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196 Saeideh Momtaz etal.
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Table 5.2. In vitro studies on medicinal plants claimed to be effective in IBD in TPM.
Study
Langmead etal.
(2002)
Hage-Sleiman
etal. (2011)
Bonaterra etal.
(2020)
Weber etal.
(2020)
Wei etal. (2015) Cuminum cyminum Essential oil Inhibition of LOX, iNOS, COX-2, IL-1,
Tabarsa etal.
(2020)
Wu etal. (2018) Malus spp. Proanthocyanidins ↓ Oxidative stress; ↑ SOD, HO-1, CAT,
likely present in the colonic lumen; 1 in 100
dilution) significantly decreased chemiluminescence in inflamed colorectal biopsies
(Langmead etal., 2002). In another study,
co-administration of fenugreek seeds (as
symbiotic) and Lactobacillus acidophilus (as
prebiotic) ameliorated colonic inflammation in rats infected with Escherichia coli via
improvement of intestinal mucosa adaptive
immunity. Macroscopic and microscopic
evaluation of duodenum revealed an improvement in intestinal lymphoid tissues, as
well as increases in butyric acid production, goblet cell mucin secretion, and the
immunoglobulin IgA from plasma cells
(Bakheet, 2020).
Plant Part
Trigonella foenum-
graecum
Althea officinalis Root Anti-inflammatory, immunostimulant
Althea officinalis Root Inhibition of LPS-induced release of
Combination of myrrh,
coffee charcoal,
and chamomile
Cuminum cyminum Water-soluble
– ↓ Chemiluminescence in inflamed
Flower ↓ Release of inflammatory mediators;
polysaccharides
Result
colorectal biopsies; antioxidant
activity
TNF-α and IL-6 in macrophages;
antioxidative and anti-inflammatory
effects
preserves barrier function of
endothelial cells; modulates cytokine/
chemokine signaling and
inflammation
and IL-6; phosphorylation of ERK and
JNK; transcriptional activation of
NF-κB
Stimulation of pro-inflammatory cytokine
production; activation of NF-κB and
MAPK signaling pathways
and GSH-Px mRNA expression;
downregulation of inflammatory
markers
such as vitamin E (Kaithwas et al., 2011;
Kaithwas and Majumdar, 2013; Rafieian-Kopaei et al., 2017). A recent study reported
that daily gavage with flaxseed oil at a dose
range of 400 to 1600mg/kg b.w. for 6 weeks
improved colonic indices of colitis and alleviated DAI and colon cell damage in DSS-induced UC in rats. Linum usitatissimum oil
consumption caused a significant reduction
in colon inflammation and oxidative condition through increase in GSH, CAT, and SOD,
as well as decrease in MDA and MPO, and
IL-6 and monocyte chemoattractant protein-1 (MCP-1) levels. Flaxseed oil enhanced
microbiota diversity and restored cecal
microbiota dysbiosis in DSS-induced colitis
(Zhou etal., 2020). In Palla etal.’s study, various concentrations of the hydromethanolic
Linum usitatissimum L.
extract of flaxseed were tested against acetic
acid-induced colitis in mice. The plant at 300
Linseed or flaxseed is a rich source of useful
fatty acids and unsaturated fatty acids such
as n-6/n-3, α-linoleic acid, lignans, dietary
and protein fiber, minerals, and vitamins
and 500 mg/kg b.w. improved the severity
of colitis, DAI, macroscopic and histologic
damage scores. Flaxseed supplementation
reduced the activities of MPO and MDA,
Table 5.3. In vivo studies on medicinal plants claimed to be effective in IBD in TPM.
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Study
Liu (2019) DSS-induced UC Rat Trigonella foenum-
Fathima etal. (2021) Acetic acid-induced UC Rat Trigonella foenum-
Bakheet (2020) Colonic inflammation,
Zhou etal. (2020) DSS-induced colitis Rat Linum usitatissimumSeed Enhancement of microbiota diversity, restoration of
Palla etal. (2016) Acetic acid-induced colitis BALB/c mice Linum usitatissimumSeed ↓ MPO and MDA; ↑ SOD, GPx, CAT, and total
Silva (2016) TNBS-induced colitis BALB/c mice Linum usitatissimumSeed Attenuation of IBD; ↓ inflammatory mediators
Rahimi etal. (2013) TNBS-induced UC Rat Linum usitatissimumSeed ↓ Colonic histopathologic and macroscopic scores
Al-Hussaini etal. (2012) Acetic acid–ethanol-
Masoumi-Ardakani etal.
(2014)
Hartmann etal. (2012) Acetic-acid-induced colitis Rat Boswellia serrata – ↑ Anal sphincter pressure; improvement of
Hartmann etal. (2014) Acetic acid-induced acute
Anthoni etal. (2006) DSS-induced colitis Mouse Boswellia serrata sAKBA ↓ DSS-induced P-selectin-mediated recruitment of
Kiela etal. (2005) DSS- or TNBS-induced
Reddy etal. (2014) DSS-induced colitis Rat Lepidium sativum Seed oil ↓ Intestinal levels of MPO, leukotriene B4, MDA,
Model Species Plant Part
Seed ↓ Colon inflammation, TNF-α, IL-1β, and IL-6;
graecum
graecum
Rat Trigonella foenum-
infection with Escherichia
coli
induced UC
Acetic acid-induced colitis Rat Matricaria
colitis
colitis
Rabbit Matricaria
– Boswellia serrata – ↓ LPO and expression lev el of NO and iNOS;
Mouse Boswellia serrata Boswellia ↑ Histopathologic scoring criteria; exacerbates
graecum
chamomilla
chamomilla
Seed ↑ Total protein, ↓ oxidative stress-relat ed enzymes;
Seed Improvement in intestinal lymphoid tissues;
Flower ↓ Serum electrolytes (Na and K); ↑ total leukocyte
Flower ↓ Severe macroscopic and histopathologic colon
Results
↑ IL-10; preserves colon mucin, ↑ colonic neutral
mucin, ↓ acidic m ucin; ↑ colon length, ↑ colon
weight/length ratio
antioxidant and anti-inflammatory effects against
IBD
↑ butyric acid production, goblet cell mucin
secretion, IgA from plasma cells
cecal microbiota dysbiosis in colitis
glutathione
of colitis
count, lymphocyte count, erythrocyte count, and
blood hemoglobin percentage
injury indices
intestinal mucosal injury
improvement of colon tissue injury and anal
sphincter pressure
inflammatory cells
mucosal ulcerations, necrosis, and edema
NO, TNF-α, and IL-1β
Continued
Evidence-Based Review of Medicinal Plant 197
Table 5.3. Continued.
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198
Study
Hamedi etal. (2016) Acetic acid-induced colitis Rat Malva sylvestris Aerial parts ↓ Inflammation; high content of polyphenols and
Mencarelli etal. (2009) T-cell-induced colitis Mouse Commiphora mukul Gum resin ↓ Colon inflammation, mediators of adaptive
Latifi etal. (2015) Acetic acid-induced UC Rat Rosa × damascena Volatile oil ↓ Histologic and macroscopic indices of colitis and
Tafti etal. (2017)
Khosropour etal.
(2019)
Jabri etal. (2015) Acetic acid-induced UC Rat Myrtus communis Seed ↓ All histologic alterations
Joo etal. (2009) DSS-induced UC Mouse Solanum nigrum Fruit ↓ NO production, LDH release, and MDA formation
El-Meligy etal. (2015) Acetic acid-induced colitis Rat Solanum nigrum Extract Effective against UC
Heidari etal. (2016) Acetic acid-induced colitis Rat Coriandrum sativumEssential oil,
Jagtap etal. (2004) Acetic acid-induced colitis Mouse Combination of
Solanki etal. (2011) N-Ethylmaleimide-induced
Hong etal. (2009) LPS-induced inflammation Mouse Medicago sativa Sprout ethyl
Model Species Plant Part
Acetic acid-induced UC Rat
Acetic acid-induced UC Rat Myrtus communis Essential oil ↓ Colonic inflammation and tissue edema, ulcer
Rat Quercus infectoria – ↓ Physical and oxidative stress parameters in colitis
experimental colitis
Myrtus communis Leaf ↓ Colonic MDA level, MPO activity. and luminol,
hydroalcoholic
extract of the
fruits
– Effective against UC and CD
bilwa (Aegle
marmelos),
dhanyak
(Coriandrum
sativum), musta
(Cyperus
rotundus), and
vala (Vetiveria
zinzanioides)
acetate extract
Results
mucilaginous polysaccharides
immunity, DAI
MPO activity
lucigenin, NO, and peroxynitrite
chemiluminescence values
index, total colitis index, and MPO activity
↓ Macroscopic and histopathologic scores, total
colitis index, MPO activity
tissue, ↓ histologic scoring like colon mucosal
damage index and DAI
↓ TNF-α, IL-6, and IL-1β levels
Saeideh Momtaz etal.
Rashidian etal. (2021) Acetic acid-induced colitis Rat Bunium persicum Essential oil ↓ Macroscopic and microscopic indices of colitis
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and MPO and TNF-α activities; suppression of
phosphorylated NF-κB protein expression
Minaiyan etal. (2012) TNBS-induced UC Rat Cydonia oblonga Juice and
hydroalcoholic
Rodríguez-Cabezas
etal. (2002)
Rodríguez-Cabezas
etal. (2003)
Larrosa etal. (2010)
Singh etal. (2009) DSS-induced colonic
Darji etal. (2010) DNBS-induced colitis Rat Punicum granatum Fruit Attenuates oxidative stress parameters, i.e., MDA,
Riaz etal. (2017) TNBS model of colitis Rat Punicum granatum Fruit ↓ Serum MPO, GSH, ALP, fibrinogen, and CRP
Shah etal. (2016) DNBS-induced colitis Punicum granatum Juice (purified
Kim etal. (2017) DSS-induced colitis Rat Punicum granatum Beverage ↓ Inflammation and ulceration in intestinal colitis
Parisio etal. (2020) DNBS-induced abdominal
Kim etal. (2014) DSS-induced colitis Rat Mango and
Kim etal. (2016) DSS-induced colitis Rat Mango and
TNBS-induced colitis Rat Plantago ovata Fiber-supplemented
TNBS-induced colitis Transgenic rats Plantago ovata Fiber-supplemented
DSS-induced colitis Rat Punicum granatum
Mice Punicum granatum Flower and ellagic
inflammation
Rat Punicum granatum – Prevention of development of abdominal pain
pain
Punicum
granatum
Punicum
granatum
extract
diet (5% w/w
P. ovata seeds)
diet (5% w/w
P. ovata seeds)
UROA ↓ Inflammation markers; modulates the gut
acid-rich fraction
punicalagin)
Juice Mango polyphenols inhibit the IGF-1R/AkT/mTOR
Juice Pomegranate polyphenols downregulate the mTOR
↓ Extent of UC lesions, extravasation, and
inflammation in damaged colon tissue
↓ Intestinal inflammation, TNF-α level, and NOS
activity in the large intestine
Improvement of the intestinal cytoarchitecture, ↓
pro- or inflammatory markers
microbiota
↓ Histamine, MPO, and oxidative stress
NO, MPO levels, increase in SOD activity
levels
↓ Disease extent and severity; represses gene
expression of TNF-α, IL-18, and IL-1β through
decrease of NF-κβ mRNA level
pathway; pomegranate polyphenols
downregulate the mTOR downstream pathway
through reductions of ERK1/2
downstream pathway through reductions in
ERK1/2; decrease of p70S6K and RPS6,
Rps6ka2, Map2k2, and Mapk1 mRNA
Continued
Evidence-Based Review of Medicinal Plant
199
200 Saeideh Momtaz etal.
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Study
Yoshioka etal. (2008) DSS or oxazolone-induced
Skyberg etal. (2011) DSS model of UC Mouse Malus spp. Polyphenols extract ↓ Pro-inflammatory cytokine expression
Lee etal. (2011) TNBS-induced colitis Rat Malus spp. Flavonoid phloretin ↓ Colon inflammation and body weight loss;
Liu etal. (2021) DSS-induced UC Mouse Malus spp. Polyphenols
Yeganeh etal. (2018) DSS-induced UC Mouse Malus spp. Peel polyphenols ↓ Mitochondrial dysfunction related to size, density,
D’Argenio etal. (2012) TNBS-induced colitis Rat Malus spp. Polyphenols ↓ Transcription and protein levels of COX-2, TNF-α,
Pastrelo etal. (2017) Acetic acid-induced colitis Rat Malus spp. – Suppression of iNOS gene expression; ↑
Zhou and Mineshita
(2000)
Minaiyan etal. (2011) Acetic acid-induced colitis Rat Berberis vulgaris Fruit Protection against colonic damage; ↓ ulcer index
Tanideh etal. (2014) Acetic acid- induced colitis Rat Berberis vulgaris Fruit ↓ Inflammation in colonic tissue, ↓ MDA activity
Kim etal. (2020) DSS-induced colitis Mouse Rumex spp. (R.
Gioxari etal. (2011) TNBS-induced colitis Rat Pistacia lentiscus Fruit Regulation of oxidant/antioxidant balance and
Model Species Plant Part
Mouse Malus spp. Procyanidins ↑ Proportions of TCRγδ and TCRαβ-CD8αα T cells
IBD
extract
TNBS-induced colitis Rat Berberis vulgaris Fruit ↓ Histologic lesions, morphologic damage, MPO
– ↓ TNF-α, IL-1β, IL-6, occludin, zonula occludens-1,
japonicus)
Results
in intraepithelial lymphocytes; suppression of
IFN-γ synthesis in stimulated intraepithelial
lymphocytes
improvement of inflammation condition in HT-29
human colonic epithelial cells
Restoration of bile acid metabolism disorder and
gut microbiota dysbiosis; inhibition of the
activation of NF-κB signaling; ↓ hyodeoxycholic
acid level, ↑ abundance of Verrucomicrobia at
phylum and Bacteroides and Akkermansia at
genus level
redox homeostasis, fatty acid β-oxidation, ATP
synthesis, apoptosis, regulatory mitochondrial
transcription factors
calpain, tissue transglutaminase
CuZnSOD mRNA level
activity
p21, p53, and Bcl-2; ↑ expression of IL-10,
claudin-2, and cleaved caspase-3; prevention of
colitis by protecting tight junction connections in
colonic tissue
modulation of inflammation
Naouar etal. (2016) TNBS-induced colitis Rat Pistacia lentiscus Oil Attenuation of erosion, cryptitis, irregular crypts,
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and crypt loss; curative intervention improvement
of ulceration, and hyperplasia, cryptitis, irregular
crypts and crypt loss
Zahouani etal. (2020) Acetic acid-induced UC Rat Pistacia lentiscus Leaf Improvement in macroscopic colonic damage;
↓ LPO and carbonylation of proteins, ↑ activities of
antioxidant enzyme such as SOD, CAT, GSH,
and GS Ts; ↓ IL-6 level in colon and plasma
Boutemine etal. (2021) DSS-induced UC Mouse Pistacia lentiscus Leaf ↓ Clinical score of acute colitis, DAI, and histologic
Fatani etal. (2016) Acetic acid-induced colitis Rat Commiphora
molmol
Khodakarm-Tafti etal.
(2015)
GST, glutathione S-transferase; TBARS, thiobarbituric acid-reactive substances.
Acetic acid-induced colitis Rat Elaeagnus
angustifolia
plasma
– ↓ Pro-inflammatory cytokines, PGE
TBARS
, NO, and
2
Fruit ↓ Erosion and ulceration, inflammatory cell
infiltration; regeneration and improvement of
mucosa
Evidence-Based Review of Medicinal Plant 201
Table 5.4. Clinical studies on medicinal plants claimed to be effective in IBD in TPM.
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202 Saeideh Momtaz etal.
Study
Langhorst
etal. (2013)
Langhorst
etal. (2014)
Gupta etal.
(1997)
Madisch etal.
(2007)
Mohammad
(2012)
No. of
Study design
Randomized,
double-blind,
doubledummy
patients Disease Plant Part of plant Control group
96 UC Combination of
chamomile,
Commiphora
molmol, Coffea
arabica
Randomized,
double-blind,
doubledummy
126 UC Combination of
myrrh,
chamomile
extract, coffee
charcoal
Randomized – UC in grade
Boswellia serrata
II and III
Double-blind,
placebo-
31 Collagenous
colitis
Boswellia serrata Extract Placebo 6 weeks ↑ Population of patients in
controlled,
multicenter
trial
Clinical study 32 IBS Anethum
graveolens
Flower dry
extract
Flower dry
extract
Gum resin
preparation
Leaves and
stems
Duration of
treatment
Results
Mesalazine 12 months Complete mucosal
healing
Healthy control
subjects
12 months ↑ CD4
+
T cells,
CD4+CD25
med
effector T
cells, and CD4+CD25
regulatory T cells
Sulfasalazine 6 weeks Improvement of stool
properties,
his
topathologic and
microscopic
manifestations of rectal
biopsies
clinical remission
Mebeverine 2 weeks Improvement in all IBS
symptoms including
pain severity, pain
frequency, stool
frequency, stool
consistency, abdominal
distension, incomplete
evacuation, urgency,
and passing of mucus
high
Tavakoli etal.
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(2019)
Abbasi etal.
(2018)
Fernández-
Bañares
etal. (1999)
Kim etal.
(2016)
Kamali etal.
(2017)
Baghizadeh
etal. (2021)
Tafazoli etal.
(2022)
Randomized,
double-blind,
placebocontrolled
clinical trial
Randomized
double-blind,
placebocontrolled
clinical trial
Open label,
parallel-group,
multicenter,
randomized
clinical trial
Randomized,
double-blind,
placebocontrolled
clinical trial
Randomized,
double-blind,
placebocontrolled
clinical trial
Randomized,
double-blind,
placebocontrolled
clinical trial
Case report 1 Chronic
20 UC Rosa ×
52 IBS Bunium persicum Consumption
105 UC Plantago ovata Seed Mesalamine 12 months Effective to maintain
– UC Mango +
78 UC Punicum
61 UC Plantago major Seed Placebo 8 weeks ↓ Visible blood in stool,
pancolitis
Oil Placebo 2 months ↓ Mayo Clinic (DAI)
damascena
Placebo 5 weeks No effect on symptoms
of powder
Beverages Placebo 4 weeks ↓ LCAI score
Punicum
granatum
Peel extract Placebo 4 weeks Therapeutic response
granatum
Plantago major – – 2 years Improvement in clinical
scores
and inflammatory
markers of patients
remission in patients
with UC
significantly higher in
patients with hot
temperament compared
to patients with cold
temperament
distension, and anal
pain
examination, patient’s
history, colonoscopy,
pathology test, and
myoclonic score
Continued
Evidence-Based Review of Medicinal Plant 203
Table 5.4. Continued.
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No. of Duration of
Study
Kaliora etal.
(2007)
Papada etal.
(2018)
Papada etal.
(2019)
oxLDL, oxidized low-density lipoprotein; LDL, HDL, high-density lipoprotein.
Study design patients Disease Plant Part of plant Control group treatment
– 18 Mild to
moderately
active CD
Randomized,
double-blind,
placebocontrolled
clinical trial
Randomized,
double-blind,
placebocontrolled
clinical trial
60(CD, n =
40; UC,
n = 20)
60(CD, n =
40; UC,
n = 20)
Active IBD
(CD and
UC)
Active IBD
(CD and
UC)
Pistacia lentiscus Chios mastic
resin
Pistacia lentiscus P. lentiscus
supplement
Pistacia lentiscus P. lentiscus
supplement
Results
Healthy controls
treated with
Chios mastic
resin
Placebo 3 months ↓ oxLDL, oxLDL/HDL,
Placebo 3 months ↓ Fecal lysozyme and
4 weeks ↓ CD activity index,
↓ plasma IL-6 and CRP,
↓ total antioxidant
potential
and oxLDL/LDL
fibrinogen, increase of
Fe
204 Saeideh Momtaz etal.
Evidence-Based Review of Medicinal Plant 205
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while inducing SOD, GPx, CAT, and total
GSH. L. usitatissimum suppressed the immune response and neutrophil infiltration
by hampering TNF-α and IFN-γ levels and
increasing IL-17 levels (Palla et al., 2016).
The same group compared the power of the
hydromethanolic extracts of flaxseed and
flaxseed oil to ameliorate acetic acid-induced
colitis in mice. It was shown that both flaxseed oil and its crude extract are favorable to
manage IBD by means of anti-inflammatory,
antibacterial, and antispasmodic activities.
However, their mechanisms of actions are
different. For instance, flaxseed extract was
more effective in reducing mortality and improvement of colonic ulcers than flaxseed oil
at 500 mg/kg; while the oil exhibited higher
anti-inflammatory effect. Antispasmodic
and anticholinergic activities of the crude extract (0.03 and 0.1 mg/ml) were greater than
for flaxseed oil (1 and 3 mg/ml). Flaxseed oil
(9 and 14 μg/ml) has shown antibacterial ac-
tivity against enteropathogenic E. coli (EPEC),
enterotoxigenic E. coli (ETEC), and enteroaggregative E. coli (EAEC); whereas the crude
extract was effective against EPEC at
100 μg/ml (Palla etal., 2020).
In a study by Silva, the influence of the
hydrolysis with Alcalase® and simulated GI
digestion on the antioxidant capacity of different flaxseed products and their protective effects on 2,4,6-trinitrobenzenesulfonic
acid (TNBS)-induced colitis in mice were assessed. Flaxseed protein hydrolysates and
phenolic fractions inhibited NO and TNF-α
secretion in stimulated macrophage RAW
cells and also reduced ROS production,
weight loss, systemic indicators of colonic
mucosal damage and inflammation, Th1
and Th17 responses, T-cell proliferation,
and inflammatory cytokine levels (Silva,
2016). An Iranian traditional herbal formula
called “Magliasa”, containing 8% w/w L. usi-
tatissimum seeds, remarkably attenuated colonic histopathologic and macroscopic
scores of colitis in TNBS-induced UC in rats.
The levels of TNF-α, IL-1β, MPO, and lipid
peroxidation (LPO) were significantly lower
in Magliasa-treated animals. It is noticeable
that Magliasa at any dose could not increase
the antioxidant capacity (Rahimi etal ., 2013).
Together, flaxseed extract ameliorates the
severity of colitis by scavenging oxygenderived free radicals and suppression of intestinal inflammation, thereby it may be a
new approach for immunotherapy in IBD.
Althaea officinalis L.
Marshmallow is a rich source of acidic polysaccharides, starch, pectins, mucilage, and
flavonoids with significant antioxidant and
soothing properties (Capek et al., 1987;
Gudej, 1991; Sendker etal., 2017). A recent
in vitro study reported antioxidant and
anti-inflammatory effects of the root extracts of Althaea officinalis. The plant was
able to protect human macrophages against
hydrogen peroxide (H
icity and H2O2-induced ROS production.
)-induced cytotox-
2O2
A. officinalis inhibited the lipopolysaccharide
(LPS)-induced release of TNF-α and IL-6 in
macrophages, additionally improving the
migratory capacity of macrophages (Bonaterra et al., 2020). Oral administration of
A. officinalis extract, once daily for 14 days,
led to a protective effect against pyloricligation/indomethacin-induced gastric ulceration in rats, probably via its antioxidant
properties, inhibition of histamine and
gastrin release, suppression of formation of
pro-inflammatory cytokines like TNF-α and
IL-1β, and promotion of mucin, NO, prostaglandin E2 (PGE2) and prostaglandin I
(PGI2) contents. The expression of the pro-
2
tective heme oxygenase-1 (HO-1) and cystathionine β-synthase (CBS) enzymes in
gastric mucosal tissue was also increased
(Zaghlool etal., 2019). The potential role of
the aqueous extract of A. officinalis flower in
gastric ulcer, inflammation, and platelet
aggregation was the subject of another research in a rat model. A. officinalis at doses of
50, 100, and 250 mg/kg b.w. exhibited antiulcerogenic, as well as acute and chronic
anti-inflammatory effects. Inhibition of
platelet aggregation was observed at 500
μg/ml concentration (Hage-Sleiman et al.,
2011). In accordance, Zaghlool etal. (2015)
found that administration of the aqueous
extract of marshmallow flower (100 mg/kg
b.w., orally for 14 days) could protect against
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