GC/MS Analysis and Potential Cytotoxic Activity of Haplophyllum tuberculatum Essential Oils Against Lung and Liver Cancer Cells

Abstract

Background: Haplophyllum tuberculatum is a plant belongs to family rutacee. It is rich in volatile oils, fixed oils, alkaloids, and furanocoumarins. It is well known for the huge number of folkloric uses in middle east. Objective: The aim of this study is to establish the chemical composition of the essential oils of Libyan H. tuberculatum and to investigate their cytotoxic potentialities.Materials and Methods: The essential oils of the aerial parts and flowers of H. tuberculatum growing in Libya were prepared by hydrodistillation. GC/MS analyses were performed on a Shimaduz capillary gas chromatograph (GC 17A ver.3) instrument directly coupled to mass spectrometer-MS QP5050A. Oil A and F of H. tuberculatum at different concentrations (0-50 μg/ml) in DMSO were tested for cytotoxicity against human tumor cell lines. Results: Oil yield was found 0.4 and 1.5 (v/w %) on dry weight basis respectively. GC/MS analysis resulted in identification of total 35 compounds. 15 compounds were common to both oils. oil A of H. tuberculatum exhibited antitumor activities against. liver carcinoma cell line (HEPG2) and lung carcinoma cell line (H1299) 4.7 μg/ml and 4.1 μg/ml. Conclusion: Essential oil of the aerial parts of H. tuberculatum is potentially active against lung (H-1299), and liver (HEPG2) carcinoma cell lines. The observed cytotoxic, activities can be attributed to the dominance of α and γ-terpinene in this oil.

Full text

Pharmacogn. J.
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Original Article
Pharmacognosy Journal, Vol 8, Issue 1, Jan-Feb, 2016 66
GC/MS Analysis and Potential Cytotoxic Activity of Haplophyllum
tuberculatum Essential Oils Against Lung and Liver Cancer Cells
Omar Mohamed Mohamed Sabry1,2*, Abeer Mohamed El Sayed1and Salmin Khalid Alshalmani2
1Department of Pharmacognosy, Faculty of Pharmacy, Cairo University, Kasr El-Einy Street, 11562, Cairo, Egypt.
2 Department of Pharmacognosy, Faculty of Pharmacy, Benghazi University, Benghazi, Libya.
ABSTRACT
Background: Haplophyllum tuberculatum is a plant belongs to family
rutacee. It is rich in volatile oils, xed oils, alkaloids, and furanocoumarins.
It is well known for the huge number of folkloric uses in middle east. Ob-
jective: The aim of this study is to establish the chemical composition of
the essential oils of Libyan H. tuberculatum and to investigate their cyto-
toxic potentialities.Materials and Methods: The essential oils of the aerial
parts and owers of H. tuberculatum growing in Libya were prepared by
hydrodistillation. GC/MS analyses were performed on a Shimaduz capillary
gas chromatograph (GC 17A ver.3) instrument directly coupled to mass
spectrometer-MS QP5050A. Oil A and F of H. tuberculatum at different
concentrations (0-50 µg/ml) in DMSO were tested for cytotoxicity against
human tumor cell lines. Results: Oil yield was found 0.4 and 1.5 (v/w %)
on dry weight basis respectively. GC/MS analysis resulted in identication
of total 35 compounds. 15 compounds were common to both oils. oil A
of H. tuberculatum exhibited antitumor activities against. liver carcinoma
cell line (HEPG2) and lung carcinoma cell line (H1299) 4.7 µg/ml and 4.1
µg/ml. Conclusion: Essential oil of the aerial parts of H. tuberculatum is
potentially active against lung (H-1299), and liver (HEPG2) carcinoma cell
lines. The observed cytotoxic, activities can be attributed to the dominance
of α and γ-terpinene in this oil.
Key words: Haplophyllum tuberculatum, Essential oils, Cytotoxicity, Lung
cancer, Liver cancer.
Address for Correspondence:
Dr. Omar Mohamed Mohamed Sabry, Department of Pharmacognosy,
College of Pharmacy, Cairo University, Kasr El-Einy Street, Cairo 11562,
Egypt.
Phone no: +201114886724
E-mail: omar.sabry@cu.edu.eg
DOI : 10.5530/pj.2016.1.14
INTRODUCTION
In Egypt the owering aerial parts of H. tuberculatum are used as a drink
to relieve fever, for abdominal upset, anemia, gastric pains, intestinal
worms, malaria, as aphrodisiac, and the decoction is used for rheumatic
pains.1 In Oman, the leaves are used as a remedy for headaches and ar-
thritis and also used for treatment of skin infections, discoloration and
parasitic diseases.2 In Saudi Arabia, H. tuberculatum is used to treat ma-
laria, rheumatoid arthritis and gynecological disorders,3 while in Sudan
the herb is used as an antispasmodic, to treat allergic rhinitis and breath-
ing diculties.4 e plant is rich in alkaloids, xed oils, volatile oils and
furanocoumarins.5-8 No published report was recorded concerning the
analysis of the volatile oil of the aerial parts and the ower of Libyan
H. tuberculatum and their biological potentialities.
MATERIALS AND METHODS
Plant material
Samples of the aerial parts and owers of Haplophyllum tuberculatum
(Forssk) A. Juss (Rutaceae) were obtained from Benghazi, Libya, identi-
ed by Dr. Reem Samir Hamdy, Lecturer of Plant Taxonomy, Botany De-
partment, Faculty of Science, Cairo University, Giza, Egypt. A voucher
specimen of the aerial parts and the owers of H. tuberculatum, were kept
in the herbarium of Department of Pharamacognosy, Faculty of Phar-
macy, Cairo University as a reference material specimen No. 2015224.
Preparation, characterization and analysis of the essential oil
Fresh samples of aerial parts and owers of H. tuberculatum (500 g) were
subjected separately to hydro-distillation. e percentage yield was calcu-
lated on dry weight (v/w) basis of the plant materials. e essential oil was
dried over anhydrous sodium sulfate and kept refrigerated until analysis.
Sample preparation for GC/FID and GC/MS analysis
Samples prepared by mixing 5µl of dehydrated essential oil with
approximately one ml of dichloromethane in auto sampler vials. Injection
volume was 1 µl injected directly to GC-FID and GC-MS.
Gas chromatography-mass spectrometry analysis (GC/MS)
GC/MS analyses were performed on a Shimaduz capillary gas
chromatograph (GC 17A ver.3) instrument directly coupled to mass
spectrometer-MS QP5050A. Capillary column SLB-5ms (30 m x 0.25
mm, lm thickness 0.25 µm) was used under the following condition:
oven temperature programmed from 40°C (3 min), then temperature
increased at rate 12°C/min to 180°C where it is hold for 5 min, then
temperature increased at rate 40°C/min to reach 240°C, where it is nally
hold for 5 min. e injector temperature was 240°C and was set at split
ratio 1:54. Carrier gas was He at ow rate 0.9 ml/min. e mass spec-
trometer operated on electronic (EI) ionization mode at 70 eV with scan
range 40-500. e transfer line temperature was 230°C.
Gas chromatography analysis (GC-FID)
e GC analysis was carried out using Shimaduz GC gas chromatograph
(GC-17 ver.3) system. FID detector temperature was 240oC. To obtain
the same elution order with GC/MS simultaneous auto injection was
done on a duplicate of the same operational conditions. Identication of
the essential oil components were carried out by comparing their relative
retention times with those of authentic samples or by comparing their
relative retention indices (RRI). e later were computed using a mixture
of a continuous series of n-alkane hydrocarbons (C4-C28) run on SLB-
5ms (non-polar) column using the same conditions as described above.
e components of the oils were fully unambiguously identied by their
mass spectral fragmentation patterns with those reported in computer-
ized MS-data bank spectral libraries (NIST and WILEY)10 or reported in
the literature.11-12 e compounds are arranged in order to GC elution on
SLB-5ms capillary column. Relative percentages were calculated based
on the GC-FID peak areas without the use of correction factors and are
compiled.
In vitro screening for cytotoxic activity
Human tumor cell lines: lung carcinoma cell line (H-1299) and liver
carcinoma cell line (HEPG2), maintained in the laboratory of the

OMAR SABRY et al.: GC/MS and Potential Cytotoxicity of Haplophyllum tuberculatum Essential Oils
Pharmacognosy Journal, Vol 8, Issue 1, Jan-Feb, 2016 67
Cancer Biology Department of National Cancer Institute, Cairo, Egypt,
were used. Oil A and F of H. tuberculatum at dierent concentrations
(0-50.000 µg/ml) in DMSO were tested for cytotoxicity against the fore-
mentioned human tumor cell line adopting sulforhodamine B stain
(SRB) assay.13 e relation between surviving fractions and oil concen-
tration was plotted to get the survival curve of each tumor cell line aer
the application of the specic concentration. e results were compared
to those of the standard cytotoxic drug, Doxorubicin (10 mg Adriamycin
hydrochloride, in 5 ml IV injection, Pharmacia, Italy) at the same con-
centrations. e dose of the test solutions which reduces survival to 50%
(IC50) was calculated.
Determination of median lethal dose LD50
e LD50 of the volatile oils was determined according to the procedures
developed by Karber (1941).14
Drugs and chemicals
Doxorubicin (10 mg Adriamycin hydrochloride, in 5 ml IV injection,
Pharmacia, Italy).
Statistical analysis
All data were expressed as mean ± SE and the statistical signicance was
evaluated using the ANOVA test followed by Duncan’s multiple range tests.
RESULTS
GC/MS analysis of essential oils
Hydro distillation of the aerial parts and owers of H. tuberculatum
yielded 0.4 and 1.5 % v/w of clear yellow colored oil exhibiting a char-
acteristic agreeable odor. e specic gravity and refractive index were
0.975, 0.968 and 1.487, 1.495, respectively. GC-MS analysis of dierent
oil samples of H. tuberculatum revealed relevant quantitative and quali-
tative variability. e components were categorized according to their
chemical nature and listed in Table 1. e oils of the aerial parts (A) and
owers (F) of H. tuberculatum showed approximately similar amounts
of hydrocarbons and oxygenated constituents e lower percentage of
hydrocarbons was recorded for the oil F (78.28%). Meanwhile, the high-
est percentage of hydrocarbon constituents was found in oil A (89.82%).
Terpene hydrocarbons were detected in appreciable amounts in oil A
(82.34%). Monoterpenes prevailed in the sample A (75.78%) while,
in sample F (72.81%) with the major α-terpinene ranged from (26.40-
24.45%) and β-terpinene ranged from (17.13-14.40%), respectively. Ses-
quiterpenes e.g. Zingiberine and β-sesquiphellandrene were detected in
oil A in traces only (0.36%) and (0.03%). Other monoterpene hydro-
carbons constituents detected in high amounts were: α-pinene (1.43-
1.33%), β-myrcene (5.69-6.05%) and 3-carene (3.87-5.43%), respec-
tively. e prole of both samples were characterized by the presence of
β-phellandrene (10.0-10.40%), 3,4-dimethyl-1,5-cyclooctadiene (6.03-
6.67%) and β-myrecene (5.69-6.04%). In oil A Oxygenated monoter-
penes were represented by 1,8 cineole (1.67%) and piperitone (5.55%).
Evaluation of cytotoxic activity
On assessing the cytotoxic activity under the experimental condition
adopted and from data displayed in Table 2 it could be concluded that the
oil A of H. tuberculatum exhibited variable antitumor activities against
the two tested cell line viz. liver carcinoma cell line (HEPG2) and lung
carcinoma cell line (H1299). In this respect, the oil A of H. tuberculatum
demonstrated the lowest IC50% when tested against H-1299 and HEPG2
cells (4.7 µg/ml and 4.1 µg/ml) respectively.
On the other hand, the oil F showed relatively higher IC50% against
H-1299 and HEPG2 cells (42.3 µg/ml and 19.7 µg/ml) respectively,
which is comparable to the standard cytotoxic drug, doxorubicin (Table
3-4). Results obtained during assessment of the cytotoxic potential of
Table 1: Percentage composition of essential oil of the aerial parts and
owers of H. tuberculatum
No. Compound * RI A (%) F (%)
11-Butanol-3-methylacetate 880 0.52 0.77
2α-ujene 929 0.32 -
3α-Pinene 937 1.43 1.33
4Pentanol 972 - 0.02
5Cyclohexen,1-methy-4-(1-
ethylethyldiene 977 1.12 -
6β-Myrcene 990 5.69 6.05
7Pentane-2,2-dimethyl 1003 0.08 -
8Octanal 1005 0.36 -
9Isovaleric acid isobutyl ester 1010 0.33 -
10 α –Phellandrene 1010 - 2.33
11 3-Carene 1013 3.87 5.43
12 Cineol 1,4 1020 3.82 0.08
13 Iso-terpinolene 1021 - 0.20
14 2-Pentanone ethylacetone 1025 0.54 0.28
15 Acetophenone-4`-methyl 1029 - 0.27
16 Cyclooctadiene-3,7-dimethyl 1034 6.03 6.66
17 β-phellandrene 1036 10.40 10.00
18 Eucalyptol 1039 1.67 0.70
19 Cis B-Ocimene 1049 0.39 0.42
20 1-Cyclo propyl pentane 1074 0.42 0.25
21 Non-2-en-1-ol 1077 - 0.49
22 n-amyl iso valerate 1099 0.27 0.43
23 Linaloal 1101 - 1.38
24 Butyric acid-2-methyl 1103 - 0.52
25 Isovaleric acid iso pentyl ester 1105 - 2.32
26 n-amyl isovalerate 1108 - 3.23
27 Octanol (n-octan-1-ol) 1130 - 0.50
28 α-Terpinen 1133 26.40 24.45
29 β-Terpinen 1151 17.13 14.40
30 Ocimenol 1175 0.03 0.05
31 Trans piperitol 1207 - 4.66
32 γ-Terpinen 1219 9.07 7.76
33 Piperitone 1267 5.55 2.07
34 (-)-Zingiberene 1505 0.36 -
35 β-Sesquiphellandrene 1540 0.04 -
Identied components 95.83 97.05
Monterpenes hydrocarbons 82.34 72.81
Oxygenated monoterpenes 13.09 7.51
Sesquiterpens hydrocarbons 0.40 0.00
Oxygenated sesquiterpenes 0.00 0.00
Aliphatic hydrocarbons 6.58 6.47
Aliphatic oxygenated compounds 1.51 9.97
Oxygenated components 13.09 17.77
Non-oxygenated components 82.74 79.28
Components are listed in order of their elution. RI*: Relative retention index on
SLB-5ms column.

OMAR SABRY et al.: GC/MS and Potential Cytotoxicity of Haplophyllum tuberculatum Essential Oils
68 Pharmacognosy Journal, Vol 8, Issue 1, Jan-Feb, 2016
the oil A of H. tuberculatum exhibited variable antitumor activities
against the two tested cell line viz, liver carcinoma cell line (HEPG2) and
lung carcinoma cell line (H1299). In this respect, the oil A of H. tubercu-
latum demonstrated the lowest IC50% when tested against H-1299 and
HEPG2 cells (4.7 µg/ml and 4.1 µg/ml) respectively. On the other hand,
the oil F showed relatively higher IC50% against H-1299 and HEPG2
cells (42.3 µg/ml and 19.7 µg/ml) respectively, which is comparable to
the standard cytotoxic drug, doxorubicin (Table 3-4). Results obtained
during assessment of the cytotoxic potential of the oil H. tuberculatum
are in accordance with formerly reported data related to γ-terpinen.15
e study was the rst concerning the cytotoxic activity of the essential
oils of H. tuberculatumon tumor cell lines.
CONCULSION
In conclusion, this report was the rst paper indicating the chemical
composition and investigating the cytotoxic potentialities of the es-
sential oils of Libyan H. tuberculatum. It is found that the essential oils
of the aerial parts of Halpophyllum tuberculatum are potentially active
against lung (H-1299), and liver (HEPG2) carcinoma cell lines. e ob-
served cytotoxic, activities can be attributed to the dominance of α and
γ-terpinene.
ACKNOWLEDGEMENTS
Special thanks to sta members of Pharmacology Unit, Cancer Biology
Department, National Cancer Institute, Cairo University, Egypt, for as-
sessment of cytotoxic evaluation in this study
CONFLICT OF INTEREST
e authors report no declarations of interest.
ABBREVIATION USED
A: e essential oils of the aerial parts, DMSO: Dimethyl sulfoxide, F:
e essential oil of the ower, GC/FID: Gas chromatography/Flame
ionization detector, GC/MS: Gas chromatography/Mass spectrometry
analysis, IC50%: e dose of the test solutions which reduces survival to
50%, RI: Retention indices, Rt: Retention times, SD: Standard deviation,
SRB: Sulforhodamine B stain assay.
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Table 2: Results of cytotoxic activity of the essential oil of H. tuberculatum
Tested Solutions
IC50 µg/ml
Lung carcinoma
H1299
Liver carcinoma
HEPG2
Essential oil A 4.7 4.1
Essential oil F 42.3 19.7
Standard drug (Doxorubicin) 3.70 7.00
Table 3: Drug cytotoxicity of H.tubrtculatum on Liver carcinoma cell line
HEPG-2
Conc µg/ml Essential oil A Essential oil F Doxorubicin
Mean ± SD
0.000 1.000 ± 0.047 1.000 ± 0.047 1.000 ± 0.009
5.000 0.407 ± 0.050 0.857 ± 0.055 0.536 ± 0.017
12.000 0.311 ± 0.065 0.602 ± 0.060 0.441 ± 0.017
25.000 0.323 ± 0.050 0.423 ± 0.029 0.377 ± 0.017
50.000 0.355 ± 0.036 0.380 ± 0.055 0.338 ± 0.011
N=6
Table 4: Drug cytotoxicity of H.tubrtculatum on Lung carcinoma cell line
H-1299
Conc µg/ml Essential oil A Essential oil F Doxorubicin
Mean ± SD
0.000 1.000 ± 0.050 1.000 ± 0.050 1.000 ± 0.057
5.000 0.465 ± 0.033 0.593 ± 0.041 0.353 ± 0.014
12.000 0.224 ± 0.041 0.597 ± 0.044 0.339 ± 0.007
25.000 0.181 ± 0.012 0.639 ± 0.075 0.303 ± 0.023
50.000 0.230 ± 0.032 0.552 ± 0.067 0.369 ± 0.011
N=6
the oil H. tuberculatum are in accordance with formerly reported data
related to γ-terpinene.15
Determination of median lethal dose LD50
e 24-hours LD50 was approximately more than 0.05 ml/kg b. wt. for
the essential oils. ese results showed that the essential oils are safe and
non-toxic.
To the best of our knowledge, this is the rst report on the chemical
composition of the essential oil of Libyan H. tuberculatum. Neverthe-
less, the composition of the essential oil from H. tuberculatum grown in
dierent regions of Egypt was previously studied.16 Monoterpenes are
non-nutritive dietary components found in the essential oils of herbs.
γ-terpinen, the major component of the oil in the present work (26-38%)
was detected only in trace amounts in the essential oil obtained from
H. tuberculatum in other countries.17-19 On the contrary, limonene (ab-
sent in the Libyan sample), linalool, and beta caryophyllene, were pres-
ent in major quantities (12.8 %, 15.5% and 12.77% ) in the essential oil
of the H. tuberculatum of Iran, United Arab Emirates, Oman and Iran
respectively.17-19 Moreover, the hydrocarbons, β-phellandrene, α-pinene,
and 3-carene were present in Libyan and Egyptian samples in compa-
rable amounts. e dierence in oil yield obtained and the composition
of essential oil in plants were aected by genetical and environmental
conditions, which is determined by growth region and harvesting time
in terms of onto genetical and diurnal variability.
On assessing the cytotoxic activity under the experimental condition
adopted and from data displayed in Table 3 it could be concluded that

OMAR SABRY et al.: GC/MS and Potential Cytotoxicity of Haplophyllum tuberculatum Essential Oils
Pharmacognosy Journal, Vol 8, Issue 1, Jan-Feb, 2016 69
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PICTORIAL ABSTRACT
• GC/MS analyses of the aerial parts and owers of H. tuberculatum grow-
ing in Libya were performed.
• Analyses resulted in identication of total 35 compounds. 15 compounds
were common to both oils.
• Oils at different concentrations (0-50 µg/ml) in DMSO were tested for
cytotoxicity against human tumor cell lines.
• Essential oil of the aerial parts of H. tuberculatum is potentially active
against lung (H-1299), and liver (HEPG2) carcinoma cell lines.
• The observed cytotoxic activities can be attributed to the dominance of α
and γ-terpinene in this oil.
ABOUT AUTHORS
Dr. Omar M. M. Sabry: Received his Ph.D. In medicinal and natural products chemistry from Oregon State
University, college of Pharmacy in 2004, having had Professor William H. Gerwick as his major advisor. His
major eld of specialization is Pharmaceutical sciences. His minor elds of specialization are medicinal and
natural products chemistry, botany and medicinal plants, Pharmacognosy, marine natural products chemistry,
herbal and alternative medicine. His research interests are quality control of alternative medicine preparations,
isolation and structural elucidation of bioactive secondary metabolites from natural sources, detection of herbal
medicinal preparations adulteration with synthetic chemical substances.
Abeer M. El Sayed: Is a lecturer at the Department of Pharmacognosy, Faculty of Pharmacy, Cairo University,
Egypt. Her research interest is in the area of medicinal plants and its biological potentiality. At faculty of pharmacy
additionally, she is also a manger assistance for the medicinal, aromatic, poisonous plant experimental station.
Dr. Salmin K. Alshalmani: Got her Ph.D. in Pharmacy, School of Biomedical Sciences, Nottingham University -
UK in 2011.
Research Interests of Dr. Salmin are:
1. Isolation and Structure Elucidation of Secondary Metabolites From Natural Sources “Terrestrial Plants And
Marine Organisms” With Important BioPharmaceutical Properties Such As Anticancer, Antimicrobial, Anti- inam-
matory and Antiviral Activities Using Different Advanced Chromatographic and Spectroscopic Techniques.
2. Running biological and pharmacological screening for chemical, natural and semi-synthetic compounds.
3. Formulation of natural products as complementry and alternative medicine.
SUMMARY