Basil (Ocimum basilicum and Ocimum tenuiflorum) Reduces Azoxymethane Induced Colon Tumors in Fisher 344 Male Rats
The objective of this study was to determine the effects of three varieties of ocimum tenuiflorum (Holy Basil) (Denmark (HBD), Cuba (HBC), India (HBI)) and one variety of ocimum basilicum (Culinary Basil) (CB) on Azoxymethane (AOM)-induced colon tumors in Fisher 344 male rats. After a 1 week period of acclimatization, rats were divided into groups. Basil leaf powder was mixed at 1% level in an AIN 93G/M based diet. Rats were administered 2 injections of AOM (s/c injections at 16 mg kg-1 body weight in saline) at 7 and 8 week of age to induce colon carcinogenesis. Rats were killed by CO2 asphyxiation and samples of colon, cecum and liver, were collected. Colon tumors were characterized according to number, size, location and tumors per tumor bearing rat ratio. Feeding Basil (1%) resulted in significantly lower tumor incidence compared to rats fed the control diet. Tumors/tumor bearing rat ratio was reduced by 78% in rats fed Basil diets compared to rats fed the control diet. Tumor size (mm) was significantly (p<0.05) smaller in treatment diets (CB: 1.20, HBD: 0.8, HBC: 0.8, HBI: 0.6 and control: 3.72) compared to control diet. Selected hepatic enzyme activities (Glutathione-S-Transferase, Superoxide dismutase and Catalase) were significantly (p<0.05) higher in the rats fed Basil compared to rats fed the control diet. Results showed that feeding Holy and Culinary Basil significantly (p<0.05) reduced the number of AOM-induced colon tumors in Fisher 344 male rats and therefore may have implications in food industry as a potential chemopreventive agent.
to cite this article:
D. Gajula, M. Verghese, J. Boateng, L. Shackelford, S.R. Mentreddy, C. Sims, D. Asiamah and L.T. Walker, 2010. Basil (Ocimum basilicum and Ocimum tenuiflorum) Reduces Azoxymethane Induced Colon Tumors in Fisher 344 Male Rats. Research Journal of Phytochemistry, 4: 136-145.
Colon cancer is one of the leading causes of cancer mortality and the third
form of cancer in US (Jemal et al., 2007) with
about 108, 070 new cases of colon cancer and 49, 960 deaths expected in 2008
(Bianchi and Burke, 2008). Epidemiological studies indicate
that human diseases such as cardiovascular diseases and cancers can be prevented
by consuming fruits and vegetables and 20-40% of cancer deaths in the US are
preventable by diet modifications (Coates et al.,
2007). Among the cancers of the digestive tract, colon cancer is most responsive
to diet modification (Block and Gyllenhaal, 2002). In
order to reduce the risk of cancer, American Cancer Society (ACS) recommending
the inclusion of whole grains, fruits and vegetables and limited consumption
of red meats in the diet. Nowadays food industry is becoming more and more interested
in herbs and spices because of their flavoring, medicinal and/or antioxidant
Basil (Ocimum basillicum L. and Ocimum tenuiflorum) is well known
for its medicinal value and one of the oldest spices within the ocimum genus
in Lamiaceae family. It is also popular as a culinary herb. The different parts
of the plant are traditionally used for the treatment of various disorders and
as an antidote for snake bites and scorpion stings (Umadevi,
2001). Basil has been used in Turkish folk medicine for many years and has
several beneficial effects for conditions such as digestive and appetite enhancing
effects. It was reported that the leafy parts of basil had tonic, antiseptic
(Kosekia et al., 2002) and insecticidal properties
(Umerie et al., 1998). In addition, Basil is
used for treatment of inflammation, dyspepsia, aches and pains (Umadevi,
According to the Asian Indian traditional system of medicine called Ayurveda,
Holy Basil (Ocimum tenuiflorum) is considered as one of the most effective
and has been widely studied in relation to diabetes and its complications medicinal
herb among the other medicinal plants (Mentreddy, 2007).
Ocimum tenuiflorum has shown both hypoglycaemic and antihyperglycaemic
properties and lowered blood glucose levels in Type 2 diabetic patients. Aqueous
extracts of the leaves and pure eugenol, which is a constituent of the extract,
were reported to reduce the biochemical and membrane changes induced by restraint
stress in rats (Sen et al., 1992). Oral feeding
of Basil leaf powder in rats for a period of one month significantly reduced
fasting blood sugar and cholesterol levels in blood, liver and heart (Rai
et al., 1997). Basil contains phytochemicals such as phenolic acids,
flavonoids, anthocyanins and carotenoids. Rosmarinic acid is the predominant
phytochemical found in O. basilicum (Gerhardt and
Schroter, 1983). Orientin and vicenin, the radio protective flavonoids from
Ocimum tenuiflorum have shown strong inhibitory effects against OH radical
activity (Umadevi, 2001). Rajakumar and Rao (1993) have
reported that isoeugenol, which has a double bond similar to that found in oreintin
and vicenin, is a good free radical scavenger.
Numerous studies reported various effects of Ocimum sp., including anti-inflammatory,
antioxidative, chemopreventive, blood-sugar lowering, nervous system stimulation
and radiation protection have been reported (Chattopadhyay,
1999; Prakash and Gupta, 2000; Umadevi, 2001). However,
there are no reported studies evaluating the chemopreventive potential of Basil
on colon tumorgenesis. In a recent study conducted by our laboratory,
we evaluated the chemopreventive potential of Basil on azoxymethane-induced
Aberrant Crypt Foci (ACF) using Fisher 344 male rat model. Therefore, we have
conducted a long-term study (end point tumor model) on the chemopreventive potential
of Basil on modulating colon tumorgenesis using the Fisher 344 rodent model.
MATERIALS AND METHODS
Animals Housing and Diet
Fifty two Fisher 344 male weanling (3 weeks old) rats were obtained from
Harlan, Indiana and were housed in stainless steel wire cages @ 2 rats per cage
in September 2007. The temperature and relative humidity were maintained at
21°C and 50%, respectively. Light and dark cycles were maintained at 12
h each. All rats were given free access to potable water and rats were fed control
(American Institute of Nutrition 93 Growth (AIN 93 G)) and treatment diets (Reeves
et al., 1993). After a one-week acclimatization period, rats were
divided into 5 groups (10 rats each in treatment groups and 12 rats in control
group). Control rats were given free access to AIN 93 G/M diet throughout the
experimental period (41 week).
|| Composition of the dietsa
|CB: Culinary Basil; HBD: Holy Basil Denmark; HBC: Holy Basil
Cuba; HBI: Holy Basil India. aFormulations of diets based on
AIN-93M: American institute of nutrition (Reeves et
al., 1993). bCommon ingredients (g): casein, 140: Dextrose,155:
Sucrose, 100: Soybean oil, 40: Fiber, 50: Mineral mix (AIN-93G), 35L Vitamin
mix, 10: L-cystein, 1.8: Choline bitartrate, 2.5
Preparation of Diet
Four accessions of Basil leaves namely Culinary Basil, Holy Basil Denmark,
Holy Basil Cuba and Holy Basil India were obtained from the Winfred Thomas Agricultural
Research Station (WTARS), Alabama A and M University, dried using a cabinet
drier (Proctor and Schwartz SCM Corporation, Horsham, PA, USA), ground to a
fine powder and mixed in the diet at 1% level (Table 1).
Feed Intake and Body Weights
Daily feed intakes and biweekly body weights were recorded throughout the
Chemicals and Dietary Ingredients
All biochemicals, except azoxymethane (Midwestern Research Institute, NCI
Repository, Kansas, MO) were obtained from Sigma Chemical, St Louis, MO. Basil
was obtained from Winfred Thomas Agricultural Research Station, Alabama A and
M University, Normal, Alabama.
For induction of ACF, all rats were given s/c injections of Azoxymethane
(AOM), (NCI Chemical Repository, Kansas City, MO.) in saline @16 mg kg-1
b.wt. at 7th week and another at 8th week of age.
Rats were killed by CO2 asphyxiation at 45 weeks of age. The
colons from rats were removed and flushed with Phosphate Buffer Solution (0.1
M, pH 7.2) and prepared for counting ACF. Liver samples were collected and immediately
frozen using liquid nitrogen and stored at -80°C for analysis of enzymes
(Glutathione S-transferase, Catalase and Superoxide dismutase).
Analysis of Cecal Contents
Ceca was flushed with potassium phosphate buffer 0.1 M, pH 7.2 and blotted
on filter paper to measure cecal weight. Cecal contents were removed and pH
Tumors were characterized based on location (proximal and distal), tumor
number, tumor size and TBR ratio (Tumor per tumor bearing rat ratio). The TBR
ratio gives a good picture of chemopreventive benefits of a particular food,
as it indicates the number of tumors in rats that developed tumors. Tumor incidence
(%) in the proximal and distal regions was also reported. Tumors were characterized
as described by Shackelford et al. (1983).
Glutathione-S-Transferase (GST) Activity
The GST in the liver and colonic mucosa was assayed with some modifications
to the procedure as outlined by Habig et al. (1974).
Liver samples (1 g) were homogenized in 10 volumes of potassium phosphate buffer
(pH 7.0, 0.1 M). The homogenates were centrifuged at 10,000x g for 30 min. The
supernatant was centrifuged for a second time at 10,000x g for 10 min. The assay
mixture (1 mL) contained potassium phosphate buffer (0.1 M, pH 6.5), 1-chloro
2, 4-dinitrobenzene (1 mM) and glutathione (1 mM). Reactions were started by
the addition of 100 μL of sample and change in absorbance at 340 nm as
a function of time was monitored using a micro plate reader. Total enzyme activity
was measured at the end of 5 min of reaction.
Determination of Catalase Activity
Liver catalase was estimated in a micro plate reader at 240 nm by monitoring
the decomposition of H2O2 as described by Aebi
(1984). The reaction mixture (1 mL) contained 0.02 mL suitably diluted cytosol
in phosphate buffer (50 mM, pH 7.0) and 0.1 mL of 30 mM H2O2
in phosphate buffer. The specific activity of catalase was expressed as moles
of H2O2 reduced per min per mg protein.
Determination of Superoxide Dismutase (SOD) Assay
Liver superoxide dismutase was assayed by the technique of Fridovich
(1989). One gram of liver sample was diluted in 9 mL of distilled water.
An aliquot of 2.0 mL of the diluted aliquot was added to 2.5 mL of 0.05 M carbonate
buffer (pH 10.2) to equilibrate in the spectrometer and the reaction started
by the addition of 0.3 mL freshly prepared 0.3 mM adrenaline to the mixture
which was mixed by inversion. The reference cuvette contained 2.5 mL buffer,
0.3 mL of substrate (adrenaline) and 0.2 mL of water. The increase in absorbance
at 480 nm was monitored every 30 sec for 150 sec. A single unit of enzyme is
defined as the quantity of SOD required to produce 50% inhibition of autoxidation.
Data were analyzed using the SAS system version 9.0 (SAS Institute, Cary,
NC) by Analysis of Variance. Values are given as Means±SEM and means
were separated using Tukeys studentized range test. The significance was
tested at the p<0.05 level.
Effect of Basil on Weight Gain, Feed intake, Cecal Weight and Cecal pH
Feed intake and weight gain were significantly (p<0.05) higher in the
rats fed the Basil (1%) diets compared to the rats fed the control (AIN-93G)
diet (Table 2). However, feed efficiency ratio (weight gain
per gram of feed intake) of treatment groups was almost equivalent to the control
rats. There were no significant (p<0.05) differences observed in cecal weight
and cecal pH among the rats fed the control (AIN-93G/M) and Basil (1%) diets.
Tumor incidence in the colon of rats fed the control diet was higher compared
to the rats fed the Basil (1%) diets (Table 3). Most tumors
developed in the distal colon in all the rats in the control and treatment groups.
Distal tumor incidence (%) was higher in rats fed CB (100%) followed by HBD
(83.3%), HBC (85.7%) and HBI (50%), where as proximal tumor incidence (%) was
higher in rats fed HBI (50%) compared to the other treatment groups [CB (0%),
HBD (16.7%) and HBC (14.3%]. However, total tumor incidence was lower in the
rats fed the Basil (1%) diets compared to the rats fed the control diet. Rats
fed HBI (30%) had the lowest tumor incidence followed by HBC (40%), CB and HBD
(50%). Over all, 50-70% reductions were seen in tumor incidence in the rats
fed Basil diets compared to the rats fed the control diet.
|| Effect of feeding basil on feed intake, weight gain, cecal
weight and cecal pH in fisher 344 male rats
|Values are Means±SEM; n = 10. Values not sharing a
common superscript are significantly different. (p<0.05) using Tukeys
studentized range test. CB: Culinary Basil, HBD: Holy Basil Denmark, HBC:
Holy Basil Cuba, HBI: Holy Basil India
|| Effect of Basil on tumor incidence (%) in Fisher 344 male
|N1/N2 (rats with tumors/number of rats in the group). CB:
Culinary Basil, HBD: Holy Basil Denmark, HBC: Holy Basil Cuba, HBI: Holy
|| Effect of Basil on tumor numbers in fisher 344 male rats
|N1/N2 (rats with tumors/number of rats in the group). Abbreviations:
CB: Culinary Basil, HBD: Holy Basil Denmark,HBC: Holy Basil Cuba, HBI: Holy
The rats in the control group had the highest number of tumors in both the
distal (36) and proximal (18) sections of the colon (Table 4).
Tumor numbers were higher in the control group compared to the rats fed the
Basil (1%) diets. Among the treatment groups, the number of tumors was lower
in the proximal colon compared to the distal colon. The number of tumors in
the proximal colon was higher in the rats fed HBI (2) compared to the rats fed
HBD (1) and HBC (1), however, the rats fed CB did not develop any tumors in
the proximal colon. In the distal colon, the number of tumors was lower in the
rats fed HBI (2) compared to the rats fed HBD (5), CB (6) and HBC (6). The total
number of tumors was lower in the rats fed HBI (4) compared to the other treatment
groups CB (6), HBD (6) and HBC (7). The reductions (%) in tumor numbers compared
to the control were 93, 89, 89 and 87 in the treatment groups fed CB, HBD, HBC
Rats fed Basil (1%) diets had significantly (p<0.05) smaller tumors (mm)
compared to the rats fed the control diet in both the proximal and distal colon
(Table 5). Among the treatment groups, rats fed HBD (0.20)
and HBC (0.20) had smaller tumors compared to the rats fed HBI (0.60) in the
proximal colon. In the distal colon, rats fed HBI had significantly (p<0.05)
smaller tumors (0.60) compared to the rats fed HBD and HBC (1.40) and CB (2.40).
Reductions (%) in tumor size compared to control rats were highest in the rats
fed HBI (88.1), followed by HBD (72.2), HBC (72.2) and CB (52.4). The total
(proximal and distal) average tumor size (mm) in rats fed the control diet was
the highest (3.72).
|| Basil effect on tumor size (mm) in Fisher 344 male rats
|N1/N2 (rats with tumors/number of rats in the group). Values
are means. Values not sharing a common superscript are significantly (p<0.05)
different using Tukeys studentized range test. CB: Culinary Basil,
HBD: Holy Basil Denmark, HBC: Holy Basil Cuba, HBI: Holy Basil India
|| Basil effect on tumors per tumor bearing rat ratio (TBR)
in Fisher 344 male rats
|N1/N2 (rats with tumors/number of rats in the group). CB:
Culinary Basil, HBD: Holy Basil Denmark, HBC: Holy Basil Cuba, HBI: Holy
The reductions (%) in tumor size compared to the control in rats fed HBI (83.8)
was the highest, followed by HBD and HBC (78.5) and lowest in the group fed
Tumors/Tumor Bearing Rat Ratio (TBR)
Tumors per Tumor Bearing Rat ratio (TBR) is the ratio of the number of tumors
in rats that developed tumors. The TBR ratios ranged from a high of 4.5 in the
rats fed the control diet to a low of 1.0 in the rats fed CB and HBI diets.
(TBR ratio was higher in rats fed the control (AIN-93G/M) diet compared to the
rats fed Basil (1%) diets as shown in Table 6). The greatest
reduction (%) in TBR ratio was observed in rats fed CB and HBI (77.8) followed
by HBD (73.3) and HBC (68.9) compared to the rats fed the control diet.
Hepatic Glutathione S-Transferase (GST) Activity
The GST activity (Units mg-1) in the liver and colonic mucosa
were significantly (p<0.05) higher in rats fed the Basil (1%) diets compared
to rats fed the control (AIN-93G/M) diet. The GST activity in the liver (Units
mg-1) ranged from a low of 6.15 in the rats fed the control diet
to a high of 22.05 in rats fed 1% HBI diet. Among the rats fed the Basil (1%)
diets, those fed HBI had the highest GST activity in the liver (22.05) followed
by HBC (15.24), HBD (14.84) and CB (12.97). A 2-3 fold increase was observed
in GST activity in rats fed Basil (1%) diets compared to the rats fed control
(AIN-93G/M) diet (Table 7).
Catalase (CAT) and Super Oxide Dismutase (SOD) Activity
The effect of feeding Basil on hepatic antioxidant enzymes (SOD and CAT)
in rats is shown in Table 8. The activities of these enzymes
were found to be significantly (p<0.05) higher in the liver of Basil fed
rats compared to the control rats. The CAT activity (μmol mL-1)
ranged from a low of 21.13 in rats fed the control diet to a high of 103.26
in rats fed 1% HBD diet. There were no significant (p<0.05) differences observed
with in the treatment groups. A 3.5-4.9 fold increase in CAT activity was observed
in the treatment groups compared to the control group.
|| Hepatic and colonic mucosa Glutathione-S-transferase activity
in the Fisher 344 male rats fed Basil
|CB: Culinary Basil, HBD: Holy Basil Denmark, HBC: Holy Basil
Cuba, HBI: Holy Basil India, CMS: Colonic Mucosal Scrapings. Values are
Means±SEM; n = 10. Values not sharing a common superscript are significantly
different (p<0.05) using Tukeys studentized range test.
|| Effect of Basil on Catalase (CAT) and Superoxide Dismutase
(SOD) activities in Fisher 344 male rats
|CB: Culinary Basil, HBD: Holy Basil Denmark, HBC: Holy Basil
Cuba, HBI: Holy Basil India. Values are Means±SEM; n = 10. Values
not sharing a common superscript are significantly different (p<0.05)
using Tukeys studentized range test
The activity of SOD (Units mL-1) ranged from a low of 2.93 in the
rats fed control diet to a high of 6.45 in rats fed 1% HBC. Among the treatment
groups, rats fed 1% HBI had significantly (p<0.05) lower SOD activity compared
to the rats fed 1% HBC. A 2.0-2.2 fold increase in SOD activity was seen in
the rats fed the Basil (1%) diets compared to the control group.
The objective of this study was to determine the long term effects of feeding
Basil (Ocimum basilicum and Ocimum tenuiflorum) on colon tumorigenesis
in azoxymethane-induced colon carcinogenesis in Fisher 344 male rats. To our
knowledge this is the first animal model experiment studying the antitumorigenic
effects of Basil against colon cancer. In previous studies, Basil (Ocimum
basilicum) has been shown to reduce the risk of skin and forestomach papillomagenesis
(Dasguptha et al., 2004).
In this study, feed intake (g day-1) was significant (p<0.05) at the end of the 45 week study. This may due to the strong aroma and flavor of the volatile oils present in Basil. Because the rats fed Basil (1%) consumed more diet, we observed a significantly (p<0.05) higher weight gain compared to the control group. However, there were no significant (p<0.05) differences observed in cecal weight and cecal pH.
Feeding Basil (1%) resulted in significantly lower tumor incidence compared
to the rats fed the control diet. Tumor incidence and number of tumors were
higher in the control fed rats. Basil (1%) diets reduced tumor incidence by
50-70% compared to the control diet. The results of this study are comparable
to the lower tumor incidence (25%) reported following administration of Basil
leaves for 12 weeks on 3'-methyl-4-dimethylaminoazobenzene (3'MeDAB) induced
neoplasia in mice stomachs (Aruna and Sivaramakrishnan,
1990). We observed a greater reduction in tumor incidence compared to the
report by Dasguptha et al. (2004), where feeding
Basil (Ocimum basilicum) leaves reduced tumor incidence by 20-40% in
benzo(a)pyrene-induced forestomach papillomagenesis in mice.
Slower growth of tumors with longer induction time was seen in mice supplemented
with Ocimum tenuiflorum seed (essential oil) compared to MCA (20-methylcholanthrene)
injected mice which may also have accounted for the enhanced survival rate of
the mice (Prakash and Gupta, 2000). In present study,
feeding Basil (1%) resulted in lower tumors per tumor bearing rat ratio (TBR)
(the number of tumors in rats that developed tumors), which may suggest the
chemopreventive potential of Basil. Rats fed Basil (1%) diets had significantly
(p<0.05) smaller tumors compared to the rats fed the control diet in both
the proximal and distal colon indicating that Basil (Ocimum basilicum
and Ocimum tenuiflorum) may have anti-inflammatory and anti angiogenic
properties. The essential oils extracted from Sweet Basil (Ocimum basilicum)
were reported to have higher antiproliferative activity (12 times more potent)
than 5-FluroUracil (Manosroi et al., 2005). The
hepatic antioxidant enzymes, Super Oxide Dismutase (SOD) and Catalase activities
were significantly (p<0.05) higher in the rats fed Basil (1%) diets compared
to the rats fed the control diet. SOD plays an important role in the antioxidant
enzyme defense system by converting superoxide radicals into hydrogen peroxide
(Li et al., 2000). The induction of SOD activity
in the rats fed the Basil (1%) diets may have caused the scavenging of Reactive
Oxygen Species (ROS) and the dismutation of superoxide radicals. Catalase activity
was significantly (p<0.05) higher after feeding Basil (1%) diets. Catalase
may have assisted in removing the hydrogen peroxide radicals produced by the
action of SOD. An increase in SOD activity, along with that of catalase, may
have resulted in lower oxidative stress and damage to cells thus resulting in
reduction of initiation of cancer. Glutathione-S-Transferase (GST) activity
was significantly (p<0.05) increased in the rats fed Basil (1%) diets compared
to the rats fed the control diet. The elevated levels of GST induced by the
Basil (1%) diet may contribute to its anticarcinogenic effects. GST enzymes
are involved in the metabolism of a wide variety of electrophilic carcinogens
(Alexandrov et al., 2002). GSTs are a family
of enzymes that assist in the excretion of carcinogens by making them soluble
via conjugation with GSH (Sundberg et al., 2002).
Thus, GSTs are used as a biomarker to investigate the chemopreventive effects
of agents (Salinas and Wong, 1999).
The results of this study show that dietary Basil may have significant implications as a chemopreventive agent. Although, all the mechanisms of action are not fully known, there is evidence suggesting its apoptotic, anti-inflammatory, anti-oxidative and anti-proliferative roles. Induction of critical detoxification and antioxidative enzymes may also have played a significant role in reducing Azoxymethane-induced colon tumors. Human clinical trials will need to be conducted to further explain its chemopreventive action.
This study was supported by funding from The Alabama Agricultural Experimental Research Station, Alabama Agricultural and Mechanical University, Normal, AL 35762.
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