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Research Paper
Studies on
Dalbergia sissoo
(Roxb.) leaves: Possible
mechanism(s) of action in infectious diarrhoea
S. Brijesh
a
, P. G. Daswani
a
, P. Tetali
b
, N. H. Antia
a, c
, T. J. Birdi
a
ABSTRACT
a
The Foundation for Medical
Research, 84A, RG Thadani
ObjectiveObjective
ObjectiveObjective
Objective: Several medicinal plants have been evaluated for their antidiarrhoeal activity.
Marg, Worli, Mumbai –
Most studies evaluated their effect on intestinal motility and antimicrobial activity and,
400018, Maharashtra, India.
therefore, did not take into account the pathogenesis of infectious diarrhoea. Features of
b
Naoroji Godrej Centre for
infectious diarrhoea like abdominal pain, cramps, inflammation, and passage of blood/
Plant Research, Lawkin Ltd.
mucus in the stools are the combined effect of one or more virulence factors of the infect-
Campus, Shindewadi, Shirwal,
ing organism. The effect of medicinal plants on the microbial virulent features can serve
Satara – 412801, Maharashtra,
as marker(s) for testing their efficacy. In this study, we evaluated the effect of a decoction
India.
c
The Foundation for Research
of dried leaves of
Dalbergia sissoo
on aspects of pathogenicity, that is, colonisation to
in Community Health, 3-4,
intestinal epithelial cells and production/action of enterotoxins. This was done to define
Trimiti-B Apts, 85, Anand Park,
its possible mechanism(s) of action in infectious diarrhoea.
Pune – 411 007, Maharashtra,
Materials and MethodsMaterials and Methods
Materials and MethodsMaterials and Methods
Materials and Methods: Antibacterial, antiprotozoal, and antiviral activities of the plant
India.
decoction were checked by agar dilution method, tube dilution method, and neutral red
uptake assay, respectively. Cholera toxin (CT) and
Escherichia coli
labile toxin (LT) were
Received:Received:
Received:Received:
Received: 13.9.2005
assayed by ganglioside monosialic acid receptor ELISA. Suckling mouse assay was used
Revised:Revised:
Revised:Revised:
Revised: 20.12.2005
to assess
E. coli
stable toxin (ST). As a measure of colonisation, the effect against adher-
Accepted:Accepted:
Accepted:Accepted:
Accepted: 3.1.2006
ence of
E. coli
and invasion of
E. coli
and
Shigella flexneri
to HEp-2 cells were studied.
Correspondence to:Correspondence to:
Correspondence to:Correspondence to:
Correspondence to:
ResultsResults
ResultsResults
Results: The decoction had no antibacterial, antiprotozoal, and antiviral activity. It re-
Tannaz J. Birdi
duced the production and the binding of CT and bacterial adherence and invasion.
Email:
ConclusionConclusion
ConclusionConclusion
Conclusion: This study showed that
D
.
sissoo
is antidiarrhoeal as it affects bacterial viru-
frchbom@bom2.vsnl.net.in
lence. However, it has no antimicrobial activity.
KEY WORDSKEY WORDS
KEY WORDSKEY WORDS
KEY WORDS: Gastrointestinal infection, Indian rosewood, plant antimicrobial.
Introduction fever, ulcers, digestive disorders, and skin diseases.
[3],[4]
It is
also known to be effective against diarrhoea and dysentery.
[3],[5]
Infectious diarrhoea is the most common infectious disease
worldwide.
[1]
Gastrointestinal infections kill 1.8 million people
Furthermore, this plant had the highest frequency of quote
(5.2%) in an ethnobotanical survey carried out by us
globally each year, mainly children in developing countries.
[2]
(unpublished observation). To the best of our knowledge, no
Acute, watery, bloody diarrhoea may be due to a variety of
experimental evidence is available on its antidiarrhoeal activity.
pathogens- bacterial (e.g., Escherichia coli, Vibrio cholerae,
This work was, therefore, undertaken to assess the
Shigella flexneri, and Campylobacter jejuni), protozoal (e.g.,
Giardia lamblia, Entamoeba histolytica and Cryptosporidium
antidiarrhoeal activity of the dried leaves of D. sissoo on
parvum) and viral (e.g. rotavirus, astrovirus, and adenovirus)
antimicrobial (antibacterial, antiprotozoal, and antiviral)
agents. These organisms disrupt intestinal functions and cause
activity and bacterial virulence parameters, such as,
diarrhoea through several mechanisms. These include
colonisation, production and action of toxins.
microbial attachment to the intestinal epithelium and localised
Materials and Methods
effacement, production of toxin(s), and penetration and
invasion of intestinal epithelial cells that result in alteration
The study design
of absorption due to the rearrangement in cytoskeletal
The institutional ethical committee (IEC) and Committee
structure.
[1]
for the Purpose of Control and Supervision of Experiments on
Dalbergia sissoo Roxb. (Fabaceae), known as Indian
Animals (CPCSEA) approved this study. The clearance from
Rosewood, is reported to be useful in many conditions including
IEC was obtained in December, 2002.
Indian J Pharmacol | April 2006 | Vol 38 | Issue 2 | 120-4
120
Cell cultures, media, and reagents
The human laryngeal epithelial cell line, HEp-2, and the
embryonic monkey kidney cell line, MA104, were obtained from
National Centre for Cell Sciences, Pune, India. The cell lines
were maintained in Dulbecco’s modified eagle medium (DMEM)
and minimal essential medium (MEM), respectively,
supplemented with 5% fetal calf serum (FCS) in 60 mm
diameter tissue culture dishes (Tarsons Pvt. Ltd, Kolkata) at
37
o
C in a 5% CO
2
atmosphere. The cells were maintained in
logarithmic growth by passage every 3-4 days.
The bacterial growth media and MEM were purchased from
Himedia laboratory, Mumbai, India. DMEM and FCS were
procured from GibcoBRL, UK. The constituents of the
Diamond’s medium for G. lamblia and the antibiotics (penicillin,
streptomycin, gentamicin, and metronidazole) were procured
from local manufacturer. Trypan blue, neutral red, polymyxin
B sulphate, anticholera toxin, and bovine serum albumin were
purchased from Sigma, USA, and swine anti-rabbit
immunoglobulin (Ig) was obtained from Dako, Denmark.
The 96-well ELISA plates were purchased from Nunclon,
Denmark, and the ELISA plate reader was purchased from
Labsystems, Finland.
Preparation of plant extract
D. sissoo leaves were collected from Parinche valley, Pune
district, Maharashtra in March 2004 and a voucher specimen
deposited at the Botanical Survey of India, Pune, under
herbarium number 124673. The decoction was prepared by
boiling 1 g of the shade dried leaves in 16 ml of the distilled
water till the volume was reduced to 4 ml. To replicate the
conditions in field, fresh decoction was prepared every time.
The decoction was centrifuged and filtered through a
membrane of 0.22 μm pore size before use. The yield of the
decoction obtained was 16.7%
+ 0.02% (w/w) with respect to
the starting material. For each experiment, 1%, 5%, and 10%
(v/v) concentrations of the decoction in appropriate media were
used.
Phytochemical analysis
Qualitative phytochemical analysis was carried out using
standard procedures
[6]
to determine the presence of
carbohydrates, glycosides, proteins, amino acids, phytosterols,
saponins, flavonoids, alkaloids, and tannins.
Microorganisms used
E. coli B170, E. coli B 831-2, E. coli TX1 (all obtained from
Centre for Disease Control, Atlanta, USA), E. coli E134 (kindly
provided by Dr. J. Nataro, Veterans Affairs Medical Centre,
Maryland, USA), V. cholerae El Tor (kindly provided by Dr. S.
Calderwood, Massachusettes General Hospital, Boston, USA),
S. flexneri M9OT (kindly provided by Dr. P. Sansonetti, Institut
Pasteur, France), G. lamblia P1 (kindly provided by Dr. P. Das,
National Institute of Cholera and Enteric Diseases, Kolkata,
India), and rotavirus SA-11 (kindly provided by Dr. S. Kelkar,
National Institute of Virology, Pune, India) were used as
representative organisms.
Antimicrobial activity
The protocol followed for assaying the antibacterial activity
of the decoction was the agar dilution method.
[7]
A log phase
culture of each bacterium grown in nutrient broth was plated
Antidiarrhoeal activity of Dalbergia sissoo
onto nutrient agar (NA) without (control) and with different
dilutions of the decoction and incubated at 37
o
C for 18-20 h.
Thereafter, the viability of individual strain was graded on a
scale of 0 (no growth) to +4 (control) depending on the extent
of the growth. Gentamicin (100 μg/ml) was used as the
antibiotic control.
The antiprotozoal activity was assayed by incubating a 24
h culture of G. lamblia trophozoites without (control) and with
different dilutions of the decoction for 24 h. The number of
viable trophozoites was counted in a haemocytometer with
trypan blue.
[8]
The antigiardial drug metronidazole (100 μg/
ml) was used as the positive control.
The antiviral activity was determined by assaying the entry
and the subsequent survival of rotavirus in MA-104 cells by
the neutral red uptake assay.
[9]
Briefly, a 72 h culture of MA-
104 cells was infected with rotavirus and incubated without
(control) and with different dilutions of the decoction for 90
min. The culture was further incubated for 72 h after removal
of the decoction and the unabsorbed virus. Thereafter, the cells
were incubated with neutral red dye for 30 min. The
intracellular dye was released with 1:1 solution of 100 mM
acetic acid and ethanol. The released dye was measured at
540 nm (reference 630 nm) in an ELISA plate reader.
Effect on toxins
The E. coli labile toxin (LT), an enterotoxin, was obtained
from E. coli B831-2 by lysing the bacterial cells with polymyxin
B sulphate.
[10], [11]
Cholera toxin (CT), an exotoxin, was obtained
as a culture supernatant of V. cholerae. LT and CT were assayed
by a modification of the ganglioside monosialic acid enzyme
linked immunosorbent assay (GM1-ELISA).
[11]
Briefly, the toxins
were added to ELISA plates pre-coated with the receptor GM1.
Anticholera toxin and peroxidase labeled swine antirabbit Ig
were used as primary and secondary antibodies, respectively.
The colour developed was read at 492 nm in an ELISA reader.
The assays were based on two protocols:
i) Preincubation: Bacterial strains were grown without
(control) and with different dilutions of the decoction in
casein hydrolysate yeast extract broth (CAYE), and the LT/
CT produced by the respective bacterial strains was
assayed using the GM1-ELISA.
ii) Competitive: To detect if the plant extract competes for
binding with GM1, the GM1-ELISA was done wherein the
toxin was assayed without (control) and with different
dilutions of the decoction.
Stable toxin (ST), which is an exotoxin, obtained as a culture
supernatant of E. coli TX1 was assayed by the method originally
described by Gianella.
[12]
Briefly, the toxin was inoculated intra-
gastrically into 2-3 day-old Swiss albino suckling mice.
Following an incubation of 3 h at room temperature, the pups
were sacrificed and the ratio of gut weight to that of the
remaining carcass weight was calculated. Ratio of > 0.083
was considered as positive.
The assays were based on two protocols:
i) Preincubation: ST obtained as supernatant of the bacterial
culture grown without (control) and with different dilutions
of the decoction in CAYE was assayed by intra-gastric
inoculation of suckling mice.
Indian J Pharmacol | April 2006 | Vol 38 | Issue 2 | 120-4
121
Brijesh et al.
ii) Competitive: ST was intra-gastrically inoculated in the
suckling mice without (control) and with different dilutions
of the decoction.
Effect on colonisation to HEp-2 cell line
The effect of the decoction on the adherence of E. coli strain
B170 to epithelial cells was assayed by a method described
earlier.
[13]
Briefly, a 48 h culture of HEp-2 cells was infected
with a log phase culture (5x10
7
cells/ml) of E. coli B170 grown
in brain heart infusion broth (BHI) and incubated for 3 h. Non-
adherent bacteria were washed off and the microcolony
formation was observed by toluidine blue staining (0.1% w/
v). HEp-2 cells having
> 5 adherent E. coli cells were counted.
The effect of the decoction on invasion by E. coli E134 and
S. flexneri was studied by a method described by Vesikari et
al.
[14]
Briefly, a 48 h culture of HEp-2 cells grown in a 24-well
tissue culture plate was infected with log phase culture (10
8
cells/ml) of the bacterial grown in BHI and incubated for 2 h.
The culture was further incubated with gentamicin (100 μg/
ml) for 3 h to kill the uninvaded bacteria. The epithelial cells
were then lysed by cold shock, and the released bacteria were
counted by plating on NA.
The assays were based on two protocols:
i) Preincubation: HEp-2 cells were incubated without (control)
and with different dilutions of the decoction in DMEM for
18–24 h prior to incubation, with the respective bacterial
strain.
ii) Competitive: Bacterial strain and HEp-2 cells were
simultaneously incubated in DMEM without (control) and
with different dilutions of the decoction.
Statistical analysis
Each assay was performed three times and the results were
expressed as their mean+SD. The differences in the mean
values of the treated groups were analysed by analysis of
variance (ANOVA). Furthermore, the significance of the
difference between the means of the test and the control
observations was established by Dunnett’s post-test.
Statistical analyses were performed using the programme
Prism 4.0 (GraphPad, Inc.). P<0.05 was considered to be
statistically significant
Table 1.
Results
Phytochemistry
The decoction contained carbohydrates, proteins,
flavonoids, and tannins. Phytosterols, glycosides, saponins,
and alkaloids were absent.
Antimicrobial activity
The decoction exhibited no antibacterial activity. Similarly,
there was no effect on the viability of G. lamblia trophozoites
or on the entry of rotavirus into MA-104 cells.
Effect on toxins
The decoction inhibited the production of CT [Table 1], while
it increased the production of LT. Binding of both LT and CT to
the GM1 receptor was reduced. [Table 1] Neither the production
nor the action of ST was affected.
Effect on colonisation
The adherence of E. coli B170 to the epithelial cells was
reduced when the HEp-2 cells were incubated with the
decoction prior to infection. [Table 2] The adherence was also
reduced when the cells were incubated with the decoction,
simultaneously with the infection. Similarly, the decoction
significantly reduced the invasion [Table 2] of both E. coli E134
and S. flexneri to the epithelial cells in both the protocols.
Discussion
According to the World Health Report 2004, diarrhoea is
the cause of 3.3% of all deaths.
[2]
The past decade has
witnessed several attempts towards the management of
diarrhoea. These include improved formulations of oral
rehydration solution (ORS) and the development of a feasible
vaccine. Although ORS has contributed to reduction in
diarrhoeal mortality rates, it is often less efficient in high stool
output state. In addition, response to vaccines in developing
countries is not encouraging.
[15]
With the threat of drug
resistance, a definite niche exists for the development of an
alternative approach to treat infectious diarrhoea. Medicinal
plants can fill this niche. This study was an attempt to explore
the antidiarrhoeal activity of crude decoction of D. sissoo
leaves.
Effect of a decoction of Dalbergia sissoo leaves on E. coli labile toxin and cholera toxin.
% Reduction in optical density
D. sissoo extract Cholera toxin assay (V. cholerae) Labile toxin assay (E. coli B-831-2)
Competitive
1
Pre- incubation
2
Competitive
1
Pre- incubation
2
1% Decoction 8.16 + 6. 42 3.41 + 13.05 11.70 + 2.21 -30.39 + 20.52
†
5% Decoction 8.01 + 5.17 22.32 + 12.07* 22.45 + 6.61** -58.26 + 34.77*
†
10% Decoction 16.99 + 8.60** 28.73 + 12.09** 28.21 + 4.71** -104.98 + 17.73**
†
One-way F 4.075 6.581 26.27 12.28
ANOVA df 2,6 2,6 2,6 2,6
P 0.0498 0.0149 0.0002 0.0023
Values are mean+SD (from three individual experiments), of percentage reduction in optical density compared with respective controls (100%).
1
Incubation of the toxin onto
GM1 receptor carried out in presence of the decoction.
2
Toxin produced by bacteria grown in the presence of decoction. *P < 0.05; **P < 0.01 by Dunnett’s post-test.
†
The
negative values indicate that there was an increase in the production of labile toxin.
Indian J Pharmacol | April 2006 | Vol 38 | Issue 2 | 120-4
122
Antidiarrhoeal activity of Dalbergia sissoo
Table 2
Effect of a decoction of Dalbergia sissoo leaves on bacterial colonisation to HEp-2 cells.
% Reduction in colonization
a
Dalbergia sissoo Adherence assay (E. coli B170) Invasion assay (E. coli E134) Invasion assay (S. flexneri)
extract Competitive
1
Pre-incubation
2
Competitive
1
Pre-incubation
2
Competitive
1
Pre-incubation
2
1% Decoction 4.68+ 0.97 14.88+3.18** 26.29+22.53 43.95+13.98** 84.39+8.87** 62.97+13.84**
5% Decoction 20.51+ 1.93 100+0** 57.84+2.1** 75.50+19.27** 88.87+4.08** 79.52+19.97**
10% Decoction 74.62+22.03** 100+0** 62.74+16.52** 96.22+4.94** 79.23+1.23 ** 97.16+3.45**
One-way F 28.74 3435 13.15 35.61 221.3 35.68
ANOVA df 2,6 2,6 2,6 2,6 2,6 2,6
P 0.0001 <0.0001 0.0018 <0.0001 <0.0001 <0.0001
a
Values represent mean + SD (from three individual experiments), of percentage reduction in colonisation compared with respective controls (100%).
1
Infection of HEp-
2 cells carried out in presence of the decoction.
2
HEp-2 cells incubated with the decoction prior to the infection. *P < 0.05; **P < 0.01 by Dunnett’s post-test.
The decoction did not have antibacterial activity against
the strains tested nor did it have antigiardial or antirotaviral
activity. It was observed that although the decoction did not
arrest the growth of V. cholerae, it prevented the production
of CT indicating that the reduction in the production of CT was
metabolic and not due to reduction in bacterial counts. There
was a two-fold increase in the production of LT in the presence
of the decoction, but its binding to the receptor was reduced.
It is known that LT and CT are closely related structurally,
functionally, biologically, and immunogenically.
[16]
Therefore,
the reduction in binding of LT and CT to GM1 receptor implies
that the decoction may contain chemical(s) that either bind(s)
directly to the receptor or to the common antigenic moiety of
the toxins.
The decoction also affected colonisation. It inhibited the
adherence of E. coli B170 and invasion by E. coli E134 and S.
flexneri. The decrease in colonisation was observed in both
the protocols suggesting that D. sissoo modifies/affects
receptors on HEp-2 cells in a way that restricts bacterial
attachment and entry. This is especially true because the
decoction did not affect the morphology of the HEp-2 cells
and, as mentioned earlier, had no antibacterial activity.
The findings of the biological assays are indicative of the
selective antidiarrhoeal action of D. sissoo leaves. The results
suggest that the leaves may not be active against diarrhoea
induced by LT and ST or those caused by protozoa and virus.
However, it appears to be most efficacious against cholera
and diarrhoeal episodes caused by enteropathogenic and
enteroinvasive bacterial strains.
To conclude, this study besides describing the possible
mechanisms of antidiarrhoeal action of D. sissoo leaves also
highlights the necessity of including multiple parameters for
judging the efficacy of medicinal plants. Assaying bacterial
virulent features as a marker for demonstrating the
antidiarrhoeal efficacy of a plant, has been previously reported
by us using two indigenous plants viz. Cyperus rotundus
[17]
and Holarrhena antidysenterica.
[18]
This is especially important
in the absence of antimicrobial activity, which in most of the
studies reported earlier
[19]-[22]
has been considered the marker
for antidiarrhoeal activity.
Acknowledgments
We are thankful to Dr. P. D’Mello and Mr. Yogesh Palav, Department of Pharma-
cognosy, Principal, K. M. Kundanani, College of Pharmacy, Mumbai, India, for their
assistance in carrying out the phytochemical studies. We are also thankful to Dr. N.
F. Mistry, Foundation for Medical Research and Foundation for Research in Com-
munity Health (FRCH), for her critical suggestions and Mr. S. Jangam and Mr. A.
Gurav, the field workers of FRCH, for collection of plant material. This work has
been supported by the Department of Science and Technology, Ministry of Science
and Technology, Government of India through grant number 91283.
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PROFESSOR PREM CHAND DANDIYA ENDOWMENT TRUST
BEST PUBLICATION BIENNIAL
PRIZES AWARDS 2004-05
The Motan Devi Dandiya Prize in Pharmacy has been awarded to Dr. R.B. Umamaheshwari for her
work on “Receptor-mediated targeting of lipobeads bearing acetohydroxamic acid for eradication of
Helicobacter pylori” carried out at Department of Pharmaceutical Sciences, Dr HS Gaur University,
Sagar. The certificate of merit in this category has been recommended for Dr. Sushama Talegaonkar,
Lecturer, Department of Pharmaceutics, Faculty of Pharmacy, Jamia Hamdard, New Delhi.
The Chandra Kanta Dandiya Prize in Pharmacology has been awarded to Mr Jayesh B Majithiya
of Pharmacy Department, Faculty of Technology and Engineering, MS University, Baroda for his work
on “Effect of pioglitazone on L-NAME and streptozotocin induced hypertension and diabetic rats and
time dependent changes in antioxidant enzymes and vascular reactivity of aorta in streptozotocin induced
diabetic rats treated with curcumin”. The certificate of Merit in this category has been recommended for
Mr. Vijai Pal Singh, Research Associate, University Institute of Pharmaceutical Sciences, Panjab
University, Chandigarh.
The awards/prizes comprising of a Scroll of Recognition together with Rs.10,000/= each and Certificates
of Merit would be presented in a suitable scientific function/sent to the winners directly.
N.K. Gurbani
Jt. Secretary
Professor Prem Chand Dandiya Endowment Trust
Indian J Pharmacol | April 2006 | Vol 38 | Issue 2 | 120-4
124
