Original Article | J Adv Med Biomed Res. 2021; 29(137): 317-323
Journal of Advances in Medical and Biomedical Research | ISSN:2676-6264
Antimicrobial Effects of Aqueous and Hydro-Alcoholic Plantago psyllium leaf
extracts on the Experimental Infection of Helicobacter pylori in a Rat Model
Shima Keshavarzi1,2
, Masood Sepehrimanesh3*
6
Omid Koohi-Hosseinabadi
1.
2.
3.
4.
5.
6.
7.
, Zeynab Sardari
7
, Bahman Mirzaei4, 5
,
, Mohammad Mehdi Sajjadpur7
Dept. of Microbiology, Fars Sciences and Research Branch, Islamic Azad University, Shiraz, Iran.
Dept. of Microbiology, Shiraz Branch, Islamic Azad University, Shiraz Iran
Dept. of Biology, University of Louisiana at Lafayette, Louisiana, USA
Dept. of Medical Microbiology and Virology, Faculty of Medicine, Mazandaran University of Medical Science,
Sari, Iran
Dept. of Medical Microbiology and Virology, School of Medicine, Zanjan University of Medical Science, Zanjan,
Iran
Central Laboratory, Shiraz University of Medical Sciences, Shiraz, Iran
Gastroenterohepatology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
Article Info
ABSTRACT
10.30699/jambs.29.137.317
Received: 2020/12/06;
Accepted: 2021/03/04;
Published Online: 01 Aug 2021;
Use your device to scan and read the
article online
Corresponding Information:
Masood Sepehrimanesh,
Dept. of Biology, University of
Louisiana at Lafayette, Louisiana, USA
E-Mail:
sepehrimaneshmasood@gmail.com
Background & Objective: Plantago psyllium has long been utilised as a
medicinal agent worldwide. The current study aims to evaluate the in vivo
antimicrobial effects of aqueous P. psyllium and a hydro-alcoholic extract of P.
psyllium on Helicobacter pylori as well as the effects of these extracts on liver and
kidney in a rat model.
Materials & Methods: A total number of 50 female Sprague Dawley rats were
experimentally infected (Except for the negative control group). The rats were divided
into five groups of 10. The groups were treated by Aqueous and Hydro-Alcoholic P.
psyllium leaf extracts. Subsequently, H. pylori antigens which were present in the in rats’
stool were measured using a serological assay. To diagnose the pathogenicity of the
kidney and liver, blood samples which had been taken before and after treatment, were
tested for renal and hepatic enzymes by Analyzer Electrolyte and Sysmex KX-21N.
Results: Following the amoxicillin treatment, the levels of aqueous and hydroalcoholic extracts of the treated rats were compared with those of the control group,
and a significant difference was observed (P<0.05). Antigen decrease was observed
in all of the groups treated with amoxicillin (P=0.0004), aqueous, and hydro-alcoholic
extracts (P<0.05). Antigen decrease in the stool was observed in all groups, which
indicates that treatment with the herbal extract could affect the infected rats.
Conclusion: P. psyllium hydro-alcoholic extract can be applied as a selective
treatment for H. pylori infection. Hopefully, experiments suggested that the
mentioned extracts could positively affect the process of disease recovery.
Keywords: Aqueous and Hydro-Alcoholic extracts, Helicobacter pylori, Plantago
psyllium
Copyright © 2021, This is an original open-access article distributed under the terms of the Creative Commons Attribution-noncommercial 4.0 International License which permits
copy and redistribution of the material just in noncommercial usages with proper citation.
Introduction
Helicobacter pylori colonizes half of the world’s
population and contributes to gastritis and gastrointestinal
ulcer disease increasing the risk of malignant gastrointestinal cancer (1). The onset of gastric adenocarcinoma
occurs with the progression of chronic superficial gastritis
to chronic gastric atrophy. Furthermore, H. pylori is a risk
factor for gastric cancer (2). It is estimated that 14,500
patients (>65 age) pass away due to H. pylori infections
annually (2). Antibiotics such as clarithromycin, metronidazole, amoxicillin, and tetracycline are used to treat of H.
pylori infections. H. pylori resistance rate has been
Volume 29, November & December 2021
estimated to range from 15% to 78%. According to
previous reports, the antibiotic resistance of the mentioned
bacterium against amoxicillin and other antibiotics has
increased [4]. Multi-drug resistant (MDR) H. pylori
isolates were screened >75% in Iran (3). Plantago
psyllium is widely used as a traditional herbal medicine
and a functional food in Asian counties (4). Polysaccharide, the main biological active compartment in Plantago spp., has a variety of biological effects including
gastrointestinal functions and antioxidant, immunemodulatory, antitumor, and hypoglycemic activities. Variety
Journal of Advances in Medical and Biomedical Research
318 P. Psyllium in vivo antimicrobial effect against H. pylori
of biological and pharmacological functions of psyllium
macromolecules have been confirmed (4). P. psyllium can
be found in almost every region of the world and people
have used P. psyllium to treat gastric and peptic ulcers for
a very long time. This herb has had medicinal uses in
Iranian traditional medicine as well (5-7). P. psyllium
seeds contain 10% mucilage, which produces D-xylose,
arabinose, D-glucose, and D-galacturonic acid through
hydrolysis (8). In the United States, a medicine called
“Metamucil” is produced from the laxative, but
researchers suggest that P. psyllium is also effective in
reducing cholesterol and glucose levels (9). Anti-bacterial
properties of herbs against H. pylori infection were
indicated in some published studies (10). Although there
are some reports about P. psyllium anti-bacterial properties (11), no study has investigated H. pylori infections.
Therefore, investigation of the antimicrobial effects of
aqueous and hydroalcoholic extracts of P. psyllium on the
infected experimental rat groups, is the main purpose of
the current study.
Taking Care of Animals
Fifty female rats of Sorague Dawly with a weight range
of 200±20 g were randomly divided into five groups. Rats
were kept in standard conditions for relative temperature
of 22±2% and received water and food every day.
Consumption doses were calculated based on previous
studies and advice of traditional medicine experts (4).
Materials and Methods
G-1: Negative control group, which was not subject to
infection and treatment at all.
Preparation of Aqueous and Hydro-alcoholic
Extracts of P. psyllium
Extraction was carried out in the faculty of pharmacy
under the supervision of experts as follows: fresh P.
psyllium was provided from Shiraz, a city in south-central
Iran. The species were matched with the German Digital
Herbarium in the Faculty of Pharmacy at Shiraz University of Medical Sciences. It was found that the species had
a herbarium number as B-W0298230 (9). To prepare the
aqueous and hydro-alcoholic extracts of P. psyllium, the
plants were dried at room temperature for five days and
were then powdered. Using the percolation method, 100
g of powdered P. psyllium leaf was poured into the
percolator and soaked in distilled water for 24 h. Another
100 g of powdered P. psyllium was soaked in another
percolator device with one litre of 70% ethanol for 72 h.
After filtering and evaporation, the obtained gelatinous
extracts were reduced under pressure in the rotary device
and were finally prepared as powder (12, 13).
G- 2: Amoxicillin antibiotic group, in which infection
was treated with 500 mg of amoxicillin.
Preparation and Culture of Bacteria
Gastric biopsy samples were taken by endoscopy from
patients who referred to Namazi hospital, Shiraz. For early
isolation of bacteria, agar enriched with yeast extract of
Columbia culture medium (Merck, Germany) was enriched with 10% defibrinated horse blood, 10 mg/L
vancomycin, 10 mg/L amphotericin B, 5 mg/L cefsulodin,
and 5 mg/L trimethoprim and incubated at 37°C (14).
According to previously published research, Urease test
was performed on biopsy samples, which were examined
for the presence or absence of H. pylori (15).
Confirmation of H. pylori Isolates
According to the previously published research, the
isolated strains were precisely reconfirmed taking advantage of traditional biochemical tests including gram staining, urease activity, oxidase, and catalase enzymes
production (14).
Volume 29, November & December 2021
Infection and Treatment
All groups, except for the negative control, received
(orally) 0.5 ml of a suspension containing 2×107 colonyforming unit per millilitre (CFU/ml) of H. pylori on
average every day in the morning for 7 days (4, 16). After
48 weeks of infections, groups were treated for 26 days.
P. psyllium extracts were performed as single dosage in
300mg final concentration for experimented groups.
Some study findings related to the herbal extract in
diarrhea showed that higher doses (500 and 1,000 mg/kg),
had antisecretory and antidiarrheal activity (17).
The experimental groups were as follows:
G- 3: Aquinas extract group, in which, after infecting,
the rats were treated with aqueous extract of P. psyllium
at a concentration of 300 mg/kg of body weight.
G- 4: Hydro-alcoholic extract group, in which, after
infecting, the rats were treated with hydro-alcoholic
extract of P. psyllium at a concentration of 300 mg/kg of
body weight. No cosolvents or surfactant were added to
the extract.
G- 5: Positive control group, in which rats were not
treated after infecting.
Biochemical Analysis of Rats’ Blood in Each
Group
Sampling (blood and stool) from the treated groups was
immediately performed eight weeks after infections. Sera
were tested in terms of renal and hepatic functions by
assessing aspartate aminotransferase (AST), alanine
aminotransferase (ALT), alkaline phosphatase (ALP),
total protein (TP), creatinine, and blood urea nitrogen
(BUN) according to the previously published research
(18) using an Analyzer Electrolyte, Hitachi 911 (Roche
Company, Switzerland) with Pars-Azmoon Commercial
Kits (Pars-Azmoon Laboratories LTD, Tehran, Iran) and
Sysmex KX-21N (Sysmex Corporation, Japan) according
to the manufacture’s manual (Fig. 2, 3). Bouin solution,
ethanol, and chloroform were obtained from Sigma-Aldrich Company, USA.
Enzyme-linked Immunosorbent Assay (ELISA)
ELISA was done taking advantage of polyclonal antibody-based Premier Platinum HpSA test, later HpSA
(Meridian Inc., Cincinnati, USA) was performed based on
the manufacturer’s instructions.
Journal of Advances in Medical and Biomedical Research
Shima Keshavarzi et al. 319
Qualitative ELISA was to be performed immediately
before and after the treatment, stool sampling was
performed for the experimental groups to detect H. pylori
antigens. Briefly, following the kit manufacturer’s recommended procedure, the plates were washed with
washing buffer [0.05 % (v/v) Tween 20 in phosphate
buffer saline (PBS)] twice. The Plates were incubated for
2 h at 37°C. Blocking was carried out using a PBS/Tween
20 solution containing 5% bovine serum albumin (BSA)
as a blocking buffer. After filing blocking and washing,
50 µl of homogenate rat stool samples were added to the
wells in duplicate. The plates were incubated for 1 h at
37°C, washed three times, and incubated with HRPconjugated anti-mouse immunoglobulin (IgG) (Sigma,
USA), which was diluted to 1:10,000 (as a secondary
antibody) at 37°C for 2 h. The plates were then washed as
described above, and the enzymatic activity was measured subsequent to adding 100 µl of tetramethylbenzidine
(TMB) substrate. After 30 min of subjoining of 100 µl 2
N H2SO4, the reaction was stopped. Finally, the optical
density (OD) of each well was determined as 405
nanometres, taking advantage of an ELISA microplate
reader (Anthos 2020, United Kingdom). Detailed data are
given in Figure 1A.
Ethical Code
All animal experiments were done in compliance with
the enlarged ethical statement and approved by the ethics
committee of Shiraz University of Medical Sciences. All
tests were performed complying the enlarged ethical
(Human and Animal) statement (95-01-13-11069). The
ethics committee approved both the human and the animal
experimentation.
Results
Extraction was done based on previously published
work using the species that had a herbarium number of B-
W0298230. A dried extract was then used to prepare the
aqueous and hydro-alcoholic extracts (9). The
experimental rat groups were infected, following a
previously published procedure (4, 16).
Antibody-mediated ELISA was used to determine the
H. pylori antigen in the homogenate rats’ stool. Following
the amoxicillin treatment, the levels of aqueous and
hydro-alcoholic extracts of the treated rats were compared
with those of the control group, and a significant difference was observed (P<0.05). A decrease in antigens was
observed for all tested groups treated with amoxicillin
(P=0.0004), aqueous, and hydro-alcoholic extracts
(P<0.05) (Fig. 1A). After two weeks of treatment with
medicine extracts, all groups showed a describing amount
of H. pylori antigen in their stool, thus indicated the
efficacy of the medicines.
Additionally, in the liver function test (LFT) assay, a
significant difference (especially in aquatic extract) was
observed in the levels of liver (AST and ALP) and renal
damage markers, including BUN and creatinine (P<0.05).
Significant differences were also seen in the levels of liver
enzymes including ALT (P=0.00001), AST (P=0.00001),
ALP (P=0.0005), and total protein (P<0.00001) content
of the serum before and after treatment. This amount was
also significant when different treated groups were
compared with each other after treatment with medicine
extracts. By comparing the amounts of liver and renal
indicators among the treated groups, it was found that the
amounts of ALP (as an example) to amoxicillin/aqueous,
amoxicillin/hydro-alcoholic, and hydro-alcoholic/aqueous were significant (P<0.05) after treatment. A statistical analysis showed that blood samples especially to
aquatic extract were significantly different in terms of
factors that affect the liver and kidney. Furthermore, all of
the findings were statistically significant when compared
with positive control after treatment (Figs. 1, 2, and 3).
Figure 1. Difference in fecal homogeneity antigen A) and Total protein in tested groups B). The error bar is representative
of the mean±sd (n=3).
Volume 29 November & December 2021
Journal of Advances in Medical and Biomedical Research
320 P. Psyllium in vivo antimicrobial effect against H. pylori
Figure 2. Biochemical analysis of liver enzymes (ALP, and AST) to tested sera in treated rat groups. A) The amount of ALP
in experimental groups B) The differences of AST in studied groups. The error bar is representative of the mean±sd (n=3).
Figure 3. Analysis of biochemical factors in treated and untreated rat sera, A) the creatinine level in various groups, and
B) the BUN differences in studied. The error bar is representative of the mean±sd (n=3).
Discussion
Antibiotics are often used to treat Helicobacter
infections, and common antibiotics cause severe damage to the normal flora of the digestive system, which,
in the long term, causes malnutrition and complicated
diseases (19). P. psyllium is a valuable medicinal plant
that researchers have always been interested in knowing more about. Numerous studies have been performed on the effects of this plant and its therapeutic role
in constipation, diarrhea, ulcerative colitis, irritable
bowel syndrome, colon cancer, diabetes, and hypercholesterolemia (20-22).
Considering the long history of the effects of P.
psyllium on treating microbial diseases in humans and
animals, in the current research, the therapeutic features of aqueous and hydro-alcoholic extracts of P.
psyllium were investigated in rat models. The findings
Volume 29, November & December 2021
showed that both extracts had significant therapeutic
effects, and additional experiments demonstrated that
these extracts have minor adverse effects on renal and
hepatic functions. Given the emergence of MDR H.
pylori isolates and the adverse effect of the mentioned
drug of choice on liver and kidney functions, it seems
appropriate to consider the use of herbal and natural
ingredients to treat H. pylori-associated infections (3).
The protective effect of pectic polysaccharide in P.
psyllium against systemic Streptococcus infections has
been shown in experimental rats. This protective effect
appeared to be due to the stimulation of the immune
system. Other antibacterial and anti-Candida effects of
pectic polysaccharide in P. psyllium were confirmed in
another review (23). In a study investigating the
antimicrobial activity of nanoparticles produced in the
Journal of Advances in Medical and Biomedical Research
Shima Keshavarzi et al. 321
examined P. psyllium, findings indicated that the
highest and the lowest concentrations of inhibitors in
Staphylococcus aureus were 100 mg/ml and 12.5
mg/ml, respectively. These results showed that P.
psyllium has good antimicrobial functioning in the
treatment of many common antibiotic-resistant infections (24). In a study conducted by Taheri et al., on the
effects of hydro-alcoholic extracts of P. psyllium on S.
aureus, the researchers found that these extracts had a
significant effect on S. aureus bacteria in vitro (25). In
the present study, the levels of fecal antigens and
antibodies against H. pylori were reduced in all
samples. This was also observed in Salmonella typhimurium bacteria (11). At last, although the mentioned
herbal extract is suitable for H. pylori treatment,
according to the obtained results especially in aquatic
extract, this cocktail has an adverse effect on liver and
renal functions compared to the hydroalcoholic extract.
Conclusion
Antimicrobial resistant patterns of human pathogens
are essential problems, resulting in the need for novel
antimicrobial resources such as plants. This study
confirmed that Aqueous and Hydro-Alcoholic P.
psyllium leaf extracts could be considered as alternative choice treatments due to the lack of renal and
hepatic side effects and their proper antimicrobial
effects in experimental H. pylori infection in a rat
model. However, further research on more samples and
human models are recommended.
Limitations
OD: optical density
BSA: bovine serum albumin
IgG: immunoglobulin G
TMB: tetramethylbenzidine
PBS: phosphate buffer saline
ANOVA: analysis of variance
LFT: liver function test
Declarations
Ethics approval and consent to participate: In this
study, all ethics including Ethics and Consent to
participate have been collected in the research. Informed
consent, (written) was obtained from all participants for
the 'Gastric biopsy samples'. Inbred Sprague Dawley rats
were purchased from the Research Institution of Pasteur,
Karaj, Iran. They were housed in standard cages (at 2325°C and 60%–70% humidity under a 12 h light/dark
cycle) with free access to standard diet and water, one
week before the experiment. Euthanasia was performed
using 2-5% halogenated ether which is an inhalant
anesthetic, according to Evaluation of the Aesthetics of
Physical Methods of Euthanasia of Anesthetized Rats,
2011 protocol.
In this survey, Ethics and Consent to participate from
their parents have been collected. All analyses were
performed using multiple-group analysis of variance
(ANOVA) by Graph Pad software (Chicago, IL, USA).
P-value≤0.05 was regarded as statistically significant.
Consent for publication
In the current study, herbal antibacterial effects were
not measured in bacterial culture media such as agar well
diffusion. Moreover, H. pylori was not measured in the
stool samples before and after treatment because of
financial restrictions. Therefore, more studies are needed
to make a precise evaluation of the bactericidal effects
of the herbal extract on H. pylori.
Competing Interests
Abbreviations
Authors' contributions
H. pylori: Helicobacter pylori
P. psyllium: Plantago Psyllium
MDR: multi-drug resistant
CFU/ml: colony-forming unit per millilitre
AST: aspartate aminotransferase
ALT: alanine aminotransferase
ALP: alkaline phosphatase
TP: total protein
BUN: blood urea nitrogen
ELISA: Enzyme-linked immunosorbent assay
Volume 29 November & December 2021
Not applicable
The authors declare no competing interests.
All authors have read and approved the
manuscript. Contributions of the authors in this study
were as follow:
S K: Performing laboratory tests
M S M: Designing the study, and writing the
manuscript
B M: Interpretation of results and rewriting the
manuscript
O K H A: Sampling
Z S: Performing laboratory tests
M M S: Performing laboratory tests
Journal of Advances in Medical and Biomedical Research
322 P. Psyllium in vivo antimicrobial effect against H. pylori
Funding
8.
Ladjevardi ZS, Gharibzahedi SMT, Mousavi M.
Development of a stable low-fat yogurt gel using
functionality of psyllium (Plantago ovata Forsk)
husk
gum.
Carbohydrate
Polymers.
2015;125:272-80.
[DOI:10.1016/j.carbpol.2015.02.051]
9.
Abou Azar S, Wehbe MR, Jamali S, Hallal A.
Small bowel obstruction secondary to a
Metamucil bezoar: Case report and review of the
literature. Case Rep Surg. 2017;2017: 2702896.
[DOI:10.1155/2017/2702896]
Not applicable.
Acknowledgments
The authors wish to express gratitude to their
colleagues in Shiraz University of Medical Sciences,
Zanjan University of medical Sciences, and Namazi
hospital in Shiraz province, Iran.
Conflict of Interest
The authors announce that they have no conflict of
interest.
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How to Cite This Article:
Keshavarzi S, Sepehrimanesh M, Mirzaei B, Kuhi Hossein Abadi O, Sardari Z, Sajjadpur M M. Antimicrobial
Effects of Aqueous and Hydro-Alcoholic Plantago psyllium leaf extracts on the Experimental Infection of
Helicobacter pylori in a Rat Model. J Adv Med Biomed Res. 2021; 29 (137): 317-323
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