Medicinal plant activity on Helicobacter pylori related diseases

Table 1 Virulence factors of Helicobacter pylori[4-7]

Virulence factor	Function
H. pylori colonization
Urease	Buffers stomach acid, toxic effect on epithelium cells, disrupting cell tight junctions, and sheathing antigen
Flagella	Active movements through mucin
BabA	Adhesin
H. pylori survival
Nox1	Resistance to killing by phagocytes, infected-site inflammation
Superoxide dismutase	Resistance to killing by phagocytes
Catalase	Resistance to killing by phagocytes
Phospholipase A	Digest phospholipids in cell membranes
Alcohol dehydrogenase	Gastric mucosal injury
Tissue inflammation and damage
Vac A	Cytotoxicity
cag PAI	31 genes coding for type IV secretion system
CagA	Immunodominant antigen (part of cag PAI)
OipA	Induce inflammation, especially for IL-8
DupA	Induce inflammation via CagA, OipA and/or VacA
HP-NAP	Neutrophil activation
Lewis x and y antigens	Molecular mimicry, autoimmunity
LPS	Low toxicity
Other
IceA	Homolog of type II restriction endonuclease

H. pylori: Helicobacter pylori; BabA: Blood-group-antigen-binding adhesion; CagA: Cytotoxin associated gene antigen; DupA: Duodenal ulcer promoting A; HP-NAP: H. pylori neutrophil activation protein; IceA: Induced by contact with epithelium factor antigen; LPS: Lipopolysaccharide; Nox1: NADPH oxidase 1; OipA: Outer inflammatory protein A; Vac A: Vacuolating cytotoxin A; IL: Interleukin.

Table 2 Anti-Helicobacter pylori activity of medicinal plant extracts and fractions

Plant	Test sample	MIC/MBC	Ref.
Strong activity (MIC: < 10 μg/mL)
Impatiens balsamina L.	Pod acetone/95% ethanol/	MIC: 0.625-2.5 μg/mL	Wang et al[52]
	ethyl acetate extracts	MBC: 1.25-2.5 μg/mL
Strong-moderate acticity (MIC: 10-100 μg/mL)
Persea americana, Annona cherimola, Guaiacum coulteri, Moussonia deppeana	Methanol extract	MIC: 7.5-15.6 μg/mL	Castillo-Juárez et al[53]
Myristica fragrans (seed), Rosmarinus officinalis (rosemary leaf )	Methanol extract	MIC: 12.5-25 μg/mL	Mahady et al[54]
Curcuma amada Roxb., Mallotus phillipinesis (Lam) Muell., Myrisctica fragrans Houtt., Psoralea corylifolia L.	70% Ethanol extract	MIC: 15.6-62.5 μg/mL	Zaidi et al[55]
Achillea millefolium, Foeniculum vulgare (seed), Passiflora incarnata (herb), Origanum majorana (herb) and a (1:1) combination of Curcuma longa (root), ginger rhizome	Methanol extract	MIC: 50 μg/mL	Mahady et al[54]
Carum carvi (seed), Elettaria cardamomum (seed), Gentiana lutea (roots), Juniper communis (berry), Lavandula angustifolia (flowers), Melissa officinalis (leaves), Mentha piperita (leaves), Pimpinella anisum (seed)	Methanol extract	MIC: 100 μg/mL	Mahady et al[54]
Abrus cantoniensis, Saussurea lappa, Eugenia caryophyllata	Ethanol extract	MIC: 40 μg/mL	Li et al[56]
Hippophae rhamnoides, Fritillaria thunbergii, Magnolia officinalis, Schisandra chinensis, Corydalis yanhusuo, Citrus reticulata, Bupleurum chinense, Ligusticum chuanxiong	Ethanol extract	MIC: 60 μg/mL	Li et al[56]
Myroxylon peruiferum	Methanol extract	MIC: 62.5 μg/mL	Ohsaki et al[57]
Weak-moderate acticity (MIC: 100-1000 μg/mL)
Aristolochia pauciner6is	Rhizome/leave fraction	MIC: 4-128 μg/mL	Gadhi et al[58]
Cistus laurifolius, Spartium junceum, Cedrus libani, solstitialis, Momordica charantia, Sambucus ebulus, Hypericum perforatum	Solvent extract and hexane fraction	MIC: 1.95-250 μg/mL	Yeşilada et al[59]
Larrea divaricate Cav (leaves and tender branches)	Aqueous extract	MIC: 40-100 μg/mL	Stege et al[60]
Acacia nilotica (L.) Delile, Calotropis procera (Aiton)	Methanol/acetone extract	MIC: 8-256 μg/mL	Amin et al[61]
W.T. Aiton, Fagonia arabica L., Adhatoda vasica Nees, Casuarina equisetifolia L.
Zingiber officinale	95% Ethanol extract	MIC: 10-160 μg/mL	Nostro et al[62]
Tephrosia purpurea (Linn.) Pers.	Methanol extract and fraction	MIC: 25-400 μg/mL	Chinniah et al[63]
Terminalia macroptera (root)	Root solvent fraction	MIC: 100-200 μg/mL	Silva et al[64]
Black myrobalan (Teminalia chebula Retz)	Water extract	MIC: 125 μg/mL	Malekzadeh et al[65]
		MBC: 150 μg/mL
Rubus ulmifolius leaves	Ethyl acetate/methanol	MIC: 134-270 μg/mL	Martinia et al[66]
Amphipterygium adstringens	Bark petroleum ether fraction	MIC: 160 μg/mL	Castillo-Juárez et al[67]
Lycopodium cernuum	Hexane fraction	MIC: 16-1000 μg/mL	Ndip et al[68]
		MBC: 125-1000 μg/mL
Ageratum conyzoides, Scleria striatinux, Lycopodium cernua	Methanol extract	MIC: 63-1000 μg/mL	Ndip et al[69]
		MBC: 195-15000 μg/mL
Sclerocarya birrea	Acetone/aqueous stem bark extract	MIC: 80-2500 μg/mL	Njume et al[70]
Including Artemisia ludoviciana subsp.mexicana 43 plants	Methanol/aqueous extract	MIC: 312-500 μg/mL	Castillo-Juárez et al[53]
Pteleopsis suberosa	Stem bark methanol extract	MIC: 313-500 μg/mL	Germanò et al[71]
Ageratum conyzoides, Scleria striatinux, Lycopodium cernua	Methanol extract	MIC: 32-1000 μg/mL	Ndip et al[69]
Including Cuminum cyminum L., Cynara scolymus L., Origanum vulgare L. 17 plants	Ethanol extracts	MIC: 600-10000 μg/mL	Nostro et al[72]
Allium sativum	Aqueous extract	MIC: 2000-5000 μg/mL	Cellini et al[73]
Weak acticity (MIC: > 1000 μg/mL)
Mentha×piperita, Peppermint Oil, Origanum vulgare, Pimpinella anisum, Aniseed Oil, Syzygium aromaticum	Essential oil	IC50: 160-1460 μg/mL	Cwikla et al[74]
Chamomila recutita L., Ilex paraguariensis A. St.-Hil.	96% Ethanol extract	MIC: < 625-1250 μg/mL	Cogo et al[75]
Allium ascalonicum Linn. (leaf)	Methanol extract	MIC: 625- 1250 μg/mL	Bolanle et al[76]
Sclerocarya birrea	Stem bark acetone/aqueous extracts	MIC90: 60-2500 μg/mL	Njume et al[70]
Punica granatum, Quercus infectoria	Ethanol extract	MIC: 160-> 2500 μg/mL	Voravuthikunchai et al[77]
Mentha×piperita, Peppermint Oil, Origanum vulgare, Pimpinella anisum, Aniseed Oil, Syzygium aromaticum	Essential oil	IC50: 160-1460 μg/mL	Cwikla et al[74]
Including Anthemis melanolepis 13 plants	70% Methanol extract	MIC: 625-5000 μg/mL	Stamatis et al[78]
Including Cuminum cyminum L. 17 plants	Ethanol extract	MIC: 75-10000 μg/mL	Nostro et al[72]
Plumbago zeylanica L.	Acetone extract	MIC: 320-10240 μg/mL	Wang and Huang[79]
		MBC: 5120-81920 μg/mL
Anisomeles indica (L.) O. Kuntze, Alpinia speciosa (Wendl.) K. Schum., Bombax malabaricum DC., Paederia scandens (Lour.) Merr.	95% Ethanol extract	MIC: 640-10240 μg/mL	Wang and Huang[80]
Allium sativum	Aqueous extract	MIC: 0.1% (v/v)	Cellini et al[73]
Including Cymbopogon citratus (lemongrass) 13 plants	Essential oil		Ohno et al[81]

MIC: Minimum inhibitory concentration; MBC: Minimum bactericidal concentration.

Table 3 Anti-Helicobacter pylori activity of compounds from plants

Compound	Original plant	MIC/MBC	Ref.
Phenolics/Simple phenols/Polyphenols
Boropinic acid	Boronia pinnata	MIC: 1.62 μg/mL	Epifano et al[82]
	Sm.
Corilagin, 1,2,3,6-tetra-O-galloyl-b-D-glucose	Geranium wilfordii	MIC: 2-8 μg/mL	Zhang et al[83]
Egallic acid	Rubus ulmifolius leaves	MIC: 2-10 μg/mL	Martinia et al[66]
3-Farnesyl-2-hydroxybenzoic acid	Piper multiplinervium	MIC: 3.75-12.5 μg/mL	Rüegg et al[84]
Epigallocatechin gallate, epicatechin gallate, epigallocatechin,		MIC: 8-256 μg/mL	Mabe et al[85]
epicatechin
Magnolol	Magnoliae officinalis	MIC: 10-20 μg/mL	Bae et al[86]
Psoracorylifols	Psoralea corylifolia	MIC: 12.5-25 μg/mL	Yin et al[87]
Resveratrol	Red wine	MIC: 25-100 μg/mL	Paulo et al[88]
Cinnamic acid		MIC: 80-200 μg/mL	Bae et al[86]
Allixin	Allium sativum	MIC90: 50 μg/mL	Mahady et al[89]
Paeonol, benzoic acid, methyl gallate,	Paeonia lactiflora Roots	MIC: 80-320 μg/mL	Ngan et al[90]
1,2,3,4,6-Penta-O-galloyl-β-D-glucopyranose		MBC: 320-1280 μg/mL
Including 3-hydroxy-2,2-dimethyl-8-prenylchromane-6-propenoic	Brazilian propolis	MIC: 130-1000 μg/mL	Banskota et al[91]
acid 10 phenolic acids
Chlorogenic acid	Anthemis altissima	MIC: 312.5-1250 μg/mL	Konstantinopoulou et al[92]
Flavonoids
Quercetin 3-methyl ether,	Cistus laurifolius leaves	MIC: 3.9-62.5 μg/mL	Ustün et al[93]
quercetin 3,7-dimethyl ether, kaempferol 3,7-dimethyl ether
Kaempferol	Rubus ulmifolius leaves	MBC: 6 μg/mL	Martinia et al[66]
Kaempferol 4’-methyl ether, quercetin, rhamnetin, isoquercetrin,	Anthemis altissima	MIC: 6.25-50 μg/mL	Konstantinopoulou et al[92]
taxifolin, eriodictyol
Including licoisoflavone B and licoricidin 16 flavonoids	Licorice	MIC: 6.25-50 μg/mL	Fukai et al[94]
Cabreuvin	Myroxylon peruiferum	MIC: 7.8 μg/mL	Ohsaki et al[57]
3,5,7-Trihydroxy-4’-methoxyflavanol, keampferol-3,4’-dimethyl ether	Brazilian propolis	MIC: 500-1000 μg/mL	Banskota et al[91]
Quinones
2-Methoxy-1,4-naphthoquinone	Impatiens balsamina L.	MIC: 0.156-0.625 μg/mL	Wang et al[95]
		MBC: 0.313-0.625 μg/mL
2-(Hydroxymethyl)anthraquinone, anthraquinone-2-carboxylic acid,	Tabebuia impetiginosa	MIC: 2-8 μg/mL	Park et al[96]
Lapachol, plumbagin	Martius ex DC
Idebenone, duroquinone, menadione, juglone, benzoquinone,		MIC90: 0.8-25 μg/mL	Inatsu et al[97]
coenzyme Q1, coenzyme Q10, decylubiquinone
Emodin	Rhei Rhizoma	MIC86-99: 250 μg/mL	Wang and Chung[98]
Coumarins
Benzoyl aegelinol, aegelinol	Ferulago campestris (Apiaceae) roots	MIC: 5-25 μg/mL	Basile et al[99]
24 Synthetic coumarin derivatives		MIC: 10-40 μg/mL	Jadhav et al[100]
23 Synthetic coumarin derivatives		MIC50: 23->100 μg/mL	Kawase et al[101]
Terpenoids
Arjunglucoside I	Pteleopsis suberosa	MIC: 1.9-7.8 μg/mL	De Leo et al[102]
Trichorabdal	Rabdosia trichocarpa	MIC: 2.5-5 μg/mL	Kadota et al[103]
Sivasinolide, altissin, 1-epi-tatridin B, desacetyl-β-cyclopyrethrosin,	Anthemis altissima	MIC: 12.5-50 μg/mL	Konstantinopoulou et al[92]
tatridin-A
(Z)-R-santalol (7), (Z)-β-santalol, (Z)-lanceol	Santalum album	MIC: 7.8-31.3 μg/mL	Ochi et al[104]
Stigmasta-7,22-diene-3β-ol	Impatiens balsamina L.	MIC: 20-80 μg/mL	Wang et al[95]
		MBC: 20-80 μg/mL
Plaunotol	Plau-noi	MIC90: 12.5 mg/mL	Koga et al[105]
Terpinen-4-ol	Sclerocarya birrea (Anacardiaceae)	MIC50: 0.004-0.06 μg/mL	Njume et al[106]
Alkaloids
1-Methyl-2-[(Z)-8-tridecenyl]-4-(1H)-quinolone,	Evodia rutaecarpa fruits	MIC: < 0.05 μg/mL	Hamasaki et al[107]
1-Methyl-2-[(Z)-7-tridecenyl]-4-(1H)-quinolone
Tryptanthrin	Polygonum tinctorium Lour.	MIC: 2.5 μg/mL	Hashimoto et al[108]
Other compounds
Pyrrolidine	Sclerocarya birrea (Anacardiaceae)	MIC50: 0.05-6.3 μg/mL	Njume et al[106]
Diallyl disulfide, diallyl trisulfide, diallyl tetrasulfide, allicin		MIC: 3-100 μg/mL	O’gara et al[109]
		MBC: 6-200 μg/mL
Palmitoyl ascorbate		MIC: 40-400 μg/mL	Tabak et al[110]
Capric acid, lauric acid, myristic acid, myristoleic acid,		MBC: 0.5-5 mmol/L	Sun et al[111]
palmitoleic acid, linolenic acid, monolaurin, monomyristin

MIC: Minimum inhibitory concentration; MBC: Minimum bactericidal concentration.