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Medicinal plants and antimicrobial activity

Article in Journal of Ethnopharmacology · September 2005

DOI: 10.1016/j.jep.2005.04.025 · Source: PubMed

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 Journal of Ethnopharmacology 100 (2005) 80–84

Perspective paper

Medicinal plants and antimicrobial activity

J.L. Rı́os ∗ , M.C. Recio
Departament de Farmacologı́a, Facultat de Farmàcia, Universitat de València. Av. Vicent Andrés Estellés s/n. 46100 Burjassot, Valencia, Spain

Received 27 April 2005; received in revised form 27 April 2005; accepted 27 April 2005
Available online 17 June 2005

Abstract

In the present paper, we analyze the past, present and future of medicinal plants, both as potential antimicrobial crude drugs as well as a source
for natural compounds that act as new anti-infection agents. In the past few decades, the search for new anti-infection agents has occupied
many research groups in the field of ethnopharmacology. When we reviewed the number of articles published on the antimicrobial activity of
medicinal plants in PubMed during the period between 1966 and 1994, we found 115; however, in the following decade between 1995 and
2004, this number more than doubled to 307. In the studies themselves one finds a wide range of criteria. Many focus on determining the
antimicrobial activity of plant extracts found in folk medicine, essential oils or isolated compounds such as alkaloids, flavonoids, sesquiterpene
lactones, diterpenes, triterpenes or naphtoquinones, among others. Some of these compounds were isolated or obtained by bio-guided isolation
after previously detecting antimicrobial activity on the part of the plant. A second block of studies focuses on the natural flora of a specific
region or country; the third relevant group of papers is made up of specific studies of the activity of a plant or principle against a concrete
pathological microorganism. Some general considerations must be established for the study of the antimicrobial activity of plant extracts,
essential oils and the compounds isolated from them. Of utmost relevance is the definition of common parameters, such as plant material,
techniques employed, growth medium and microorganisms tested.
© 2005 Elsevier Ireland Ltd. All rights reserved.

Keywords: Antimicrobial activity; Medicinal plants; Antibacterial; Antifungal

1. Introduction the essential oils of these plants rather than their extracts
that have had the greatest use in the treatment of infectious
Long before mankind discovered the existence of pathologies in the respiratory system, urinary tract, gastroin-
microbes, the idea that certain plants had healing potential, testinal and biliary systems, as well as on the skin. In the case
indeed, that they contained what we would currently charac- of Melaleuca alternifolia, for example, the use of the essen-
terize as antimicrobial principles, was well accepted. Since tial oil (tee tree oil) is a common therapeutic tool to treat
antiquity, man has used plants to treat common infectious acne and other infectious troubles of the skin (Vanaclocha
diseases and some of these traditional medicines are still and Cañigueral, 2003).
included as part of the habitual treatment of various maladies. In the present paper, we analyze the past, present and
For example, the use of bearberry (Arctostaphylos uva-ursi) future of medicinal plants, both as potential antimicrobial
and cranberry juice (Vaccinium macrocarpon) to treat urinary crude drugs as well as a source for natural compounds that
tract infections is reported in different manuals of phytother- act as new anti-infection agents.
apy, while species such as lemon balm (Melissa officinalis),
garlic (Allium sativum) and tee tree (Melaleuca alternifo-
lia) are described as broad-spectrum antimicrobial agents 2. Past
(Heinrich et al., 2004). That being said, it has generally been
In the past few decades, the search for new anti-infection
∗ Corresponding author. Tel.: +34 963 544 973; fax: +34 963 544 973. agents has occupied many research groups in the field of
E-mail address: riosjl@uv.es (J.L. Rı́os). ethnopharmacology. Recio et al. (1989a) reviewed the most

0378-8741/$ – see front matter © 2005 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.jep.2005.04.025
 J.L. Rı́os, M.C. Recio / Journal of Ethnopharmacology 100 (2005) 80–84 81

relevant articles on this subject published between 1978 and the factors that influence the in vitro antimicrobial activity of
1988, compiling a list of 75 species in which the authors essential oils and their mechanisms of action. Moreover, they
had established the activity of the extract along with both include an overview of the susceptibility of human and food-
the spectrum of and the principles responsible for this activ- borne bacteria and fungi towards different essential oils and
ity. In general, the review showed that phenolics are the their constituents. The most relevant ones, which include the
predominant active chemical in these plants, with Gram pos- essential oils of thyme, origanum, mint, cinnamon, salvia and
itive bacteria being the most sensible germs. The review clove, have antimicrobial properties.
also revealed, however, the major problem with this type of
research, namely the lack of uniformity in the criteria selected
to study the activity. This has in the past lead to relevant con- 3. Present
tradictions between the results obtained by different groups
and even for the same authors studying the same sample with When we reviewed the number of articles published on the
different methods (Pellecuer et al., 1976). To try to solve this antimicrobial activity of medicinal plants in PubMed during
important problem, Rı́os et al. (1988) published a review of the period between 1966 and 1994, we found 115; however,
the experimental methods used for studying the activity of in the following decade between 1995 and 2004, this number
both plant extracts and essential oils to date. They proposed more than doubled to 307. Focusing the search specifically
the use of diffusion methods for studying polar compounds of on the antimicrobial activity of essential oils, 187 references
small or medium molecular size and determining the antimi- appeared in PubMed between 1971 and 2005; however, in a
crobial spectrum because this method allows researchers to search processed by the ISI web of knowledge, the number of
test different compounds against one microorganism. The references for essential oils was much higher (323 between
solid dilution method was recommended for studying polar 1986 and 2005). These figures demonstrate the increased
and non-polar substances as well as all types of complex interest for this type of research among that portion of the
extracts. This method is especially good for determining the scientific community dedicated to the investigation of the
relative potency of extracts or essential oils and for estab- medicinal properties of plants. In the studies themselves one
lishing their antimicrobial spectrum as it facilitates the use of finds a wide range of criteria. Many focus on determining the
different strains against the extract on the same plate. Finally, antimicrobial activity of plant extracts found in folk medicine
the liquid dilution method is the best way to establish the real (Ngwendson et al., 2003), essential oils (Alma et al., 2003)
potency of a pure compound, but solubility is an obvious or isolated compounds such as alkaloids (Klausmeyer et al.,
requisite. 2004), flavonoids (Sohn et al., 2004), sesquiterpene lactones
The protocols proposed by Rı́os et al. were widely (Lin et al., 2003), diterpenes (El-Seedi et al., 2002), triter-
accepted by many research groups as can be seen by the penes (Katerere et al., 2003) or naphtoquinones (Machado
numerous times the paper has been cited. The proposed meth- et al., 2003), among others. Some of these compounds were
ods have been used principally in the study of plant extracts isolated or obtained by bio-guided isolation after previously
of medium or no polarity. The article has been most often detecting antimicrobial activity on the part of the plant. These
cited in articles published in the Journal of Ethnopharma- papers comprise about 65% of all the articles on micro-
cology (23% of all the citations of the article), followed by bial activity and medicinal plants published and compiled
those appearing in Pharmaceutical Biology (12%), but all by PubMed. Although this type of research is the most com-
told it has been cited in 42 journals, some of them extremely mon, set criteria to study the activity is often lacking: either
specific. the selection of microorganisms is not well established, the
To examine the problem of a lack of unified criteria more in assayed doses are extremely high, the positive control is not
depth, we can look particularly at the study of the antimicro- clearly defined or the methods are inadequate. In fact, many of
bial activity of essential oils. Janssen et al. (1987) reviewed these papers view the antimicrobial activity as merely a com-
the characteristics of these kinds of complex mixtures as well plement of the study, without showing interest in the plant’s
as the techniques used for studying them and concluded that therapeutic potential.
the results are difficult to compare as the test methods dif- A second block of studies focuses on the natural flora of a
fered so widely. They thus proposed that in future the strain specific region or country. Examples of such articles that have
number of the tested microorganism, the composition of the been published recently include studies of medicinal plants
essential oil and the conditions under which it was obtained from Brazil (Duarte et al., 2005), Thailand (Wannissorn et al.,
be included as an integral part of the report. 2005), Turkey (Uzun et al., 2004), Lebanon (Barbour et al.,
Recently, Kalemba and Kunicka (2003) reviewed the clas- 2004), Argentina (Salvat et al., 2004), Colombia (López
sical methods commonly used for the evaluation of the et al., 2001), India (Jeevan Ram et al., 2004), Malaysia (Wiart
antibacterial and antifungal activities of essential oils, includ- et al., 2004), Ghana (Konning et al., 2004), Peru (Rojas et al.,
ing the agar diffusion method (paper disc and well), the 2003), Uganda (Olila et al., 2001), Cameroon (Nkuo-Akenji
dilution method (agar and liquid broth) and the turbidimet- et al., 2001), Qatar (Mahasneh, 2002), the Ivory Coast
ric and impedimetric monitoring of microorganism growth in (Atindehou et al., 2002) and the Democratic Republic of the
the presence of tested essential oils to draw conclusions about Congo (Otshudi et al., 2000). Others prefer to study a wider
82 J.L. Rı́os, M.C. Recio / Journal of Ethnopharmacology 100 (2005) 80–84

region that includes different countries such as Asia (Almas, isolation of potential principles. Thus, when the activity of
2001) or Africa (Tshibangu et al., 2002), or a wide zone fractions and compounds is inferior to the total extract or
within one country such as Siberia (Kokoska et al., 2002). fraction, rather than invalidating the results, this should con-
These papers represent 17% of the articles on microbial activ- firm the known anti-infection properties of the plant. In the
ity and medicinal plants compiled by PubMed. This criterion last 25 years, there was a predominant tendency to publish
may be useful for understanding the activity of plants used in the activity of plants or natural products in isolation, but we
folk medicine in different parts of the world, but it is much think that the next 25 years should be spent in part on prob-
more random than an ethnopharmacological criterion, which ing this activity more in depth. The fact that a plant extract
is more adequate here. exhibits activity is of interest, but it is only a preliminary
The third relevant group of papers is made up of specific piece of data and should be followed by the identification
studies of the activity of a plant or principle against a con- of the active compounds by means of a bio-guided assay.
crete pathological microorganism. These studies have in the Finally, research should be kept up in order to uncover as
past focused on activity against Candida albicans (Duarte much potentially interesting data as possible, including tox-
et al., 2005), Helicobacter pylori (O’Gara et al., 2000), icity against animal or human cells, mechanisms of action,
enterohaemorrhagic Escherichia coli (Voravuthikunchai effects in vivo, positive and negative interactions with com-
et al., 2004), sexually transmitted diseases (Tshikalange et mon antibiotics and so forth. In this vein, Shibata et al. (2005)
al., 2005) including Neisseria gonorrhoeae (Shokeen et al., studied the effect of ethyl gallate on ␤-lactam susceptibil-
2005), bacteria resistant to known antibiotics such as Staphy- ity in methicillin-resistant and methicillin-sensitive strains
lococcus aureus, which is resistant to methicillin (Machado et of Staphylococcus aureus. They demonstrated that it inten-
al., 2003) or vancomycin-resistant enterococci (Fukai et al., sified the antibiotic effect and that the synergistic activity of
2004), as well as activity against multi-drug resistant bacteria the alkyl gallates is specific for ␤-lactam antibiotics since
such as Salmonella typhi (Rani and Khullar, 2004). no significant changes were observed in the potency of the
Finally, another criterion was the study of plants used for other classes of antibiotics tested. This study supports the
cosmetic or alimentary purposes, especially as a preservative, possible use of these principles together with known antibi-
or the study of spices to justify their use as antimicrobial otics to increase their potency and avoid undesirable side
agents. While spices are thought to be antimicrobial agents effects. Another interesting study reports on the effect of
against human pathogenic bacteria and yeasts, when Arora 5 -methoxyhydnocarpin, a compound isolated from chaul-
and Kaur (1999) tested different spices, only garlic and clove moogra oil, on the activity of berberine (Stermitz et al., 2000).
were found to exhibit antimicrobial activity. Indeed, some While 5 -methoxyhydnocarpin exhibited no antimicrobial
bacteria, which showed resistance to certain antibiotics were activity on its own, it greatly enhanced the action of berber-
sensitive to extracts of both garlic and clove. ine against Staphylococcus aureus. The authors observed that
All the cited criteria seem sufficient to justify the studies, the level of accumulation of berberine in the cells increased
but we believe that the research should be focused on achiev- sharply in the presence of 5 -methoxyhydnocarpin, allow-
ing definitive knowledge about the plant and its properties. ing this natural product to effectively disable the bacterial
For example, in one of our studies we screened 140 medicinal resistance mechanism against berberine since otherwise this
plants (two extracts of each) used in the Mediterranean region alkaloid is readily extruded by multi-drug resistance pumps
as anti-infection agents (Rı́os et al., 1987; Recio et al., 1989b), of the human pathogen Staphylococcus aureus. In this case,
and then selected one of them to study comprehensively, with this study supports the potential use of a weak antimicrobial
the isolation and identification of the active principles as well natural product together with another compound to increase
as the subsequent determination of the spectra and potency of its activity. This type of finding could further boost the use of
the isolated compounds. The selected species was Helichry- medicinal plants, extracts or natural products, either alone,
sum stoechas, from which we isolated 10 principles. In the combined or together with antibiotics.
end, however, only four of them exhibited activity in a range
of 3–25 ␮g/ml against Gram positive bacteria (Rı́os et al.,
1991). 5. Proposals and conclusions

Some general considerations must be established for the

4. Future study of the antimicrobial activity of plant extracts, essential
oils and the compounds isolated from them. Of utmost rele-
Over the next few years, the study of medicinal plants vance is the definition of common parameters, such as plant
as antimicrobial agents should be focused in part on ascer- material, techniques employed, growth medium and microor-
taining specific information about the plant’s antimicrobial ganisms tested.
activity, avoiding studies in which researchers use this crite- Scientific criteria should be used in the selection of the
rion merely as a complement to a phytochemical study. The plant material. Moreover, to avoid the use of random criteria,
isolation of active compounds should be undertaken in light the selection of plants should be made from an ethnophar-
of the known activity of the plant and likewise follow a guided macological perspective. All the species tested should be
 J.L. Rı́os, M.C. Recio / Journal of Ethnopharmacology 100 (2005) 80–84 83

perfectly described and identified; this must include the with quantities higher than 1 mg/ml for extracts or 0.1 mg/ml
specifics of collection including location, season, date and for isolated compounds should be avoided, whereas the pres-
time of day. The use of commercial samples should be limited ence of activity is very interesting in the case of concentra-
to cases of standardized extracts or defined phytomedicines. tions below 100 ␮g/ml for extracts and 10 ␮g/ml for isolated
The solvent and the extraction system may both modify the compounds.
final results. The most appropriate method would be that in In summary, it is our firm belief that the study of medic-
which the extract were the same as that used in folk medicine inal plants as antimicrobial agents is necessary for gaining
or phytotherapy, although in the lab the use of methanol or insight into medicinal flora and their real value, but the use of
ethanol extract is much more common, sometimes making a standard method for investigation is essential. Likewise, the
room for the essential oil. The results are notably affected. concentrations or dilutions used must be appropriate. More-
Thus, in the in vitro test carried out by Ross et al. (2001) with over, research in this area should be carried on until the agent
garlic, the activity of garlic powder against most bacteria was responsible for the activity has been determined or, as the case
higher than for the plant or crude drug; however, these authors may be, the most active fraction or extracts have been discov-
specify that garlic oil offers even greater therapeutic poten- ered. Finally, different kinds of studies on the mechanisms of
tial. For their part, Nostro et al. (2000) demonstrated that action, interactions with antibiotics or other medicinal plants
species such Helichrysum italicum or Phytolacca dodecan- or compounds, and the pharmacokinetic profile of the extracts
dra showed moderate activity against Escherichia coli when should be given high priority.
the diethyl extract obtained after extraction of the aqueous
suspension of the drug powder was used, but that there were
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