Anti-Helicobacter pylori activity of plants used in Mexican traditional medicine for gastrointestinal disorders

Abstract

Helicobacter pylori is the major etiological agent of chronic active gastritis and peptic ulcer disease and is linked to gastric carcinoma. Treatment to eradicate the bacteria failed in many cases, mainly due to antibiotic resistance, hence the necessity of developing better therapeutic regimens. Mexico has an enormous unexplored potential of medicinal plants. This work evaluates the in vitro anti-H. pylori activity of 53 plants used in Mexican traditional medicine for gastrointestinal disorders.
To test the in vitro antibacterial activity, agar dilution and broth dilution methods were used for aqueous and methanolic extracts, respectively.
Aqueous extracts of Artemisia ludoviciana subsp. mexicana, Cuphea aequipetala, Ludwigia repens,and Mentha x piperita (MIC 125 to <250 microg/ml) as well as methanolic extracts of Persea americana, Annona cherimola, Guaiacum coulteri, and Moussonia deppeana (MIC <7.5 to 15.6 microg/ml) showed the highest inhibitory effect.
The results contribute to understanding the mode of action of the studied medicinal plants and for detecting plants with high anti-Helicobacter pylori activity.

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Journal of Ethnopharmacology 122 (2009) 402–405
Contents lists available at ScienceDirect
Journal of Ethnopharmacology
journal homepage: www.elsevier.com/locate/jethpharm
Ethnopharmacological communication
Anti-Helicobacter pylori activity of plants used in Mexican traditional
medicine for gastrointestinal disorders
Israel Castillo-Juáreza, Violeta Gonzáleza, Héctor Jaime-Aguilara, Gisela Martínez a,
Edelmira Linaresb, Robert Byeb, Irma Romeroa,∗
aDepartamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad Universitaria, C.P. 04510, México, D.F., Mexico
bJardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, C.P. 04510, México, D.F., Mexico
article info
Article history:
Received 14 October 2008
Received in revised form 2 December 2008
Accepted 21 December 2008
Available online 27 December 2008
Keywords:
Helicobacter pylori
Antibacterial activity
Mexican medicinal plants
Gastritis
Aqueous extract
Methanol extract
abstract
Aim of the study: Helicobacter pyloriis the major etiological agent of chronic active gastritis and peptic ulcer
disease and is linked to gastric carcinoma. Treatmentto eradicate the bacteria failed in many cases, mainly
due to antibiotic resistance, hence the necessity of developing better therapeutic regimens. Mexico has
an enormous unexplored potential of medicinal plants. This work evaluates the in vitro anti-H. pylori
activity of 53 plants used in Mexican traditional medicine for gastrointestinal disorders.
Materials and methods: To test the in vitro antibacterial activity, agar dilution and broth dilution methods
were used for aqueous and methanolic extracts, respectively.
Results: Aqueous extractsof Artemisia ludoviciana subsp. mexicana, Cuphea aequipetala, Ludwigia repens,and
Mentha ×piperita (MIC 125 to <250␮g/ml) as well as methanolic extracts of Persea americana, Annona che-
rimola, Guaiacum coulteri, and Moussonia deppeana (MIC <7.5to 15.6 ␮g/ml) showed the highest inhibitory
effect.
Conclusions: The results contribute to understanding the mode of action of the studied medicinal plants
and for detecting plants with high anti-Helicobacter pylori activity.
© 2009 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
The Gram-negative bacterium Helicobacter pylori is the most
important etiological agent of chronic active type B gastritis and
peptic ulcer diseases, and is linked to gastric carcinoma (Atherton,
2006). The prevalence of Helicobacter pylori is about 40% in devel-
oped countries and 80–90% in the developing world (Perez-Perez
et al., 2004). Once acquired, Helicobacter pylori infection usually
persists for life unless treated by antimicrobial therapy.
The conventional eradication triple therapy combines two
antibiotics and a proton pump inhibitor. The success rate follow-
ing this therapy is approximately 80% and is constantly decreasing
worldwide, mainly due to the antibiotic resistance (Wolle and
Malfertheiner, 2007). However, these therapies involve taking too
many drugs, which may causeside ef fects that, in addition tosignifi-
cant cost of the treatment, promote insufficient patient compliance.
These factors, together with antibiotic resistance, indicate the need
to find new anti-Helicobacter pylori treatments.
Mexico is one of the five Megadiverse countries of the world
given that about 50% of the 22,000 vascular plant species are
∗Corresponding author. Tel.: +52 55 56232511; fax: +52 55 56162419.
E-mail address: irma@bq.unam.mx (I. Romero).
endemic (Villase˜
nor, 2004). Over 3000 of these plants are used
medicinally (Bye et al., 1995). About one-third of these plants are
employed in the treatment of a variety of ailments associated with
the gastrointestinal system (Argueta et al., 1994).
In recent years the studies regarding the anti-Helicobacter pylori
activity of medicinal plants have increased considerably. Never-
theless, only one work has evaluated the anti-Helicobacter pylori
activity of some Mexican medicinal plants and that focused on
Yucatán, México (Ankli et al., 2002). Taking into account the enor-
mous potential of Mexican medicinal flora, the aim of this study is
to evaluate the in vitro anti-Helicobacter pylori activity of 53 plants
used in Mexican traditional medicine for gastrointestinal illness.
2. Materials and methods
2.1. Plant material
Plants were selected based on ethnobotanical studies made
in Mexico. The plants were obtained commercially or collected
from different parts of the country and were identified. Voucher
specimens were deposited in the National Herbarium of Mexico
(MEXU) of the National Autonomous University of Mexico. The list
of plants used and other valuable information is found in Table 1.
0378-8741/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.jep.2008.12.021

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I. Castillo-Juárez et al. / Journal of Ethnopharmacology 122 (2009) 402–405 403
Table 1
Anti-Helicobacter pylori activity of aqueous extracts(AE) and methanol extracts (ME) of Mexican medicinal plants.
Botanical species scientific name (Family) Common nameaFolk usagebPlant part usedcMIC (␮g/ml) Yield (%) Voucher number
AE ME AE ME
Dianthus caryophyllus L. (Caryophyllaceae) Clavel DD AP >1000 >500 1.8 0.8 1211828
Equisetum myriochaetum Schlecht. & Cham. (Equisetaceae) Cola de caballo U, G, SA, DI AP >1000 >500 1.7 0.8 2303
Taxodium mucronatum Ten.(Taxodiaceae) Ahuehuete DI L/B >1000 >500 6.4 0.4 1211841
Hibiscus sabdariffa L. (Malvaceae) Flor de Jamaica SA, DD F >1000 >500 18.2 17.7 1492
Hemiangium excelsum (Kunth) A.C. Sm. (Hippocrateaceae) Cancerina (GC) G, U, SA R/B >1000 >500 5.2 4.4 1549
Teloxys ambrosioides (L.) W.A.Weber (Chenopodiaceae) Epazote morado SA, DI, PA AP >1000 500 0.7 1.7 1201177
Anoda cristata (L.) Schltdl. (Malvaceae) Alaches SA L/S >1000 500 1.8 2.9 1222018
Poliomintha longiflora A. Gray (Lamiaceae) Orégano (NLMM/RCM) II, PA L/S >1000 250 10.3 8.0 1502
Quercus rugosa Née (Fagaceae) Encino U, SC, DI L >1000 125 0.7 2.2 1211827
Haplopappus spinulosus (Pursh) DC. (Asteraceae) Árnica Blanca II AP >1000 125 4.6 3.1 1204422
Capsella bursa-pastoris (L.) Medik. (Brassicaceae) Bolsa de Pastor U AP >1000 62.5 3.7 0.3 1211823
Tanacetum parthenium (L.) Sch. Bip. (Asteraceae) Santa María SA AP >1000 62.5 2.1 3.5 1201179
Machaeranthera cf. parviflora A. Gray (Asteraceae) Árnica morada DD AP >1000 31.2 4.2 2.4 1204424
Cymbopogon citratus (DC.) Stapf (Poaceae) Telimón SA L >1000 31.2 1.7 3.7 1201181
Ocimum basilicum L. (Lamiaceae) Albahaca SA, D, PA, DI AP >1000 31.2 9.8 2.0 1211816
Marrubium vulgare L. (Lamiaceae) Marrubio SA, DI, G L/S >1000 31.2 2.9 1.5 1201172
Plectranthus amboinicus (Lour.) Spreng. (Lamiaceae) Oreganón II AP >1000 31.2 6.7 5.4 1204423
Moussonia deppeana (Schltdl. & Cham.) Klotzsch ex Hanst.
(Gesneriaceae)
Tlanchichinole U, DI, SA L/S >1000 15.6 1.0 1.4 1201171
Guaiacum coulteri A. Gray (Zygophyllaceae) Cuachalalate blanco, Guayacán G,U, DD B >1000 ≤15.6 2.1 1.9 2042
Persea americana Mill. (Lauraceae) Aguacate DD, DI, PA, SA L >1000 <7.5 5.7 5.5 1201175
Tecoma stans (L.) Juss. ex Kunth(Bignoniaceae) Tronadora G, SP, DI AP 1000 500 7.0 2.9 1211818
Teloxys ambrosioides (L.) W.A.Weber (Chenopodiaceae) Epazote verde SA, DI, PA AP 1000 250 1.7 1.6 1201176
Plantago major L. (Plantaginaceae) Llantén DI AP 1000 250 2.9 1.8 1211826
Calandrinia micrantha Schltdl. (Portulacaceae) Chivitos DD L/S 1000 250 0.1 1.6 1222019
Machaeranthera tanacetifolia (Kunth)Nees (Asteraceae) Árnica Morada de Chihuahua U AP 1000 125 2.4 5.8 1222012
Tillandsia usneoides (L.) L. (Bromeliaceae) Heno G, DD AP 1000 125 2.2 2.3 1214144
Hesperozygis marifolia Epling (Lamiaceae) Orégano (NLJM) II, SA AP 1000 62.5 7.4 8.8 1501
Ruta chalepensis L. (Rutaceae) Ruda SA, DD, PA AP 1000 62.5 2.1 2.9 1201180
Campyloneurum amphostenon (Kunze exKlotzsch) Fée
(Polypodiaceae)
Lengua de ciervo PA L 1000 <62.5 2.2 0.7 1230313
Machaeranthera riparia (Kunth) A.G. Jones (Asteraceae) Árnica Morada de lavar, Chihuahua DD AP 1000 62.5 5.7 7.7 1222013
Eryngium carlinae F. Delaroche (Apiaceae) Hierba del sapo DD AP 1000 31.2 1.0 0.3 1211838
Lippia berlandieri Schauer (Verbenaceae) Orégano II, DD, SA AP 1000 31.2 1.8 0.8 1507
Verbena carolina L. (Verbenaceae) Verbena U, SA, PA AP 1000–500 62.5-125 3.1 2.9 1201174
Olea europaea L. (Oleaceae) Olivo DD, SA L/S 500 >500 5.0 6.4 1211834
Tagetes lucida Cav.(Asteraceae) Pericón SA, DI, DD L/S 500 500 4.0 5.3 1201173
Amphipterygium adstringens (Schltdl.) Standl.
(Anacardiaceae)
Cuachalalate (GC) G, U,SC B 500 250 1.8 5.8 1490/1491
Priva grandiflora (Ortega) Moldenke(Verb enaceae) Hierba de San Juan DI AP 500 250 1.6 1.5 1214141
Eupatorium petiolare Moc. ex DC. (Asteraceae) Hierba del Ángel DI, DD AP 500 125 4.7 1.3 1211817
Monarda austromontana Epling (Lamiaceae) Orégano de Chihuahua DD AP 500 125 5.0 4.3 2041
Gnaphalium canescens DC. (Asteraceae) Gordolobo G, SA, DI AP 500 62.5 8.6 1.8 1211825
Larrea tridentata (Sessé & Moc. ex DC.) Coville
(Zygophyllaceae)
Gobernadora DD AP 500 62.5 4.9 6.1 1493
Tithonia diversifolia (Hemsl.) A.G. (Asteraceae) Árnica SA, DD AP 500 62.5 5.5 6.1 1201170
Grindelia inuloides Willd. (Asteraceae) Árnicade Tepeaca DI AP 500 62.5 3.7 3.9 1222015
Buddleja perfoliata Kunth (Loganiaceae) Salvia de Bolita DD AP 500 <62.5 4.2 1.7 1211839
Heterotheca inuloides Cass. (Asteraceae) Árnica del país U, G, DI AP 500 31.25 1.5 2.0 1211822
Mirabilis jalapa L. (Nyctaginaceae) Maravilla DI, SP AP 250 >500 1.3 0.4 1211819
Cyrtocarpa procera Kunth (Anacardiaceae) Chupandilla DI B 250 ≥500 11.2 17.0 2043
Teloxys graveolens(Willd.) W.A. Weber (Chenopodiaceae) Epazote de zorrillo SA, DD, PA, DI AP 250 62.5 1.7 0.8 1211814
Annona cherimola Mill. (Annonaceae) Chirimoya DI, PA, U L/S 250 <15.6 1.9 0.5 1211832

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Mentha ×piperita L. (Lamiaceae) Hierbabuena (FCH) SA, DD, G, DI L/S <250 500 2.1 4.4 1211815
Cuphea aequipetala Cav. (Lythraceae) Hierba del cáncer DI, SA AP 125 >500 2.3 0.7 1211831
Ludwigia repens J. R. Forst. (Onagraceae) Silveria G AP 125 500 4.5 7.0 1222022
Artemisia ludoviciana Nutt. subsp. mexicana (Willd. ex
Spreng.) Fernald (Asteraceae)
Estafiate SA, DI, PA L/S 125 250 2.3 1.8 1211833
Amoxicillin 0.05 0.1
Metronidazole 75 300
aBotanical species were mainly obtained from “Sonora” Market (México, D.F.) or collected in the field. When specified, plants were obtained from: NLMM: “Mesón de Estrella” Market, Monterrey, Nuevo León; NLJM: “Juárez”
Market, Monterrey, Nuevo León; RCM: “Real de Catorce” Market; GC: Gathering center (Axochiapan, Morelos/Jolalpan, Puebla); FCH: Hydroponic Culture, Facultad de Ciencias, UNAM.
bFolk usage: G: gastritis; U: stomach and/or duodenal ulcer; SA: stomach ache; DI: diarrhea; PA: parasites; DD: digestive disorders; II: intestinal infections; SC: stomach cancer; SP: stomach problem.
cAP: aerial part; L/S: leaf/stem; B: bark; L: leaf; R/B: root/bark; F: flower; L/B: leaf/branch.
2.2. Extract preparation
Fifty grams of each sample was used to prepare the extracts. For
aqueous extracts (AEs), the plant was boiled for 10 min with 600 ml
of tap water, filtered and centrifuged for 10 min at 3000 rpm; after-
wards the supernatant was lyophilized. In the case of methanol
extracts (MEs), the material was extracted for 72 h with 200 ml
of methanol. After filtration, the extracts were evaporated under
reduced pressure, below 50◦C.
2.3. Bacterial strain and culture conditions
Helicobacter pylori standard strain ATCC 43504 was grown on
Casman agar base (BBL) plates supplemented with 5% defibrinated
sheep blood, and 10␮g/ml vancomycin for a day at 37 ◦C under
microaerophilic conditions (10% CO2). The strains were identified
by Gram staining morphology and biochemical testing.
2.4. Minimum inhibitory concentration (MIC) determinations
The AEs were tested with the agar dilution method according to
the Clinical and Laboratory Standards Institute (CLSI) recommenda-
tions, in Mueller–Hinton agar (DIFCO) plates with 5% defibrinated
sheep blood, vancomycin (10 mg/l), trimethoprim (5mg/l), ampho-
tericin B (2 mg/l), and polymyxin B (2.5 mg/l), and containing the
plant extract to be tested. The AEs were dissolved in a minimal
volume of sterile distilled water to obtain a final concentration
in the plate of 125, 250, 500, and 1000 ␮g/ml. A volume of 0.1ml
Helicobacter pylori (∼107CFU) was spread onto the plates and incu-
bated for 5 days as previouslydescrib ed. Growthcontrol plates were
included in each experiment. The MIC was determined from visual
examinations as being the lowest concentration of the extracts in
the plate with no bacterial growth.
For the MEs, MIC was determined in broth cultures containing
Mueller–Hinton broth (DIFCO), 0.2% ␤-cyclodextrin and 10␮g/ml
vancomycin, incubated under gentle shaking (150 rpm) for the time
of the experiment in the above described conditions. The extracts
were dissolved in DMSO to give final concentrations in the culture
of 7.8, 15.6, 31.2, 62.5, 125, 250, and 500␮g/ml. These dilutions
(in a volume of 20 ␮l DSMO) were added to 3 ml of Helicobacter
pylori broth culture at the beginning of the exponential growth
phase (∼108CFU/ml). A660 was determined after 18h of incuba-
tion and was used to calculate the percentage of growth inhibition
with respect to a control that grew only with DMSO (which does
not have any effect on bacterial growth at the used concentration).
All the experiments were performed in triplicate. Amoxicillin
and metronidazole were used as reference antibiotics for validation
of results.
3. Results
Methanolic and aqueous extracts of 53 different plant species
(49 genera in 29 families) used in Mexican traditional medicine to
treat gastrointestinal disorders were screened in vitro for their anti-
Helicobacter pylori activity. The results are shown in Table 1, and the
species are organized in the order of aqueous extract effectiveness.
The resulting activities were classified as follows: for AEs, MIC val-
ues in ␮g/ml >1000, null; 1000, low; 500, moderate; 250, good;
and <250 to <125, strong; for MEs, MIC values in ␮g/ml >500, null;
500–250, low; 125–62.5, moderate; <62.5 to 31.25, good; and 15.6
to <7.8, strong.
AEs of Mentha ×piperita,Artemisia ludoviciana subsp. mexi-
cana,Cuphea aequipetala, and Ludwigia repens showed the highest
inhibitory effect; in contrast, MEs of these plants had little action
against Helicobacter pylori. Among the MEs, the most active plants
were Persea americana,Annona cherimola,Guaiacum coulteri, and
Moussonia deppeana, with MIC values of <7.5, <15.6, ≤15.6, and

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I. Castillo-Juárez et al. / Journal of Ethnopharmacology 122 (2009) 402–405 405
15.6 ␮g/ml, respectively. It is interesting to note that only the AE
of Annona cherimola also had good activity against the bacteria.
Compared with the reference antibiotic amoxicillin, the most
active extracts inhibit the growth of Helicobacter pylori at much
higher concentrations; but compared with metronidazole, the MEs
with MIC values of 250␮g/ml or less were better than metronida-
zole. It is worth noting that we tested extracts and not isolated
compounds; hence the isolation of different and potent compounds
from the most active extracts is encouraging.
4. Discussion and conclusions
Before the recognition of Helicobacter pylori as the main etiolog-
ical agent of chronic gastritis and peptic ulcer disease, the research
studies to elucidate the mechanisms by which traditionalme dicinal
plants exert their actions were focused on their gastroprotective,
and/or anti-acid, and/or anti-inflammatory effects (Borrelli and
Izzo, 2000). In recent years a great deal of research has been under-
taken to determine a direct action of plants upon Helicobacter pylori.
Although CLSI has made important recommendations to standard-
ize the antimicrobial susceptibility testing procedures, and some
plant screenings have begun to apply them, in vitro studies still
lack a normalization that would allow for the meaningful compar-
isons of activity. However, because these guidelines are proposed
for testing pure compounds, their strict utilization must be adjusted
in the case of crude plant extracts, mainly in the case of apolar
ones, where its solubility is restricted in the agar dilution method
recommended by the CLSI. Therefore it is necessary to develop a
reliable standardized method to test in vitro the anti-Helicobacter
pylori activity of plant extracts.The broth dilution method used here
allows the rapid partition of most of the methanolic extract tested,
making this methodology a good candidate for routine screening
work for apolar extracts.
The present study represents the first directed work to test
exclusively the in vitro activity against Helicobacter pylori of a large
number of Mexican traditional plants used for gastrointestinal ill-
ness. Also it reports for the first time the strong anti-Helicobacter
pylori activity of the AEs from Artemisia ludovicianasubsp. mexicana,
Ludwigia repens, and Cuphea aequipetala, and the MEs from Persea
americana,Guaiacum coulteri,Moussonia deppeana, and Annona che-
rimola. It would be promising to use them alone or in combined
therapies in in vivo studies to confirm their bioactivity.
The anti-Helicobacter pylori activity of Amphipterygium adstrin-
gens bark and its components have been published recently
(Castillo-Juarez et al., 2007). Other species used in this work,
have previously been proved against the bacteria. The 95% ethanol
extract of Chenopodium ambrosioides (the basionym of Teloxys
ambrosioides) resulted to have a moderate activity against the bac-
teria (Wang and Huang, 2005). It has also been reported that the ME
and AE of Mentha ×piperita had weak activity against Helicobacter
pylori (Mahady et al., 2005; Nostro et al., 2005); nevertheless, we
found that our AE had strong anti-Helicobacter pylori activity. Also,
the 70% aqueous methanol extract of Ocimun basilicum has been
reported as inactive against Helicobacter pylori 43504 (Stamatis et
al., 2003); but our ME at 100% had good activity against the bac-
teria. As we stated before, it is difficult to compare results. These
discrepancies may be due to the method of bioassay employed as
well as other variables such as the bacterial number or the solvent
used to make the extraction.
The methodology used in this work was standardized in order
to test the activity of many different plants, so we cannot exclude
the possibility that in some cases the active components were not
extracted, for example the most volatile ones that would evaporate
when plants are boiled.
Many of the most active anti-Helicobacter pylori plants have a
long history of traditional use as water-based remedies for gas-
trointestinal afflictions (Argueta et al., 1994). We found four MEs
exhibited strong antibacterial activity against Helicobacter pylori
even though records of their traditional preparation do not include
alcohol-based preparations; hence their observed activity in vitro
suggests new areas of field and laboratory research as well as novel
applications in community based health programs.
In general, the results indicated that 77% of the assayed plants
are active in at least one of the tested extracts, having from moder-
ate to strong antibacterial activityagainst Helicobacter pylori. Taking
into account that many of the active medicinal plants are also
used as condiments or food ingredients (e.g., Ocimum basiliscum,
Persea americana,Lippia berlandieri,Teloxys graveolens), their fre-
quent consumption could have a preventive effect in controlling
the Helicobacter pylori population of infected people, rather than
an eradicating action.
Our results provide valuable information about plants with high
anti-Helicobacter pylori activity, which will become the starting
material for bioassay guided fractionation to determine the active
constituents of the plant extracts. These data also contribute to the
understanding of the mode of action of these medicinal plants and
to the development of new anti-Helicobacter pylori therapies.
Acknowledgements
Partially supported by DGAPA-UNAM (IN-218108). We thank
Carlos Iglesias, Jardín Botánico Francisco Xavier Clavijero, Jalapa for
his collaboration in the collection of Tithonia diversifolia, and Paul
Hersh, Jardín Etnobotánico del INAH Morelos, for his support in the
collection of Cyrtocarpa procera.
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