil hydrodistilled from commercial resin a total of 28 components were identified with octanol acetate (40.6%) as dominant one, while in the commercial one 18 components were identified and the most represented was α-thujene (75.9%). The antimicrobial activity of essential oils was determined by the disc-diffusion method against nine microorganisms. Both isolated and commercial oil exhibited similar inhibitory strengths (mm of inhibition zone) against: S. aureus ATCC 25923 (10.66 and 12.66), B. cereus house strain (16.33 and 11.33), E. coli ATCC 25922 (11.33 and 10.66) with that difference that only commercial one inhbited C. albicans ATCC 2091 (12.66). The results for antioxidant activity determined spectrophotometrically by DPPH test favoured commercial essential oil under the same conditions after 40 minutes of incubation.
Boswellia serrata also known as Indian frankincense tree, belongs to the family Burseraceae and is widespread in dry regions of India, Yemen, Nigeria and Pakistan, as well in Arabian Peninsula 1 2. The Boswellia tree produces a resin that is also known by the names: frankincense, sallaki, idigenous olibanum, luban 3. This frankiscence has a trading history between Europe and China for the past 5.000 years 4. Since ancient times, this natural resin has been used for embalming and in cultural ceremonies due to its incense. Members of Hindu, Babylonian, Persian, Roman, Chinese, Greek, and ancient American civilizations practiced burning this resin to soothe their souls and please their gods with the smoke and fragrance it produces 5. It is a coloured, exuded like “tear” shaped solid with odour described as dry, slightly green, fresh-balsamic and tenacious. When pyrolysed, it gives well known incense characteristic of the churches 6 (both Orthodox and Chatolic 4).
B. serrata is considered the 'true frankincense' producing tree. Interest in the scientific study of this plant species is on the rise, and modern science has revealed that its oleo-gum-resin is comprised of over 200 different natural products (30-60% resin, 5-10% essential oils, and polysaccharides such as galactose, arabinose, and xylose). In Islamic traditional medicine in Arabian countries, frankincense is mentioned in Avicenna’s (Ibn Sina’s) Canon of Medicine and is used to treat tuberculosis, amnesia, infections, bruises, diarrhea, burns, stomach issues, and eye sores. It is also referenced in Chinese traditional medicine, where frankincense-based pills are used to treat bronchial, nasopharyngeal, or pancreatic carcinoma 4. The frankincense is also a part of Ayurvedic system of medicine because of its anti-inflammatory properties 7 8, and used in threatment of diarrhoea, dysentery, ringworm, boils, fevers (antipyretic), skin and blood diseases, cardiovascular diseases, mouth sores, bad throat, bronchitis, asthma, cough, vaginal discharges, hair-loss, jaundice, hemorrhoids, syphilitic diseases, irregular menses and stimulation of liver 5. The powdered olibanum form is used to relieve toothache 9.
The content of secondary metabolites in resin varies significantly. Some species are rich in monoterpenes, while others contain diterpenes or triterpenes 10. The qualitative and quantitative composition of chemical compounds in the resins of different Boswellia species depends on geographical location, climatic conditions and the timing of resin collection 11. An overview of the main chemotypes of Boswellia species is given in Table 1.
The resin obtained from the Indian frankincense tree contains pentacyclic triterpenoids and boswellic acids (BAs) as dominant compounds (25-35% 13. Six major boswellic acids were reported: α and β-boswellic acids are the leading contenders (BA, 10–21%), followed by Acetylated α and β-Boswellic acids (ABA, 0.05–6%), 11-keto-β-boswellic acid (KBA, 2.5– 7.5%) and 3-O-acetyl-11-keto-β-boswellic acid (AKBA, 0.1–3%) 14. BA and their derivatives are in-vitro non-redox inhibitors of 5-lypoxigenase (5-LOX), an enzyme in neutrophils responsible for the conversion of endogenous arachidonic acid into leukotrienes that cause vasoconstriction, bronchospasm and chemotaxis 15. These acids possess numerous activities including anti-inflammatory, antitumor, immunomodulatory and in the treatment of inflammatory bowel diseases 8 14.
The essential oil and resin of frankincense are used in treatment of many diseases. Interest in this plant is growing 7 due to the therapeutic potential of its isolates 16. The various activities demonstrated by the isolates (essential oil, extracts) of B. serrata resin have led to the development of different formulations in the pharmaceutical and cosmetic industry e.g. 50 ml of “Eau de Parfum” containing B. serrata extract is sold for 165$ 17. In “Western medicine” frankincense was introduced in the early 20th century to treat various inflammation diseases and is listed in the 7th supplement of the European Pharmacopoeia 4. Standardized preparations of Boswellia serrata extract (BSE) are commercially available and are used to treat inflammatory diseases such as: rheumatoid arthritis, Crohn's disease, ulcerative colitis and inflammatory bowel disease 18. Based on current data, BSE can be considered as an alternative to non-steroidal anti-inflammatory drugs (NSAIDs) 19 due to less pronounced gastrointestinal and cardiovascular side effects 20. Unlike NSAID, which are well known to disrupt glycosaminoglycan synthesis and lead to joint damage in arthritis, it has been shown that BA significantly reduces the decomposition of this polysaccharide 21. Studies have also shown that extracts from this species can be effective against malignant breast diseases and may prevent the spread of certain forms of leukemia and brain tumors, thanks to the presence of BA 22. The essential oil of Indian frankincense exhibits a wide range of pharmacological activities, including antioxidant, antimicrobial, anticancer, anti-inflammatory, neuroprotective, and antiulcer activity 23 24 25. The determination of the chemical composition of B. serrata essential oil is based on a method that combines gas chromatography (GC) with mass spectrometry (MS) 26 27. Due to the presence of pinene, frankincense essential oil modulates antibiotic resistance by reducing the minimum inhibitory concentration (MIC) of gentamicin, erythromycin and triclosan up to 512 times 28, and in addition, thujene, camphene, β-Pinene, myrcene, limonene also exhibit antimicrobial activity 29. Of all BA, AKBA is the most potent antibacterial compound against oral cavity pathogens 14. The essential oil of Indian frankincense is used as an antiseptic agent in mouthwashes, and to treat asthma and coughs 30, and because of all above mentioned benefits, it is highlt valuable and widely commercialized.
The aim of this paper is to provide a comparative analysis of the chemical composition, antimicrobial properties and antioxidant activity of B. serrata essential oils isolated from commercially available frankincense resin and the one that is commercially available on the Serbian market.
Plant material
Commercial essential oil of Indian frankincense was used in this work (Probotanic D.O.O., Belgrade, Serbia) bought in local drugstore (Leskovac, Serbia) and B. serrata frankincense resin bought in specialized store (Belgrade, Serbia). Just before the essential oil was isolated, the Indian frankincense resin was grounded to a fine, brown powder.
Reagents and chemicals
The following reagents and chemicals were used: ethanol, 96% (Centrohem Zemun, Serbia), 2,2-diphenyl-1-picrilhydrazyl (DPPH) radical, alkane standard solution C8-C20 (~40 mg/L each, in hexane), alkane standard solution C21-C40 (Sigma Chemical Company, St. Louis, USA) and diethyl ether (J.T. Baker, New Jersey, USA).
Isolation of Indian frankincense resin essential oil
The essential oil from frankincense resin was isolated using Clevenger’s distillation. Precisely, 50.0 g of resin was weighed and grounded by a pestle in mortar, quantitatively transferred to the boiling flask, and 500.0 mL of distilled water was added afterwards (hydromodule 1:10, m/v). The distillation continued up to 4 h, after which a light yellow essential oil was obtained and therefore stored in a refrigerator at 4oC up to analysis.
Gas chromatography-mass spectrometry (GC/MS) of isolated and commercial B. serrata resin essential oils
The GC/MS analysis of essential oils was performed on a gas chromatograph instrument Agilent Technologies 7890B coupled with inert, selective 5977A mass detector of same company. Isolated and commercial essential oil was dissolved in diethyl ether and 1 µL of prepared solution was injected in split (40:1) injector operation mode at temperature 220°C.
As a carrier was used helium of purity 99,999% at a constant flow rate of 1 mL/min. The components were separated on a non-polar, silica capillary column HP-5MS (30 m × 0.25 mm × 0.25µm; Agilent Technologies, Santa Clara, CA, USA). The oven temperature was increased linearly starting from 60°C to 246°C at speed of 3°C/min. The total time of the analysis was 62 min. The eluate was by the MSD transfer temperature line 250 °C transferred to quadrupole mass spectrometer with electron ionization (ion source and quadrupole mass analyzer temperatures were 230°C and 150°C, respectively, and electron energy was 70 eV) and analysed in Scan mode, in m/z range of 41-415 Da. Analysis was performed in triplicate.
Data analysis was done by MSD ChemStation Data Analysis in combination with AMDIS (Automatic Mass Spectral Deconvolution and Identification System) and NIST MS Search softwares (Agilent Technologies, USA).
For definitely identification of the components of the mixture were used experimentally determined retention indices by using a series of homologous n-alkanes C8-C20 as a standard. The identification of the components is based on the comparison of their retention indices (RIexp) to values from literature (RIlit), on the comparison of their mass spectra with spectra from Willey, NIST and RTLPEST library (MS) and when was possible, by co-injecting of responding standard (Co-I).
Quantitative analysis was done by applying the surface normalization method GC/FID of signal without any corrections.
Antimicrobial activity of isolated and commercial Indian frankincense essential oils
Antimicrobial activity of isolated and commercial Indian frankincense essential oil was tested against 9 microorganisms, four Gram-positive bacteria: Staphylococcus aureus ATCC 25923, Bacillus cereus in house strain, Bacillus subtillis ATCC 6633, Listeria monocytogenes ATCC 15313; four Gram-negative bacteria: Escherichia coli ATCC 25922, Pseudomonas aeruginosa ATCC 27853, Proteus vulgaris ATCC 8427, Klebsiella pneumoniae ATCC 700603 and fungus Candida albicans ATCC 2091.
Disk-diffusion method was applied for antimicrobial analysis. The substrates were sterilized in an autoclave, 15 minutes at temperature 120 °C and pressure 110 kPa. Microorganism suspensions were prepared by the method of direct suspension of colonies. Colonies were suspended directly from the plate into 10 mL of sterile 0,8% physiological solution. The turbidity of the starting suspension was adjusted by comparing with the turbidity of 0.5 McFarland standard solution so that suspension contains 108 CFU/mL of bacteria, that is 106 CFU/mL yeast cells. Bacterial suspensions were seeded onto the surface of the Mueller hinton plates containing agar („Torlak”, Belgrade, Serbia), while the suspension of yeas was seeded onto the surface of the Sabouraud malt agar („Torlak”, Belgrade, Serbia). On the hardened inoculated substrate, sterile disks of diameter 9 mm (Schleicher&Schuell) were placed, which are impregnated with 50 μL of essential oil. The samples were incubated during 24 h at 37○C for bacteria and 48 h at 25 ○C for yeast. After incubation, the zones of inhibition of microorganisms growth were measured by the diameter measuring of the inhibition zone together with the disc and expressed in millimeters. The presence of a transparent inhibition zone was a confirmation of the antimicrobial activity of the tested sample. DMSO was used as a negative control, while commercial disks (6 mm) of Ciprofloxacin 5 µg (Carl Roth, Karlsruhe, Germany) and antimycotic Nystatin 100 I.U. (Carl Roth, Karlsruhe, Germany) were used as positive control.
Antioxidative activity of isolated and commercial Indian frankincense essential oils – DPPH test
The antioxidative activity of isolated and commercial Indian frankincense essential oils were determined spectrophotometricaly using the DPPH test. The solutions of essential oil in ethanol concentration of 0.5 mg/mL were prepared. After that, a series of solutions of different concentrations was made (0.0078-0.0625 mg/mL). Ethanolic solution of DPPH radical was added into 2.5 mL of prepared solutions of essential oil. Absorbance was measured at 517 nm after 20 and 40 minutes of incubation at a room temperature. Also, absorbance was determined for ethanolic solution of DPPH radical (1 mL of DPPH radical and 2.5 mL of ethanol) as for ethanolic solution of essential oils (2.5 mL of essential oil and 1 mL of ethanol). The free radical scavenging capacity was calculated by formula 31:
DPPH radical scavenging capacity (%) = 100 - [(AS– AB) × 
] AS= Absorption of the „sample“ at 517 nm. „Sample“ - ethanolic solution of samle treated with DPPH radical (2.5 mL of sample + 1 mL of DPPH radical); AB = Absorption of the „blank“ at 517 nm. „Blank“ - ethanolic solutionof sample which was not treated with DPPH radical (2.5 mL of sample + 1 mL of ethanol); AC = Absorption of the „control“ at 517 nm. „Control“ - diluted ethanolic solution of DPPH radical (2.5 mL of sample + 1 mL of DPPH radical).
Qualitative and quantitative composition of isolated and commercial Indian frankincense essential oils
The appearence of frankincense resin as well as the isolated and commercial essential oils is shown in Figure 1.
The GC/MS method was used to determine the chemical composition of the isolated Indian frankincense essential oil, and the results are presented in Table 2.
The chemical composition of the commercial Indian frankincense essential oil was determined in the same manner, and the results of the analysis are presented in Table 3.
Antimicrobial activity of isolated and commercial Indian frankincense essential oils
The antimicrobial activity of isolated and commercial B. serrata frankincense essential oils were tested against Gram-negative bacteria, Gram-positive bacteria and fungus. The results obtained are presented in Table 4.
Antioxidant activity of isolated and commercial Indian frankincense essential oils
Antioxidant activity of commercial and isolated essential oils from B. serrata frankincense was analyzed by DPPH test and obtained results are shown in Figure 4.
Qualitative and quantitative composition of isolated and commercial Indian frankincense essential oils
Based on the obtained results (Table 2), the most abundant compounds in the isolated Indian frankincense essential oil are octanol acetate (40.6%), (Z)-nerolidol (11.9%) and incesole (11.2%), with their structural formulas presented in Figure 2.
Based on the results of the analysis (Table 3), monoterpenes are dominant compounds in the commercial essential oil comprising 95.0% of the total with α-thujene (75.9%), α-pinene (5.8%), sabinene (3.7%) and δ-3-carene (3.5%). The structures of the most abundant components identified in the commercial essential oil of Indian frankincense are presented in Figure 3.
The essential oils of most species in this genus are rich in monoterpenes. The essential oil of B. carterii contains α-pinene, α-thujene, limonene, sabinene, myrcene and p-cymene 12, while in essential oil of B. frereana dominates α-pinene, α-thujene, p-cymene and sabinene 32 33 34. The essential oil of Boswellia sacra is rich in α-pinene, myrcene and limonene 33 35 36. α-thujene can be found in essential oils of the following species: B. serrata, B. ameero, B. elongate, B. popoviana, B. nana 37. On the contrary, the essential oil of B. papyrifera contains octyl acetate and octanol as its dominant compounds 33 38 39.
Singh et al., 2007 and Camarda et al., 2007 have determined that in the essential oil of Indian frankincense resin α-thujene is dominant. This is consistent with the results obtained in this study 40 41.
Based on previously published GC/MS analysis results, the most prevalent compounds in commercial Indian frankincense essential oil are from the group of monoterpenes, such as α-thujene 42 and α-pinene 34. The high content of monoterpenes in the commercial sample analyzed in this study may be the result of long-term storage, as the conversion of oxygenated monoterpenes into their corresponding monoterpene hydrocarbons occurs due to deoxygenation under uncontrolled humidity and temperature conditions 40. It has been shown that the frankincense resin of B. serrata yields a higher content of essential oil (3.30 – 9.37%) compared to B. sacra (5.5%), B. elongate (2.3%), B. ameero (1.8%) and B. socotrana (1.2%) 43 44. Variations in the chemical composition of essential oils may also result from extraction methods and conditions, agroecological factors, storage conditions, seasonal variations, and geographical differences 45 46 47.
In the study by Gupta et al. (2016) the chemical composition of essential oils from three geographical locations was compared: essential oil of B. serrata resin collected in forest called Šivpuriat northwest part of Madhya Pradesh (India) and commercial samples. Based on their GC/MS analysis results, the commercial samples contained a higher percentage of monoterpenes (81.9-88.1%) with α-thujene (61.4-69.8%) as the most abundant compound, which is consistent with the results obtained in this study. On the other hand, the essential oil isolated from resin collected from wild habitats contained a higher percentage of oxygenated monoterpenoids (15.7%) and sesquiterpenes (19.2%). The higher percentage of monoterpene hydrocarbons in commercial samples, particularly α-thujene, α-pinene and δ-3-carene, may be related to their increased antioxidant and antifungal activity 26.
α-thujene is a monoterpene that is also found in eucalyptus, juniper, dill and coriander. Although there are only a few data on the biological activity of α-thujene, it was reported as a potential insecticide, anti-inflammatory and antimicrobial agent 48.
On the other hand, pinenes exhibit numerous biological activities and are used as fungicides, antiviral and antimicrobial agents as well as in fragrances and aromas. It has been shown that they have an inhibitory effect on breast cancer and leukemia. Pinenes are by the US Food and Drug Administration generally recognized as safe 28, which allows their use in various products. α-pinene also exhibits anti-inflammatory, antioxidant, anti-cancer, antibacterial and antinociceptive properties. It has been proven that they are highly versatile in polymer synthesis, with polymers synthesized from pinene demonstrating higher quality than those produced from other sources 49.
Antimicrobial activity of isolated and commercial Indian frankincense essential oils
The antimicrobial activity of various essential oils derived from aromatic plants is extensively studied due to the need for new antimicrobial agents and the increasing resistance of bacteria to conventional antibiotics 8.
The tested essential oils tested in this study exhibited weak to moderate activity against tested microorganisms. Gram-positive bacteria demonstrated sensitivity to the tested essential oils: S. aureus ATCC 25923 and B. cereus in house strain, as well as Gram-negative bacteria E. coli ATCC 25922. The detected zones of inhibition are significantly smaller compared to the effect of the antibiotic (Table 4). The essential oils of Indian frankincense did not show activity against the other tested bacterial strains. In addition, commercial essential oil if Indian frankincense showed inhibitory effect against fungus C. albicans ATCC 2091, while it was not observed when isolated essential oil was tested. To better understand the spectrum of antimicrobial effects of B. serrata essential oils, further research is needed, including testing against a larger number of pathogens. The results obtained in this study represent an important contribution particularly in light of the increasing resistance of pathogens to antibiotics, which is one of the greatest threats to global human health. As bacterial resistance to various antibiotics is one of the biggest global challenges, every investigation into new antimicrobial agents of natural origin can contribute to solving this problem 8.
Sadhasivam et al. (2016) tested the antimicrobial activity of nine commercially available essential oils against Propionibacterium acnes, Malasezzia spp., Trichophyton spp. and C. albicans which primarly cause infections of skin, scalp and nails. Among the nine tested essential oils – Cyperus scariosus, Syzgium aromaticum, Carum carvi, Coriandrum sativum, Syzgium cumini, Elettaria cardamom, Occimum sanctum and Piper nigrum, the one of B. serrata exhibited superior antimicrobial activity against the tested microorganisms, with the maximum activity observed against Trichophyton spp. 48.
The combination of B. serrata essential oil with azoles (fluconazole, ketoconazole, posaconazole and voriconazole) showed synergistic activity against the azole-resistant strain of C. albicans, highlighting Indian frankincense essential oil as a powerful antifungal agent. However, terbinafine has been shown to exert an antagonistic effect on Indian frankincense essential oil. Additionaly, this essential oil exhibited antibiofilm activity against Staphylococcus epidermidis, further supporting its use as a potent antimicrobial agent 48. An experiment was conducted to test the essential oils of B. papyrifera and B. rivae in relation to bacterial biofilm production. The results indicated that B. papyrifera exhibits antimicrobial activity against S. aureus and S. epidermidis. Similarly, the efficiency of B. rivae essential oil was confirmed against C. albicans biofilms. These results are significant because staphylococcal biofilms are often resistant to conventional antibiotics at concentrations up to 1,000 times higher than of their MIC 39.
Mothana et al. (2011) tested the antimicrobial activity of B. dioscorides, B. elongate and B. socotrana essential oils against two Gram-positive bacterias (S. aureus and B. subtilis), two Gram-negative bacteria (E. coli and P. aeruginosa) and the fungus C. albicans. Gram-positive bacteria were found to be more sensitive to the tested essential oils than Gram-negative bacteria, while the fungus showed resistance. The highest activity against S. aureus and B. subtilis was observed with B. socotrana essential oil, as confirmed by the lowest minimum inhibitory concentration (MIC) values (1.87 mg/mL) 50. Camarda et al. (2007) demonstrated that limonene is responsible for the antifungal activity of essential oils 41. The absence of limonene in mentioned species examined by Mothana et al. (2011) may explain the lack of activity against the tested fungus 50. In the tested commercial essential oil, the limonene content is 2.5%, and it demonstrated activity against C. albicans. This was not the case with the isolated essential oil, where limonene is present only in trace amounts. The results obtained are consistent with the previously mentioned experiments. For the other microbes tested in this study, both essential oils demonstrated activity against the same microbes, exhibiting nearly identical levels of activity despite their differing qualitative and quantitative chemical compositions.
It is important to note that the essential oil of B. carterii exhibits significant activity against methicillin-resistant Staphylococcus aureus (MRSA), which is resistant to penicillin antibiotics (MIC 3.52 μg/mL) 41. The antimicrobial activity exhibited by the essential oils of different species of the Boswellia may be the result of the presence of: E-β-ocimene, limonene, α-pinene, α-thujene, myrcene, octanol, octyl acetate, trans-verbenol and terpinen-4-ol 51. In fact, α-pinene 52, myrcene 52 and limonene 53 possess antimicrobial activity themselves.
Based on the results obtained from both this study and the experimental work of other authors, it is evident that, despite certain differences in the chemical composition of essential oils from various Boswellia sources, these hydro-isolates can be considered serious candidates for the treatment of microbial infections caused by different etiological agents.
Antioxidant activity of isolated and commercial Indian frankincense essential oils
The percentage of antioxidant activity increases linearly with the concentration of essential oils (Figure 4). The incubation time of the samples also influences the neutralization of DPPH radicals. After 20 and 40 minutes of samples incubation at room temperature, the absorbances of the obtained solutions were measured at 517 nm. It was observed that the commercial oil, within a concentration range 0.0078 to 0.0625 mg/mL exhibited a higher antioxidant potential (7.70 – 10.01%) after 40 minutes of incubation. The isolated essential oil, under the same incubation conditions, exhibited lower antioxidant activity (6.90-8.40%) within the tested concentration range (0.0079-0.063 mg/mL). This difference can be attributed to the variation in the chemical composition of the essential oils. The synthetic antioxidant BHT demonstrated an EC50 value of 0.021 mg/mL after 20 minutes of incubation with the DPPH radical 54.
Ayub et al. (2018) reported that the extraction method used affects both the yield and antioxidant activity of essential oils derived from the resin of B. serrata. The essential oil isolated by hydrodistillation exhibited the lowest free radical scavenging potential, while the essential oil obtained through supercritical fluid CO2 extraction displayed the potential. The difference in antioxidant activity between the essential oils can be attributed to the fact that the oil obtained through supercritical fluid extraction contains significantly more phenolic compounds than the oil obtained by steam distillation. Variations in the antioxidant activity of essential oils are likely due to differences in the chemical composition of the oils isolated by various extraction methods 29.
On the other hand, the percentage yield of the essential oil isolated by hydrodistillation is significantly higher than that of the oil obtained through supercritical liquid CO2 extraction. The differences in yield among essential oils obtained by hydrodistillation, steam distillation, and supercritical liquid CO2 extraction are often attributed to the polarity of CO2, which is a non-polar solvent with variable insulating power 29.
Ruberto and Barrata (2000) tested the antioxidant activity of three essential oils obtained from B. dioscorides, B. elongate and B. socotrana finding that their free radical scavenging activity was weak (22%, 21% and 28%, respectively) at concentration 1 mg/mL in comparison to the high antioxidant effect of ascorbic acid (96%) 55. The weak antioxidant activity can be attributed to the lower content of phenolic compounds in the essential oils of the mentioned species, primarily thymol and carvacrol. It is believed that the higher free radical scavenging activity of B. socotrana essential oil results from its increased content of oxygenated monoterpenes 44. Barrata et al. (1998) analyzed the antioxidant activity of essential oil from the species B. thurifera and concluded that the tested essential oil exhibits good antioxidant activity, comparable to that of α-tocopherol and butylated hydroxytoluene (BHT) 56. The latest experimental results related to Boswellia essential oil (a commercial mixture of B. carteri, B. sacra, B. papyrifera, and B. frereana) indicate that at a concentration of 50 µg/mL, the inhibition (%) was 15.18, compared to 25.22 for ascorbic acid 7.
Compared to other popular essential oils, the essential oil of B. serrata exhibited lower free radical scavenging activity than that of Mentha piperita and Melissa officinalis 57 58. However, the results obtained in this study are very similar to the recent findings by Gupta et al., who tested the antioxidant activity of B. serrata methanol extracts using the DPPH method 59.
In this paper, a comparison of qualitative and quantitative chemical composition of isolated and commercial Indian frankincense essential oil (B. serrata) available on Serbian market was given, and it was a basis for interpreting results obtained in antimicrobial and antioxidant activity tests.
By applying GC/MS method it was proved that commercial and isolated essential oils from B. serrata resin differ in chemical composition: in the commercial Indian frankincense essential oil monoterpene hydrocarbons are the most abundant (95.0%), followed by aromatic compounds (3.3%) and oxygenic monoterpenes (1.1%), while the essential oil isolated from commercially available B. serrata resin contained octanol acetate as dominant compound (40.6%), followed by (Z)-nerolidol (11.9%) and incesole (11.2%). The differences in the chemical composition of isolated and commercial essential oils of B. serrata are in a relation to their antimicrobial and antioxidant activity.
The commercial essential oil showed better antimicrobial activity against S. aureus ATCC 25923 than isolated one. The isolated essential oil showed better antimicrobial activity against B. cereus in house strain and E. coli ATCC 25922. Activity against C. albicans was shown only by commercial essential oil, while sensitivity of this microbe was not noticed against isolated essential oil.
The commercial essential oil of B. serrata resin showed slightly higher antioxidant activity than isolated essential oil. After 40 min of incubation period, commercial essential oil in concentration range from 0.0078 to 0.0625 mg/mL neutralizes DPPH radicals in percentage range from 7.70 to 10.01%, while at same concentration isolated essential oil neutralizes DPPH radicals in slightly lower percentages (from 6.90 to 8.40%).
The Indian frankincense resin and essential oil are valuable source of natural antioxidant and antimicrobial biochemical compounds.
The authors wish to thank Republic of Serbia—Ministry of Science, Technological Development and Innovation, for financing scientific research work, number: 451-03-65/2024-03/200133 and 451-03-66/2024-03/200133, University of Niš, Faculty of Technology.
The authors have no competing interests.
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Published with license by Science and Education Publishing, Copyright © 2024 Natalija Tošić, Vesna Nikolić, Ljiljana Stanojević, Jelena Stanojević, Ljubiša Nikolić, Ana Dinić, Ivana Gajić, Maja Urošević and Vojkan Miljković
This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit
http://creativecommons.org/licenses/by/4.0/
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| In article | View Article | ||
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| In article | View Article | ||
| [17] | Fiele Fragrances - BOSWELLIA Eau de Parfum | CAPSULE PARFUMERIE accessed on 10.07.2024. | ||
| In article | |||
| [18] | Mursch, K. and Behnke-Mursch, J, "Internet-based interaction among brain tumour patients. Analysis of a medical mailing list", Acta Neurochirurgica, 64(2). 71-75. 2003. | ||
| In article | View Article PubMed | ||
| [19] | Sudhakar, A., Shantakumar, J. and Joseph, M.V, "Evaluation of Anti-Inflammatory Activity of Enriched Boswellia Extract (Olibose®) in Human Dermal Fibroblast Cells In-vitro". American Journal of Phytomedicine and Clinical Therapeutics, 9(2:6). 1-6. 2021. | ||
| In article | |||
| [20] | Abdel-Tawab, M., Werz, O. and Schubert-Zsilavecz, M, "Boswellia serrata: an overall assessment of in vitro, preclinical, pharmacokinetic and clinical data", Clinical Pharmacokinetics, 50(6). 349-369. 2011. | ||
| In article | View Article PubMed | ||
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| In article | |||
| [22] | Lemenih, M. and Tejetay, D, "Frankincense and myrrh resources of Ethiopia: Medicinal and industrial uses", Ethiopian Journal of Science, 26(2). 161-172. 2003. | ||
| In article | View Article | ||
| [23] | Efferth, T. and Oesch, F, "Anti-inflammatory and anti-cancer activities of frankincense: Targets, treatments and toxicities", Seminars in Cancer Biology, 80. 39-57. 2022. | ||
| In article | View Article PubMed | ||
| [24] | Hamidpour, R., Hamidpour, S., Hamidpour, M. and Shahlari, M, "Frankincense (Ru Xiang; Boswellia Species): From the Selection of Traditional Applications to the Novel Phytotherapy for the Prevention and Treatment of Serious Diseases", Journal of Traditional and Complementary Medicine, 3(4). 221-226. 2013. | ||
| In article | View Article PubMed | ||
| [25] | Iram, F., Khan, S.A. and Husain, A, "Phytochemistry and potential therapeutic actions of Boswellic acids: A mini-review", Asian Pacific Journal of Tropical Biomedicine, 7(6), 513-523. 2017. | ||
| In article | View Article | ||
| [26] | Gupta, M., Rout, P.K., Misra, L.N., Gupta, P., Singh, N., Darokar, M.P., Saikia, D., Singh, S.C. and Bhakuni R.S, "Chemical composition and bioactivity of Boswellia serrata Roxb. essential oil in relation to geographical variation". Plant biosystems, 151(4). 623-629. 2016. | ||
| In article | View Article | ||
| [27] | Venkatesh, H. N., Sudharshana, T. N., Abhishek, R. U., Thippeswamy, S., Manjunath, K. and Mohana, D.C, "Antifungal and antimycotoxigenic properties of chemically characterised essential oil of Boswellia serrata Roxb. ex Colebr", International Journal of Food Properties, 1-13. 2017. | ||
| In article | View Article | ||
| [28] | Salehi, B., Upadhyay, S., Orhan, E.I., Jugran, K.A., Jayaweera, L.D.S., Dias, A.D., Sharopov, F., Taheri, Y., Martins, N., Baghalpour, N., Cho, C.W. and Sharifi-Rad, J, "Therapeutic potential of alpha- and beta-pinene: A Miracle Gift of Nature". Biomolecules, 9(11). 738. 2019. | ||
| In article | View Article PubMed | ||
| [29] | Ayub, A.M., Hanif, A.M., Sarfraz, A.R. and Shahid, M, "Biological activity of Boswellia serrata Roxb. oleo gum resin essential oil: effects of extraction by supercritical carbon dioxide and traditional methods", International Journal of Food Properties, 21(1). 808-820. 2018. | ||
| In article | View Article | ||
| [30] | Banno, N., Akihisa, T., Yasukawa, K., Tokuda, H., Nakamura, Y., Nishimura, R., Kimura, Y., and Suzuki, T, "Anti-inflammatory activities of the triterpene acids from the resin of Boswellia carterii". Journal of Ethnopharmacology, 107(2). 249-253. 2006. | ||
| In article | View Article PubMed | ||
| [31] | Stanojevic, Lj., Marjanovic-Balaban, R.Z., Kalaba, D.V., Stanojevic S.J. and Cvetkovic, J.D, "Chemical composition, antioxidant and antimicrobial activity of Chamomile flowers essential oil (Matricaria chamomilla L.)". Journal of Essential Oil Bearing Plants, 19(8). 2017-2028. 2016. | ||
| In article | View Article | ||
| [32] | Basar, B, Phytochemical investigations on Boswellia species. Ph.D. Thesis, Universitat Hamburg, Istanbul. 2005. | ||
| In article | |||
| [33] | Hamm, S., Bleton, J., Connan, J. and Tchapla, A, "A chemical investigation by head-space SPME and GC/MS of volatile and semi-volatile terpenes in various olibanum samples", Phytochemistry, 66(12). 1499-1514. (2005). | ||
| In article | View Article PubMed | ||
| [34] | Van Vuuren, S.F., Kamatou, G.P.P. and Viljoen, A.M, "Volatile composition and antimicrobial activity of twenty commercial frankincense essential oil samples". South African Journal of Botany, 76(4). 686-691. 2010. | ||
| In article | View Article | ||
| [35] | Al-Saidi, S., Rameshkumar, K.B., Hisham, A., Sivakumar, N. and Al-Kindy, S, "Composition and antibacterial activity of the essential oils of four commercial grades of Omani luban, the oleo-gum resin of Boswellia sacra Flueck", Chemistry and Biodiversity, 9(3). 615-624. 2012. | ||
| In article | View Article PubMed | ||
| [36] | Ni, X., Suhail, M.M., Yang, Q., Cao, A., Fung, K.M., Postier, R.G., Woolley, C., Young, G., Zhang, J. and Lin, H.K, "Frankincense essential oil prepared from hydrodistillation of Boswellia sacra gum resins induces human pancreatic cancer cell death in cultures and in a xenograft murine model", BMC Complementary and Alternative Medicine, 12(1). 253. 2012. | ||
| In article | View Article PubMed | ||
| [37] | Madera, P., Paschova, Z., Ansorgova, A., Vrškovy, B., Lvončik, S. and Habrova, H, "Volatile compounds in oleo-gum resin of Socotran species of Burseraceae". Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 65(1). 73-90. 2017. | ||
| In article | View Article | ||
| [38] | Bekana, D., Kebede, T., Assefa, M. and Kassa, H, "Comparative phytochemical analyses of resins of Boswellia species (Boswellia papyrifera (Del) Hochst., Boswellia neglacta S. Moore, and Boswellia rivae Engl.) from northwestern, southern, and southeastern Ethiopia", ISRN Analytical Chemistry, 2014. 1-9. 2014. | ||
| In article | View Article | ||
| [39] | Schillaci, D., Arizza, V., Dayton, T., Camarda, L. and Di Stefano, V, "In vitro anti-biofilm activity of Boswellia spp. olegum resin essential oils", Letters in Applied Microbiology, 47(5). 433-438. 2008. | ||
| In article | View Article PubMed | ||
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