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Oroxylum indicum stem bark extract exerts antitumor potential against Ehrlich’s ascites carcinoma in Swiss albino mice

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Abstract

Introduction and Aim: Constant efforts are exerted to explore unique bioactive principles from natural sources that possess more effective and specific antineoplastic activities. In the present study, we aimed to evaluate the antitumor activity of stem bark extract of Oroxylum indicum in mice bearing Ehrlich ascites carcinoma (EAC). Materials and Methods: Ninety female Swiss albino mice were categorized into fifteen groups (n=6). The animals were inoculated with 1x106 EAC cells. Tumor control animals received sterile water once daily for 10 consecutive days. Positive control group was injected with Cisplatin (CP) (one dose – 3.5 mg/kg body weight). The treatment groups were administered with O. indicum (OI) stem bark ethanol extract once daily with 50mg/kg, 200mg/kg and 400mg/kg body weight for eleven consecutive days. The blood parameters and serum hepatic enzymes activity was determined. The percentage increase in weight, the median survival time, the increase in median life span was calculated. The cytotoxic effect of CP and OI extract was determined. Results: There was significant reduction in the white blood cells count in OI and CP treatment group compared to increased level in EAC control group. The RBC count and Hemoglobin level which was significantly decreased (p<0.05) in the tumour mice, was enhanced in the drug treatment groups. The EAC control group showed significant increase in tumour cell count (p<0.05) whereas, treatment of EAC tumor bearing mice with OI and CP significantly increased the non-viable tumor cell count (p<0.05). Conclusion: OI stem bark ethanol extract reduced the toxic implications of Ehrlich ascites carcinoma, reverted the haematological and biochemical changes induced by tumour. These results call for additional research on isolating and identifying the responsible bioactive elements in order to clarify the underlying processes of the anticancer impact.
Biomedicine: 2022; 42(4): 686-692 July - August 2022
DOI: https://doi.org/10.51248/.v42i4.1559 Biomedicine- Vol. 42 No. 4: 2022
Research article
Oroxylum indicum stem bark extract exerts antitumor potential against
Ehrlich’s ascites carcinoma in Swiss albino mice
Sharmila K.P.1, Shilpa S. Shetty1, Suchetha Kumari2, Madhyastha Harishkumar3, Ashwini Prabhu4
Satheesh Kumar Bhandary B.5
1Central Research Laboratory, 2Dept. of Biochemistry,5Dept. of Otorhinolaryngology, K.S Hegde Medical Academy,
NITTE (Deemed to be) University, Deralakatte, Mangaluru, Karnataka, India
3Dept. of Cardio-Vascular Physiology, Faculty of Medicine, University of Miyazaki, Japan
4Dept. of Biosciences, Yenepoya Medical College, Yenepoya (Deemed to be) University, Mangaluru, Karnataka, India
(Received: February 2022 Revised: May 2022 Accepted: May 2022)
Corresponding author: Satheesh Kumar Bhandary B. Email: satheeshbhandary@gmail.com
ABSTRACT
Introduction and Aim: Constant efforts are exerted to explore unique bioactive principles from natural sources
that possess more effective and specific antineoplastic activities. In the present study, we aimed to evaluate the
antitumor activity of stem bark extract of Oroxylum indicum in mice bearing Ehrlich ascites carcinoma (EAC).
Materials and Methods: Ninety female Swiss albino mice were categorized into fifteen groups (n=6). The animals
were inoculated with 1x106 EAC cells. Tumor control animals received sterile water once daily for 10 consecutive
days. Positive control group was injected with Cisplatin (CP) (one dose 3.5 mg/kg body weight). The treatment
groups were administered with O. indicum (OI) stem bark ethanol extract once daily with 50mg/kg, 200mg/kg and
400mg/kg body weight for eleven consecutive days. The blood parameters and serum hepatic enzymes activity was
determined. The percentage increase in weight, the median survival time, the increase in median life span was
calculated. The cytotoxic effect of CP and OI extract was determined.
Results: There was significant reduction in the white blood cells count in OI and CP treatment group compared to
increased level in EAC control group. The RBC count and Hemoglobin level which was significantly decreased
(p<0.05) in the tumour mice, was enhanced in the drug treatment groups. The EAC control group showed
significant increase in tumour cell count (p<0.05) whereas, treatment of EAC tumor bearing mice with OI and CP
significantly increased the non-viable tumor cell count (p<0.05).
Conclusion: OI stem bark ethanol extract reduced the toxic implications of Ehrlich ascites carcinoma, reverted the
hematological and biochemical changes induced by tumour. These results call for additional research on isolating
and identifying the responsible bioactive elements in order to clarify the underlying processes of the anticancer
impact.
Keywords: Oroxylum indicum; cisplatin; Ehrlich ascites carcinoma; hepatic enzymes; hematology.
INTRODUCTION
he effectiveness of medicinal plants in curing
practically all human illnesses has been
established. Numerous recognized and
unidentified phytochemicals have reportedly been
extracted, isolated, and clinically investigated for their
potential therapeutic benefits (1).
The bioactive chemicals that have been extracted from
various plant sections have been used to create a
number of contemporary medications (2). These
phytomedicines are employed in traditional medical
systems because they are readily available, highly
specific, and effective in actions with less side effects
and lower prices than synthetic pharmaceuticals. The
rise of lifestyle disorders like diabetes, cardiovascular
problems, and cancer has brought attention to ongoing
efforts to develop potential remedies utilizing natural
resources. In the world, cancer has become one of the
main causes of death, taking over 6 million lives each
year (3). In the series of malignant diseases, the
patients suffer from the unregulated multiplication of
abnormal cells which invade the body and initiate
atypical progression at other sites (4). The current
treatment modality for this deadly disease
(chemotherapy, radiotherapy, and surgery) possesses
some drawbacks, such as high cost, unavailability in
the resource-limited countries, loss of normal cells,
development of secondary malignancies and serious
post-treatment complications, thus increasing the
demand for the introduction of novel drugs (5). The
alternative approach is the screening of potential
candidate plants used in traditional systems of
medicine for novel pharmacologic activities. Several
clinically promising phytochemicals, such as vinca
alkaloids (vincristine and vinblastine), bleomycin,
paclitaxin, taxol, etc., are currently used for treating
several neoplastic diseases in humans. Some unique
bioactive compounds from natural sources possess
T
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more effective and specific antineoplastic activities.
Due to this property, continuous efforts are being
exerted globally for their exploration.
Oroxylum indicum (L.) Kurz is distributed in southeast
and South Asian nations. It is indigenous to India and
is grown all throughout the country's forested areas,
primarily in the Western Ghats and the foothills of the
Himalayas. The Indian government has designated it
as a medicinal plant that is fragile. The Indian people
use O. indicum extensively to cure a variety of
illnesses (6).
The wide traditional usage of O. indicum and the lack
of scientific study on this medicinal plant were the
main factors that encouraged us to study the antitumor
activity of stem bark extract of O. indicum in mice
bearing Ehrlich ascites carcinoma. Further, the
antineoplastic effects in this study was particularly
carried out in the advanced stage of tumor growth with
Ehrlich ascites carcinoma, since cancer is mostly
detected in late stages.
MATERIALS AND METHODS
The entire experiments were carried out at the Central
Research Laboratory, K.S Hegde Medical Academy
after obtaining ethical clearance from the Institutional
Animal Ethics Committee, K.S Hegde Medical
Academy (Ref: KSHEMA/IAEC/17/2017).
Plant material and extraction
Oroxylum indicum (OI) stem bark was collected from
Mangaluru region. The fresh stem bark was cut into
small pieces, thoroughly cleaned with distilled water
to eliminate any remaining plant matter before being
allowed to air dry for five days at 27°C30°C. The
dried stem bark was ground into a fine powder using a
mixer grinder and then subjected to Soxhlet extraction
using 99% ethanol for 72 hours. The stem bark extract
was dried using a rotary flash evaporator (Rotavap
superfit PBU-6) for 15 minutes at 60°C before being
placed in an airtight container and kept in the fridge
until needed. A taxonomist from Alva's College in
Moodubidri, Dakshina Kannada, recognized and
verified the stem bark.
Experimental work
Female Swiss albino mice (n=90), ranging in age from
four to six weeks and weighing 25 ± 5 g, were chosen
from the animal house facility. The experimental
chamber, which had a temperature of 23 ± 2°C,
controlled humidity levels, and a cycle of light and
dark lasting 12:12 hours, was acclimated by the
animals. The mice were kept in sterile polypropylene
cages with bedding made of sterile rice husk, with a
maximum of six mice per cage. The mice were given
free access to water and autoclaved normal mice diet
pellets. The animal experiments were carried out
according to the guidelines of the Institutional Animal
Ethics Committee (IAEC) after obtaining the ethical
clearance (Ref: KSHEMA/IAEC/17/2017).
Ehrlich Ascites Carcinoma (EAC) cells were initially
procured from the Radiobiology laboratory, KMC,
Manipal, Karnataka, India. They were maintained by
weekly intraperitoneal (i.p.) inoculation of 106
cells/mouse.
Acute toxicity studies
The acute toxicity studies were conducted to
determine the safe dose of O. indicum (OI) stem bark
extract according to OECD guidelines (7). Six female
Swiss albino mice were allowed to fast by removing
food and water for 18 hours. The oral drug
administration (OI - 2000 mg/kg body weight) was
followed immediately by the administration of food
and drink to the animals. To prepare the doses,
distilled water was used, and the dose volume was
limited to 1 mL per 100 g of body weight. Following
administration of the test drugs, the animals were
continually monitored for the first 4 hours, 24 hours,
and 48 hours to observe for any changes in overall
behavior or physiological activity and mortality (8).
Analysis of hematological parameters
Female Swiss albino mice weighing 20 ± 5 g and aged
46 weeks were used as the test subjects. Each mouse
received 1x106 EAC cells in 0.1 ml of physiological
saline. They were divided into the subsequent groups
(n = 6).
Group I - Tumor control: The animals of this group
were orally administered sterile water once per day
for a total of 11 days.
Group II Positive control: The animals in this
group received a single injection of 3.5 mg/kg body
weight of cisplatin.
Groups III, IV and V were orally administered with
O. indicum stem bark extract at doses of 50 mg/kg,
200 mg/kg, and 400 mg/kg body weight
respectively once daily for 11 consecutive days,
with the first administration beginning 24 hours
after tumour inoculation.
All the test animals were routinely checked for
changes in body weight, toxicological symptoms, and
mortality. After tumour inoculation, the weights of the
animals were measured every third day across all
groups. Blood was drawn from each mouse by cardiac
puncture with the anticoagulant heparin. The total
white blood cell count (WBC), differential leukocyte
counts, total red blood cell count, and hemoglobin
content was measured using veterinary blood counter.
(ERMA INC. model PCE-210VET, Japan).
Determination of hepatic enzymes activity and
biochemical markers
Serum was separated, and using a semi-automatic
analyzer (Star 21 Plus Rapid Diagnostics) and a
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commercial kit in accordance with the manufacturer's
instructions, the activity of SGOT, SGPT, and ALP
was assessed. A semi-automatic analyzer was used to
determine the amounts of total protein, uric acid, and
triglycerides in the separated serum using a
commercial kit and following the manufacturer's
instructions.
Determination of mean survival time (MST) and
average body weights of tumor bearing mice
Six mice per group were used in a separate experiment
to determine how cisplatin and OI extract affected the
length of survival time. The percentage increase in
body weight was calculated using the formula -
percent increase in weight = [(animal weight on
corresponding day/animal weight on day 0) - 1] 100.
(9). The formula: [first death + final death in the
group]/2 was used to compute the median survival
time (MST), as previously stated by Uma Devi et al.
The formula (MST of treated mice - MST of control)
x100]/MST of control was used to calculate the
increase in median life span (percent IMLS) as
previously described by Uma Devi et al. (10).
Effect on the tumor cell viability in vitro
Six mice per group were used in a separate experiment
to investigate the cytotoxic effects of the test
substances as detailed earlier by Mazumdar et al.,
1997. (11). On the 11th day of tumour development,
0.1 mL of ascitic fluid was aseptically aspirated.
Trypan blue and cell suspension were combined
thoroughly in equal parts. Hemocytometer was
charged with the diluted suspension. Under a
microscope, the viable cells (unstained) in the WBC
chamber were counted, and the average number of
cells in the four chambers was determined as follows:
Total number of cells = mean number of cells ×
dilution factor × 104.
Statistical analysis
The obtained results were analyzed by ANOVA test
and expressed as Mean ± SEM. Tukey’s multiple
comparison test was used for intergroup comparison
by Prism 7.0 software. A ‘p’ value < 0.05 was
considered statistically significant. For all in vivo
experiments, six animals were used per group.
RESULTS
Effect of OI Ex on body weight changes in EAC
bearing mice
After the tumour started to develop on day 5, a
continuous rise in body weight was seen up to end of
the study (11th day). The maximum gain of body
weight was observed in the EAC control group. In
case of OI 200 mg treated group, a significant
decrease in body weight was observed (p < 0.001) on
day 9 and in CP treatment group a significant decrease
in body weight was observed (p < 0.001) on day 6 and
day 9 compared to EAC mice (Table 1).
The WBC count in the EAC tumor bearing mice was
found to be elevated compared to the control mice
which was significantly different (p<0.05). OI-200
mg, OI - 400mg/kg body weight and CP 3.5 mg
significantly reduced (p<0.05) the WBC count
compared to EAC group. RBC count and hemoglobin
level which was significantly decreased (p<0.05) in
the tumor mice was enhanced in the drug treatment
groups. The significantly decreased level of platelet
counts in the tumor bearing mice did not show any
improvement in the drug treatment groups (Fig.1).
Effect of (OI Ex) on hepatic enzyme activity in
EAC bearing mice
We observed elevated activity of SGPT, SGOT, ALP
in EAC control group. However, the SGPT activity in
the control and Cisplatin treatment groups decreased
significantly (p < 0.05) compared to tumor control.
Whereas the OI extract treated groups did not exhibit
significant changes in SGPT activity. The tumor
control group exhibited increased SGOT activity
whereas the control, CP and OI Ex treated animals
showed significant decrease in the SGOT activity
(p<0.05). No significant changes were observed in
alkaline phosphatase activity in the Control, CP, OIEx
treated groups compared to tumor control (p>0.05)
(Fig. 2). Total protein level also did not exhibit any
significant changes between the tumor control and
treatment groups. There was a significant increase in
the uric acid level of the tumor control group whereas
the control and treatment groups showed significant
decrease in the uric acid level (p<0.05). The serum
triglyceride level decreased in the tumor control group
whereas the control and treatment groups showed
increased level of triglycerides (p<0.05) which was
significantly different (Fig. 3).
Table 1: Effect of OI Ex on body weight changes in
EAC bearing mice
Group
Percent increase in weight as compared
to 0th day
Day 3
Day 6
Day 9
EAC
control
6.42±0.45
19.94±4.71
27.54±5.06
OI-50
4.48±1.74
14.20±2.28
23.42±3.65a
OI-200
4.60±0.40
7.65±1.73
10.85±1.0a
OI-400
3.66±2.32
11.18±4.44
11.86±3.42
CP-3.5
2.81±1.07
3.99±1.59a
4.51±1.47a
In the present study, significant increase in body
weight, ascitic tumor volume, tumor weight and tumor
cell count were observed in EAC control (p<0.05).
Treatment of EAC tumor bearing mice with OI extract
and cisplatin significantly decreased the body weight,
viable tumor cell count and increased the non- viable
tumor cell count (p<0.05).
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Fig. 1. Effect of OI Ex on Hematological parameters such as WBC count (1A), RBC count (1B),
Hb level (1C) and Platelet count (1D) in EAC bearing mice. Values are expressed as Mean ± SEM, (n=6 per group),
a = p<0.05 as compared to EAC tumor control group.
Fig.2: Effect of OI Ex on hepatic enzyme activity such as SGPT (2A), SGOT (2B) and alkaline phosphatase (2C) in
mice with EAC. Values are expressed as Mean ± SEM, (n=6/ group), a= p<0.05 as compared to EAC tumor control group.
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Fig. 3: Effect of OI Ex on Total Protein (3A), Uric acid level (3B) and Triglyceride level (3C) in EAC bearing
mice. Values are expressed as Mean ± SEM, (n=6 per group), a = p<0.05 as compared to EAC tumor control group
Table 2: Effect of OI extract on survival time in EAC bearing mice
Groups
Increase in median
life span (%IMLS)
EAC control
____
OI 50
0
OI 200
33.33
OI 400
16.66
CP-3.5
83.33
Fig.4. Effect of OI Ex on cell viability in EAC bearing mice (4A & 4B) by trypan blue dye exclusion assay.
Values are expressed as percentage, (n=6 per group), a = p<0.05 as compared to EAC tumor control group
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DISCUSSION
Ascitic fluid is an essential nutritional requirement for
the growth of EAC cells and a rapid increase in ascitic
fluid would be a means to meet the nutritional
requirement of tumor cells (12).
Mice with tumours gained more weight because of an
increase in ascitic fluid volume. In the current study,
the EAC control group showed an increase in body
weight, ascitic tumour volume, tumour weight, and
tumour cell count. OI extract and cisplatin treatment
dramatically reduced body weight, the number of
viable tumour cells, and raised the number of non-
viable tumour cells in mice carrying EAC tumours.
These findings point to either a direct cytotoxic effect
of OI extract and CP on tumour cells or a local indirect
effect that may include macrophage activation and
suppression of vascular permeability (13).
Anemia and myelosuppression caused by hemolytic or
myelopathic diseases have frequently been seen in
ascites carcinoma due to iron shortage, which
ultimately results in a decrease in the amount of RBC.
The Hb content, RBC count, and WBC count all
returned to normal following treatment with OI
extract. These findings from our study indicate the
haematoprotective properties of OI extract (14).
Serum enzymes are crucial neoplastic diagnostic
indicators and for understanding the state of the
disease. According to a number of studies, tumour
cells harm the liver and disrupt the metabolism of
hepatic cells, which alters the activity of serum
enzymes. Similar findings were found in our
investigation, which revealed higher SGPT, SGOT,
and ALP levels in the EAC control group. It is
possible to interpret the elevated levels of these
biochemical indicators because of EAC-induced
hepatocellular damage. Treatment with cisplatin and
OI extract at all three doses returned the increased
SGOT activity to normal range, showing protection
against hepatotoxicity caused by tumour cell generated
toxicity. (15).
Total protein levels significantly decreased in tumor-
bearing animals, which may be explained by enhanced
neoplastic cell mitosis, high blood flow and capillary
permeability, which allow plasma proteins to escape
into the peritoneal cavity, as well as hepatic cell
necrosis (16).The nuclear degenerative alterations
could be the cause of reduced total protein level that
were seen in both the current investigation and
previous studies (17). Similarly, Habib et al. (18)
found that mice carrying EAC had significantly lower
levels of total protein and albumin.
The constant standards for evaluating the effectiveness
of any anticancer medication have been life
expectancy extension and a drop in WBC (19). The
life span of the mice with EAC was clearly extended
when OI extract was given to the animals by limiting
the activity of the EAC cells. Animals with cancer
may live longer if nutritive fluid volume is reduced
and tumour growth is stopped. A similar effect was
shown in EAC-bearing mice treated with OI extract
(20). The plant extract was successful in lowering the
ascites fluid volume, increasing the percentage of life
span, and decreasing the number of viable cells, all of
which support its anticancer capabilities. Trypan blue
dye exclusion assay for in vitro cytotoxicity studies
revealed that O. indicum extract is toxic to the EAC
(21).
Patients with malignancy frequently experience
disturbances in their glucose metabolism, and
hypoglycemia is a hallmark of all cancers (22).
Uncontrolled gene expression raises the concentration
of proteins, and as cells divide more quickly, the level
of uric acid rises in EAC-bearing animals. Since liver
is the immediate target organ affected by fast growing
EAC cells, it causes alteration in the lipid profile (23).
In our study, we found that the OI extract treated
animals restored the biochemical alterations caused by
EAC cells. This demonstrates the anticancer efficacy
of OI extract on EAC cells.
The bioactive substances Scutellarein, Baicalein,
OroxylinA-7-O-beta-D-glucuronide, Hispidulin,
Oroxylin B, Chrysin derivative, and Oroxylin A,
which were found in the extract by LC-MS, may be
the cause of the anticancer potency of OI stem bark
extract (24).
CONCLUSION
The current discovery that Oroxylum indicum's
ethanolic stem bark extract has tumour growth
inhibitory activity is highly encouraging and verifies
the plant's traditional use as a medicine, which may be
explained by the combined effects of the
phytochemicals it contains. The potency of the active
substances (Scutellarein, Baicalein, OroxylinA-7-O-
beta-D-glucuronide, Hispidulin, Oroxylin B, Chrysin
derivative, and Oroxylin A) may be increased by
certain minor compounds, which may have an additive
or synergistic effect, lessen the toxic effects of the
treatment, reverse the changes in haematological
parameters caused by tumours, and provide significant
benefit. These findings call for additional research on
isolating and identifying the bioactive component(s)
that are responsible for the anticancer action in order
to clarify the underlying mechanism(s).
ACKNOWLEDGEMENT
The authors remain grateful to NITTE (Deemed to be
University) for providing the facilities to carry out this
research study. We remain thankful to the
radiobiology laboratory, KMC, Manipal, Karnataka
for providing the Ehrlich Ascites Carcinoma (EAC)
cells.
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CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
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