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gastrointestinal problems, dental decay, or for regulating blood cholesterol levels (Ali-
Shtayeh, Yaniv, & Mahajna, 2000; Hanlidou, Karousou, Kleftoyanni, & Kokkini, 2004;
Kartalis et al., 2016; Triantafyllou, Chaviaras, Sergentanis, Protopapa, & Tsaknis, 2007
).
Mastic gum or oil is also used in dermatological products, toothpastes, drinks, or food
products (
Pachi et al., 2020). Even low concentrations of ethanol extracts of mastic gum
inhibited the growth of Helicobacter pylori (NCTC 11637) (
Huwez, Thirlwell, Cockayne, &
Ala’Aldeen, 1998
) by altering bacterial cell wall as seen using a transmission electron
microscope (
Marone et al., 2001). Other studies contradict this finding where mice given
2 g of mastic gum twice daily for a week did not exhibit strong antibacterial activity
with MIC (7.8 mg/L) and MBC (31.25 mg/L) against H. pylori strains tested (
Loughlin,
Ala’Aldeen, & Jenks, 2003
). Other studies show antibacterial activity of mastic gum and
mastic oil against Staphylococcus aureus, Salmonella enteritidis, and other food-borne micro-
organisms at 0.11.5 vol./vol. oil concentrations (
Tassou & Nychas, 1995). Aqueous mastic
extracts also exhibit antifungal activity (
Ali-Shtayeh & Abu Ghdeib, 1999). Resin essential
oil was more effective against different Gram-positive bacteria, Gram-negative bacteria,
and fungi ( Candida albicans, Candida tropicalis, and Torulopsis glabrata) with MIC ranging
from 1.25 to 9 mg/mL compared to essential oil from twigs and leaves (
Magiatis, Melliou,
Skaltsounis, Chinou, & Mitaku, 1999
). Mastic gum has an MBC of 0.0710 mg/mL activity
against Gram-negative anaerobic bacteria or other microorganisms that cause oral cavities
(
Karygianni et al., 2014). They are proposed to have potential antiplaque activity
(
Takahashi et al., 2003). Different compounds are responsible for mastic gum antimicrobial
activity such as linalool and alpha-terpineol with MBC 3.05 and 2.43 mg/mL, respectively,
against E. coli (
Paraschos et al., 2011).
Apiaceae
Prangos asperula
Prangos asperula Boiss. (Farsh Al Dabe’e, Rough Prangos) belongs to the Apiaceae family
and its aerial parts are traditionally used in the Mediterranean and the Middle East coun-
tries to treat digestive disorders, dermatological problems, hemorrhoids, and blood pres-
sure problems (
Loizzo et al., 2008). It also has wound healing, antidiabetic, antimicrobial,
antiviral, and antioxidant activities (Mneimne, Baydoun, Nemer, & Arnold, 2016). P. asper-
ula grows widely in Bakish (
Loizzo et al., 2008), Ehden, Shouf, and other Lebanese high
mountains at altitudes of 12001500 m (
Bouaoun, Hilan, Garabeth, & Sfeir, 2007; Mneimne
et al., 2016
). Ethyl acetate and hexane extracts from Prangos pabularia Lindl. consist of cou-
marins, terpenoids, glycosides, pyrone derivatives, furanocoumarin derivatives, and other
compounds (
Tada et al., 2002). Alkaloids, coumarins, and terpenoids were isolated from
oils from different plant parts (roots, flowers, or fruits) of Prangos species with promising
biological activity. The essential oils from P. asperula exhibit antimicrobial activity with the
strongest activity against S. aureus (15.06 mm), followed by E. coli (11.80 mm), and
Aspergillus fumigatus (9.16 mm) using the disc diffusion method (
Mneimne et al., 2016).
Bouaoun et al. (2007) also found strong activity of the essential oil against Gram-positive
bacteria (S. aureus, S. faecalis), Gram-negative bacteria (E. coli and Salmonella typhi), and
fungi (C. albicans).
64 2. Plants used in Lebanon and the Middle East as Antimicrobials
Medicinal Plants as Anti-infectives
Asteraceae/Compositae
Matricaria species
Matricaria species are flowering plants of the family Asteraceae that includes Lac tuca
sativa L. (lettuce), Helianthus annuus L. (sunflowers), Cynara scolymus L. (artichoke), and
Matricaria recutita (L.) Rauschert (chamomiles). Matricaria are well known for their use
as herbal teas, in cosmetics, in folk medici ne, or for aromatic purposes (
Mohammad,
2011; Sharifi-Rad, Nazaruk et al., 2018
). M. recutita or Matricaria chamomilla (German
chamomile) are rich in secondary metabolites such as lactones, flavonoids, coumarins,
and phenolic compounds (
Kazemi, 2014). Different applications include using chamo-
mile for the treatment of headaches, conjunctivitis, chronic fever, inflammation, and der-
matitis (
Mahdizadeh, Ghadiri, & Gorji, 2015). Chamomile and different plants of the
Matricaria genus are also known for their antimicrobial, analgesic, and antiinflammatory
effects (
Miraj & Alesaeidi, 2016; Shoara et al., 2015; Singh, Khanam, Misra, & Srivastava,
2011
). The essential oils of these plants may help in natural preservation of food
(
Sokovi
´
c, Glamo
ˇ
clija, Marin, Brki
´
c, & van Griensven, 2010) and have an antibacterial
effect against Gram-positive and Gram-negative bac teria (
Kazemi, 2014). These oils
mainly exhibit a bacteriostatic effect against Gram-positive bacteria (
Marino, Bersani, &
Comi, 2001
).
Fabri, Nogueira, Dutra, Bouzada, and Scio (2011) studied the antimicrobial activity of
the methanolic extract of M. recutita l eaves using the broth microdilution method and
attributed this activity to the presence of phenols, tannins, triterpenoids, and flavo-
noids. However, in another study, both t he cyclohexane and ethanolic extracts of M.
chamomilla flowers did not exhibit much antibacterial activity (
Carvalho, Silva, Silva,
Scarcelli, & Manhani, 2014
). Subcritical water extracts of Matricaria species exhibit
strong antimicrobial activity (MIC 39 μg/mL) against E. coli and A. niger (Metrouh-
Amir, Duarte, & Maiza, 2015
). Both flowers and leaves of a 50% hydroalcoholic extract
of M. recutita extracts showed antimicrob ial activity of their fractionated extracts against
Pseudomonas syringae (
Mo
´
ricz et al., 2012), S. aureus,andStaphylococcus epidermidis
strains (
Jesionek et al., 2015). Stronger antibacterial activity was observed from essential
oils or extracts of Matricaria species against Gram-positive bacteria (Munir et al., 2014).
Many factors such as environmental conditions, extraction methods, and extraction sol-
vents affect the composition and biological activity of plant extracts (
Sharifi-Rad,
Nazaruk et al., 2018
). The amount of α-bisabolol in essential oi ls of Matricaria species
contributes to its antifungal (Pauli, 2006) and antibacterial activity (Mekonnen, Yitayew,
Tesema, & Taddese, 2016
).
Berberidaceae
Berberis libanotica
Berberis species (barberry) belong to the Berberidaceae family. They are spiny shrubs
present in altitudes of around 1200 m. More than 450 species exist (
Irshad, Pervaiz,
Abrar, Fahelboum, & Awen, 2013; Malik et al., 2017
) and are attributed different biolog-
ical activities such as antirheumatic and antineuralgic (
El B eyrouthy et al., 2008), anti-
cancer, antiinflammatory, antimicrobial, and antiseptic (Ali et al., 2013). They are
65Lebanese plants with antimicrobial activity
Medicinal Plants as Anti-infectives
known for the treatment of heart disease, gastrointestinal disorders, and hemorrhoids
(
Tetik, Civelek, & Cakilcioglu, 2013). Berberis libanotica Ehrenb. ex C.K.Schneid. is tradi-
tionally prepared as a decoction mixed with flour, as a maceration in alcohol, or as a
decoction in association with Geranium r obertianum L., Thymus syriacus Boiss., and
Melissa officinalis L. (
El Beyrouthy et al., 2008).
Berberis species are rich in alkaloids, phenols, and flavonoids. The major alkaloid is ber-
berine; other alkaloids are found in lower percentages such as berbamine, jatrorrhizine,
palmatine (
Ali et al., 2013). Malik et al. (2017) found a higher phenol and flavonoid content
and a lower berberine content in B. libanotica compared to Berberis aetnensis C. Presl.
Berberine isolated from Berberis heterophylla Juss. ex Poir. showed antimicrobial activity
against clinical isolates of S. aureus and different Candida species; whereas the aqueous
extract did not exhibit any activity (
Freile et al., 2003). B. libanotica methanol fractions
showed greater antioxidant activity than B. aetnensis fractions; both root extracts inhibit
acetylcholinesterase and butyrylcholinesterase activity (
Wojtunik-Kulesza, Oniszczuk,
Oniszczuk, & Waksmundzka-Hajnos, 2016
).
Cannabaceae
Humulus lupulus
Humulus lupulus L. is a flowering plant in the Cannabinaceae (hemp) family known
for its important role in the beer brewing industry (
Zanoli & Zavatti, 2008). The female
flower cones (hops) are fragrant and have a bitter flavor. They provide aromatic, medi-
cal, antimicrobial, and preservative qualities due to their polyphenolic and acyl phloro-
glucides content (
Moir, 2000; Morcol, Negrin, Matthews, & Kennelly, 2020). The flowers
are used as a dye source, food flavoring, perfume, spice, and to make beer or other bev-
erages. Traditionally, H. lupulus flowers are known for their effect in treating sleep dis-
turbances; however, this sedative activity was not clinically proven. Native American
tribes used hop s as a sedative, analgesic, antirheumatic, and as an antiinflammatory
agent (
Zanoli & Zavatti, 2008). Many studies report the antibacterial and antifungal
activity of essential oils or extracts from H. lupulus flowers, leaves, and seeds (
Abram
et al., 2015; Nionelli, Pontonio, Gobbetti, & Rizzello, 2018
). A stronger antifungal a ctivity
was observed from hop cone extract against Penicillium and Aspergillus strains ( Alonso-
Esteban et al., 2019; Nionelli et al., 2018
). Hop seed extracts gave strong antibacterial
activity with MICs ranging from 0.01 mg/mL against B. cereus and 0.15 mg/mL against
E. coli and Salmonella typhimurium (
Alonso-Esteban et al., 2019). Different active com-
pounds from hops such as humulone and lupulone (
Oshugi et al., 1997; Simpson & Smith,
1992; Teuber & Schmalreck, 1973; Zanoli & Zavatti, 2008
) exhibit antibacterial (mostly against
Gram-positive bacteria) and antifungal activity (
Mizobuchi & Sato, 1984). Xanthohumol was
also found to have a wide antimicrobial and antiviral activity (
Gerhauser, 2005). Hop cone
extracts, mainly lupulone and xanthohumol, exhibit antibacterial (
Yamaguchi, Satoh-
Yamaguchi, & Ono, 2009
) and antibiofilm activity against different Staphylococcus species with
different profiles of resistance (
Bogdanova et al., 2018). Abram et al. (2015) suggest that other
compounds such as catechins present in hop extracts may be responsible for antimicrobial activ-
ity against S. aureus (MIC, 0.003 mg/mL).
66 2. Plants used in Lebanon and the Middle East as Antimicrobials
Medicinal Plants as Anti-infectives
Cistaceae
Cistus species
Cistus species are perennial shrubs, native to the Mediterranean area that are known
in folk medicine for their role against different disorders and as antiinfective agents
(
Bouamama, Noe
¨
l, Villard, Benharref, & Jana, 2006; Ustu
¨
n, Ozc¸ elik, Akyo
¨
n, Abbasoglu, &
Yesilada, 2006
). Decoctions from plant leaves, flowers, or aerial parts are an effective rem-
edy against microbial infections (
Bassole
´
& Juliani, 2012; Salin et al., 2011; Viapiana,
Konopacka, Waleron, & Wesolowski, 2017; Zidane et al., 2013
), skin inflammations (Leto,
Tuttolomondo, La Bella, & Licata, 2013
), pain, constipation, rheumatism, snakebites,
wounds, urinary diseases, and disorders (
Gu
¨
rdal & Ku
¨
ltu
¨
r, 2013). A survey in Kos, a
Greek Mediterranean island where most of Hippocrates medical practices were derived
shows that at higher altitudes Cistus salviifolius L. and Teucrium capitatum L. were the most
commonly encountered species (
Leto et al., 2013). Both plants are rich in a volatile sesqui-
terpene, germacrene D that has both antibacterial and cytotoxic activities (
Barrajo
´
n-
Catala
´
n et al., 2011; Leto et al., 2013
). However, even within the same plant species,
the difference in the fruiting stage, climatic and soil conditions lead to differences in
the main sesquiterpene hydrocarbons. Germacrene D was the dominant essential oil found
in C. salviifolius in Sicily, camphor in Spain and Greece (
Demetzos, Angelopoulou, &
Perdetzoglou, 2002; Morales-Soto et al., 2015
), and β-damascenone in Sardinia (Mastino,
Marchetti, Costa, & Usai, 2017
).
C. salviifolius is traditionally used as a tea substitut e, ointment, or as a cicatrizing or
astringent agent. The antibacterial activity of C. salviifolius is not only related to its essen-
tial oils or terpenes (
Gertsch, 2011; Gu
¨
venc¸ et al., 2005; Morales-Soto et al., 2015) but also
to its polyphenolic compounds. Antimicrobial activity against Gram-negative and Gram-
positive bacteria are reported from organic solvent extracts derived from Cistus creticus
L. (
Gu
¨
venc¸ et al., 2005) and Cistus ladanifer L. (Ferreira et al., 2012) or aqueous extracts
derived from Cistus populifolius L. and C. ladanifer (
Barrajo
´
n-Catala
´
n et al., 2011). Aqueous
extracts from C. salviifolius exhibit strong antibacterial or bacteriostatic activity against
S. aureus that may be attributed primarily to polar compounds and to other flavonols,
whereas inhibitory activity against E. coli may be linked to flavonols and galloylated flava-
nols (
Toma
´
s-Menor et al., 2013). C. salviifolius, C. populifolius, Cistus laurifolius L., C. ladani-
fer, and Cistus monspeliensis L. have strong antifungal activity with a MIC of 0.625 mg/mL
(
Karim et al., 2017). In addition to their antibacterial and antifungal properties, Cistus
species also have antiviral, antiparasitic, and insecticidal activities (Hutschenreuther,
Birkemeyer, Gro
¨
tzinger, Straubinger, & Rauwald, 2010; Morales-Soto et al., 2015; Verdeguer,
Bla
´
zquez, & Boira, 2012
).
Conifers
Conifers are mostly evergreen woody plants with around 630 species worldwide. In
Lebanon, there are 10 indigenous conifer species (from five genera) (
Talhouk, Zurayk, &
Khuri, 2001
) and others were imported to Lebanon for ornamental purposes such as
Cupressus macrocarpa (Hartw.) D.P.Little (goldcrest). Cedrus libani A. Rich. is the national
emblem of Lebanon and its wood was used since ancient times in building of temples and
67Lebanese plants with antimicrobial activity
Medicinal Plants as Anti-infectives
boats (Chaney & Basbous, 1978). Egyptians used Cedrus libani essential oils for mummifica-
tion. Conifers play an important part in Lebanese folk medicine. Abies cilicica (Antoine &
Kotschy) Carrie
`
re was used in folk medicine in Lebanon for the treatment of rheumatism
and in Turkey for the treatment of bronchitis, gastrointestinal disease s, and asthma
(
Sargin, 2015). Cupressus sempervirens L. f. horizontalis (Mill.) Voss is known as antiasth-
matic, antitussive, and antirheumatic; while Juniperus excelsa M. Bieb. and J. oxycedrus L.
are known as antirheu matic and antineuralgic (
El Beyrouthy et al., 2008). Different
Lebanese conifer essential oils, harvested in Lebanon, were tested for their antimicrobial
activity against different fungi and bacteria. The MICs of conifer essentials oils were deter-
mined against a range of bacteria and fungi resp onsible for skin infections using the broth
microdilution technique. The essential oils from J. oxycedrus, J. excelsa, and C. libani show
strong activity against S. aureus (MIC of 64 μg/mL). Dermatophyte species were sensitive
(MIC values 3264 μg/mL) to essential oils from C. sempervirens, A. cilicica, J. excelsa,
C. libani, J. oxycedrus, and C. macrocarpa (
Fahed et al., 2017).
Lamiaceae
An ethnopharmacological study to compare traditional medicinal plants in Turkey
(Marmaris district) and the Mediterranean countries reveals the presence of 64 medicinal
plant species (from 35 families) and the use of nine essential oils. Many of the commonly
used traditiona l plants belong to the Lamiaceae (13 species) and Asteraceae (four species)
families. Some of the reported commonly used medicinal plants are Salvia fruticosa Mill.
(mostly its essential oils), Origanum onites L., Mentha pulegium L., Lavandula stoechas L., and
Satureja thymbra L. Other medicinal plants that are endemic to Lebanon, Syria, and Turkey
include Sideritis libanotica (Benth.) Bornm and Thymus cilicicus Boiss. & Bal. (
Gu
¨
rdal &
Ku
¨
ltu
¨
r, 2013
).
The Lamiaceae family is a large family with around 7886 species (245 genera) with valu-
able secondary metabolites that have attracted different industries (
Bekut et al., 2018;
Khoury, Stien, Eparvier, Ouaini, & El Beyrouthy, 2016
). They are utilized in the food, phar-
maceutical, and cosmetic industries. Although the Lamiaceae family is distributed glob-
ally, a large concentration of these plants is found in the Mediterranean region. Some
are used as ornamentals (Ajuga, Salvia, and Coleus) and others as culinary herbs such as
thyme (Thymus), sage (Salvia), mint (Mentha), rosemary (Rosmarinus), oregano or marjoram
(Origanum), lavender (Lavandula), and basil (Ocimum). Around 136 species (29 genera) of
Lamiaceae species are found in Lebanon (
El Beyrouthy, Dhifi, & Arnold, 2013). Many are
used in the Lebanese cuisine in salads such as S. fruticosa, Rosmarinus officinalis L., Thymbra
spicata L. (
Bozkurt, 2006; Eruygur, C¸ etin, Ata¸s, & C¸ evik, 2017), and Coridothymus capitatus
(L.) Reichenb. fil. Others are mixed with cheese (Thymus and Origanum) to form
“Shanklish” or used to form “manakeesh” a baked dough with a mixture of thyme herbs
on the top (Origanum syriacum L., S. thymbra, and T. spicata) in addition to Rhus coriaria
Linn. (sumac) and sesame seeds (
Khalil et al., 2019; Khoury et al., 2016). Other indigenous
Lamiaceae species widely used in Lebanese folk medicine include the genera Salvia,
Rosmarinus, Satureja, Origanum, Thymus, Lavandula, Melissa, and Mentha (
Khoury et al.,
2016). The essential oils of these plants and different extracts (methanol, ethanol, and other
68 2. Plants used in Lebanon and the Middle East as Antimicrobials
Medicinal Plants as Anti-infectives
solvent extracts) are widely used in Lebanese folk medicine (El Beyrouthy et al., 2008,
2013; El Beyrouthy, 2009
). Khoury et al. (2016) tested the antimicrobial activity of the essen-
tial oils of 11 Lamiaceae species against standard strains of S. aureus (Gram-positive), E. coli
(Gram-negative), C. albicans (yeast), and Trichophyton rubrum (dermatophyte clinical isolate).
T. spicata, S. thymbra, C. capitatus, L. stoechas,andO. syriacum exhibited antimicrobial activity.
The amount of carvacrol and thymol (
Marchese et al., 2016) in the essential oils positively
correlated with the antimicrobial activity (
Khoury et al., 2016).
Phlomis species
Another member of the Lamiaceae family, the Phlomis genus is also known for its culi-
nary usages and biological activity. Its essential oils, flavonoids, phenylethyl alcohol, and iri-
doids contribute to different pharmacological activities. Extracts are used in the treatment of
gastric ulcer, diabetes, hemorrhoids, wounds, and inflammation (
Amor et al., 2009). Phlomis
is part of a very popular traditional herbal tea mixture in Lebanon and Syria. It is commonly
known as “Zhourat” or “Zahraa” and it consists of dried flowers or leaves of different
plants including Phlomis syriaca Boiss. (leaves and flowers), Rosa damascena Mill. (flowers),
Aloysia citrodora Pala
´
u(leaves),Zea mays L. (flowers), M. chamomilla (flowers), Elaeagnus
angustifolia L. (flowers and leaves), Micromeria myrtifolia Boiss. & Hohen (aerial parts), and
other herbs (
Carmona, Llorach, Obon, & Rivera, 2005; Obo
´
n, Rivera, Alcaraz, & Attieh,
2014
). It is believed that the mixture has stronger antioxidant activity (Guimara
˜
es, Barros,
Carvalho, & Ferreira, 2011
) and acts as an effective treatment for colds and bronchitis
(
Baydoun et al., 2015). Essential oils and methanol extracts from different Phlomis species
exhibit antibacterial effects against S. aureus, E. coli, Klebsiella pneumonia, and other patho-
genic bacteria (
Morteza-Semnani, Saeedi, Mahdavi, & Rahimi, 2006).
Cyclotrichium species
Cyclotrichium genus is a member of the Lamiaceae family used as spices in different
food recipes and well known in the traditional folk medicine (
Formisano, Oliviero, Rigano,
Saab, & Senatore, 2014
). It is an aromatic plant, with a mint-like smell, endemic to
Lebanon, Syria, Turkey (
O
¨
zdemir et al., 2017), Iraq, and Iran (Tepe, Sokmen, Sokmen,
Daferera, & Polissiou, 2005). Cyclotrichium origanifolium (Labill.) Manden. & Scheng (men-
thol) and M. myrtifolia essential oils have different activities such as antipyretic, antifungal,
and antibacterial activities (
Formisano, Mignola, et al., 2007; Formisano, Rigano, et al.,
2007
). C. origanifolium essential oils exhibit the strongest antibacterial activity (MIC
0.068 mg/mL) followed by nonpolar solvent extracts; whereas the polar extracts (aque-
ous and ethanol extracts) did not exhibit antimicrobial activity (
Tepe et al., 2005). C. origa-
nifolium essential oils are rich in pulegone, menthone, and limonene. The me thanol extract
had the strongest free radical scavenging activity (
Tepe et al., 2005).
Salvia species
Salvia species constitute around one-quarter of the Lamiaceae family and are highly
diverse with over 900 species worldwide (
Kamatou, Makunga, Ramogola, & Viljoen,
2008
). Some Salvia species are popular as aromatic herbs, essential oils, medicinal plants,
ornamental plants, or as food due to their good flavors. Commonly used Salvia species
in the food market include Salvia officinalis L. (common sage), Salvia hispanica L. (chia),
69Lebanese plants with antimicrobial activity
Medicinal Plants as Anti-infectives
Salvia sclarea L. (clary sage), Salvia miltiorrhiza Bunge (danshen), and Salvia lavandulifolia
Vahl (Spanish sage) (
Sharifi-Rad, Ozcelik, et al., 2018). Other economically important spe-
cies such as Salvia fruticosa Mill., Salvia tomentosa Mill., and Salvia verbenaca L. are known
for their biological activities such as antimicrobial, antioxidant , antiplasmodial, anticancer,
antipyretic, antinociceptive, antihyperglycemia, skin curative agents, and help against the
loss of memory. They are also used in the treatment of the common cold, tonsillitis, men-
strual pain, abdominal pain, and nausea (
Bulut, Haznedaro
˘
glu, Do
˘
gan, Koyu, & Tuzlacı,
2017; Gu
¨
rdal & Ku
¨
ltu
¨
r, 2013; Kamatou et al., 2008; Sharifi-Rad, Ozcelik, et al., 2018; Zengin
et al., 2019
).
In South Africa, sages form a fundamental part of traditional healing especially in the
treatment of malaria, microbial infections, inflammation, and disinfection (
Kamatou
et al., 2008
). Salvia africana-lutea L. leaves, fruits, or flowers are prepared fresh or dried as
herbal tea mixtures for the traditional treatment of c olds, bronchitis, or tuberculosis
(
Kamatou et al., 2008; Ulubelen, Topcu, & Johansson, 1997). Salvia africana-caerulea L. and
other Salvia species are also used in the treatment against the flu (
Kamatou et al., 2008).
The leaves of Salvia repens Burch. ex Benth. can be used to treat sores (by adding to a
bath), root decoctions can help in the treatment of diarrhea, and the smoke (due to burn-
ing of plants or leaves) can help in the disinfection of a room or to repel insects. In
Europe, Salvia runcinata Benth. decoctions are used for the treatment of allergies
(
Kamatou et al., 2008). The Chinese S. miltiorrhiza, used for treating heart disease,
achieved around 205 million USD in the global market in 2008 (
Jia, Huang, Zhang, &
Leung, 2012
). Though many Salvia species are cultivated in different locations, around
250 species are endemic to Central Asia and the Mediterranean (
Walker, Sytsma,
Treutlein, & Wink, 2004
). S. fruticosa is endemic to the Eastern Mediterranean basin
(
Sharifi-Rad, Ozcelik, et al., 2018).
Salvia species are rich in different bioactive compounds such as terpene derivatives,
essential oils, phenolic compounds, flavonoids, and tannins (
Bahadori, Eskandani, De
Mieri, Hamburger, & Nazemiyeh, 2018; Sharifi-Rad, Ozcelik, et al., 2018
). Different reviews
and papers discuss terpenoids isolated from Salvia and relate them to the plant’s bioactive
properties (
Jash, Gorai, & Roy, 2016; Sharifi-Rad, Ozcelik, et al., 2018). Many of these com-
pounds from Salvia are attributed antimicrobial activities. An abietane diterpene, galdosol
(from Salvia canariensis L. aerial parts) exhibits antibacterial activity against S. aureus,
Bacillus subtilis, and Micrococcus luteus (
Gonza
´
lez et al., 1989). Ethanolic extracts from aerial
parts and roots of S. fruticosa, Salvia cilicica Boiss., S. officinalis, and S. tomentosa exhibit
antifungal activity. Essential oils from S. fruticosa had a MIC of 256 and 512 μg/mL against
T. rubrum and C. albicans, respectively (
Khoury et al., 2016; Sharifi-Rad, Ozcelik, et al.,
2018
). Essential oils from S. officinalis exhibit antimicrobial activity against C. albicans,
E. coli, and S. aureus (
Cutillas, Carrasco, Martinez-Gutierrez, Tomas, & Tudela, 2017).
Three terpenoids from Salvia multicaulis Vahl exhibit activity against tuberculosis
(
Ulubelen et al., 1997). Different antibacterial and antiplasmodial compounds have been
isolated from Salvia chamelaegnea Berg., Salvia radula Benth., and S. verbenaca. Carnosol,
oleanolic acid, 7-O-m ethylepirosmanol, and ursolic acid isolated from Salvia species or
other members of the Lamiaceae family exhibit antimicrobial activities (
Kamatou, Van
Vuuren, Van Heerden, Seaman, & Viljoen, 2007
). Ursolic acid and carnosol were also iso-
lated from Rosmarinus officinalis (
Kamatou et al., 2008).
70 2. Plants used in Lebanon and the Middle East as Antimicrobials
Medicinal Plants as Anti-infectives
Rosmarinus officinalis
Rosmarinus officinalis L. commonly known as Rosemary is a perennial herb that belongs
to the Lamiaceae family. Its secondary metabolites are attributed to different biological
activities such as antibacterial (
Bozin, Mimica-Dukic, Samojlik, & Jovin, 2007), antiinflam-
matory, antinociceptive (
De Melo et al., 2011; Este
´
vez, Ramı
´
rez, Ventanas, & Cava, 2007;
Gonza
´
lez-Trujano et al., 2007
), antimutagenic (Tajehmiri, Ghasemi, Sabet, Chakoosari, &
Abdolahzadegan, 2014
), antioxidant (Ra
ˇ
skovi
´
c et al., 2014), hepatoprotective (Abdel-
Wahhab, El-Shamy, El-Beih, Morcy, & Mannaa, 2011
), antidiabetic (Bakırel, Bakırel, Kele¸s,
U
¨
lgen, & Yardibi, 2008
), and anticancer (Moore, Yousef, & Tsiani, 2016; Ngo, Williams, &
Head, 2011
). Some of the main bioactive compounds in rosemary are rosmarinic acid, caf-
feic acid, carnosic acid, carnosol, and triterpenoid acids (
Ngo et al., 2011).
Thymol/carvacrol rich species
Essential oils from Thymus vulgaris L. and other thyme species exhibit bacteriostatic
effect against both Gram-positive and Gram-negative bacteria (
Alibi et al., 2020; Marino,
Bersani, & Comi, 1999; Rota, Herrera, Martı
´
nez, Sotomayor, & Jorda
´
n, 2008
). The essential
oils of T. vulgaris exhibit strong antibiofilm, antimicrobial, antiquorum sensing, and antiox-
idant activities. The inhibition diameter zone was greater than 20 mm for 85.71% of 105
multidrug-resistant strains tested (
Alibi et al., 2020). Thymol (2-isoprop yl-5-methylphenol)
showed the strongest inhibitory activity compared with carv acrol, eugenol, trans-cinnamic
acid, and others with MIC 1.0 and 1.2 mmol/L against S. typhimurium and E. coli, respec-
tively (
Olasupo, Fitzgerald, Gasson, & Narbad, 2003). Similarly, thymol from essential oil
of Thymus syriacus Boiss. also exhibited antibacterial activity against different Gram -
negative bacteria (
Al-Mariri, Swied, Oda, & Al Hallab, 2013). Thymol showed antibacterial
activity against S. aureus and S. epidermidis clinical isolates with different profiles of resis-
tance with MIC 0.03%0.06% vol./vol. using the agar dilution method (
Nostro et al.,
2004
). Gram-positive strains (MIC 0.31 mg/mL against S. aureus) were more sensitive than
Gram-negative strains (MIC 5.00 mg/mL against E. coli) as shown using the microdilution
method (
Trombetta et al., 2005). The activity of thymol may be through affecting the integ-
rity of the lipid membrane. Different reviews on the antibacterial and antifungal effects of
thymol are found in the literature (
Marchese et al., 2016). Chloroform and methanol
extracts of T. syriacus exhibit antimycobacterial activity with MIC 6.3 and 50 μg/mL,
respectively (
Askun, Tumen, Satil, Modanlioglu, & Yalcin, 2012; Jurno, Netto, Duarte, &
Machado, 2019
). Thymus leucotrichus Hala
´
csy methanol and acetone extracts and T. syriacus
essential oil showed activity against verocytotoxigenic E. coli strains (
Al-Mariri & Safi,
2014; Nabavi et al., 2015; Ulukanli, Cigremis, & Ilcim, 2011
).
Za’atar plants: Satureja thymbra; Origanum syriacum
Different plant species from the Lamiaceae family are referred to in the Arab world by
the name “za’atar.” These plants are known for their aromatic flavor, culinary uses,
and folk medicine preparations (
Ali-Shtayeh, Yaghmour, Faidi, Salem, & Al-Nuri, 1998).
“Za’atar” includes Satureja thymbra L., Origanum syriacum L. (white oregano), C. capitatus,
and T. spicata (
Shehadeh et al., 2019). S. thymbra Lamiaceae grows wild in the
Mediterranean area and is also cultivated for commercial use. It has different antibacterial
71Lebanese plants with antimicrobial activity
Medicinal Plants as Anti-infectives
activity due to its essential oils (Azaz, Ku
¨
rkcu
¨
oglu, Satil, Baser, & Tu
¨
men, 2005;
Chorianopoulos et al., 2006; Markovi
´
c et al., 2011
) and its phenolic compounds (Skoula,
Grayer, & Kite, 2005
). The combination of essential oils and phenolic extracts was shown
to have both antibacterial and antioxidant activity and thus decrease lipid auto-oxidation
in fish coating material (
Choulitoudi et al., 2016).
Origanum syri acum is a perennial herbaceous wild plant that is native to the
Mediterranean region. It has white aromatic flowers and hairy leaves with a strong taste.
It is widely used in folk medicine in Lebanon, Syria, Palestine, and Jordan for the treat-
ment against microbial infections, throat pain, abdominal pain, or other disorders
(
Aburjai, Hudaib, Tayyem, Yousef, & Qishawi, 2007; Ali-Shtayeh et al., 2000; Husein et al.,
2014; Shehadeh et al., 2014; Shehadeh, Suaifan, & Darwish, 2017
). Origanum species essen-
tial oils and different solvent extracts exhibit antimicrobial, anticancer, and antioxidant
activity (
Abdel-Massih, Fares, Bazzi, El-Chami, & Baydoun, 2010; Al Hafi et al., 2016;
Benelli et al., 2019; El Gendy et al., 2015; Khoury et al., 2016; Loizzo et al., 2009; Viuda-
Martos et al., 2010
). O. syriacum from different regions in Palestine show MIC with moder-
ate activity (MIC 9725000 μg/mL) against five standard bacterial strains. Higher
lipophilic content or hydrophilic (thymol-rich) essential oils led to increased antibacterial
activity against Gram-positive bacteria. However, increase in carvacrol led to stronger
inhibitory activity against both Gram-positive and Gram-negative bacteria (
Saidi,
Ghafourian, Zarin-Abaadi, Movahedi, & Sadeghifard, 2012; Shehadeh et al., 2019
). The
antimicrobial activity of essential oils of O. ehrenbergii Boiss. and O. libanoticum Boiss.
(endemic to Lebanon) and O. syriacum (endemic to the Levantine) is affected by carvacrol
content. O. ehrenbergii (60.8% carvacrol) and O. syriacu m (79% carvacrol) showed moderate
antimicrobial activity (MIC 4001200 μg/mL), whereas O. libanoti cum (0% carvacrol) was
inactive against yeast and pathogenic bacteria tested (
Al Hafi et al., 2016).
Different Lamiaceae genera
The concentration of different compounds in extracts or essential oils derived from
members of the Lamiaceae family (Origanum, Satureja, Thymbra, Phlomis) vary with envi-
ronmental conditions (
Baydar, Sa
˘
gdic¸, O
¨
zkan, & Karado
˘
gan, 2004; Kizil, 2010; Miguel
et al., 2004
), soil characteristics (Economou et al., 2014), extraction procedure, and develop-
mental stage at the time of collection (Zhang & Wang, 2008). Among 27 indigenous
Lebanese plants, methanol extracts of nine herbs show antimicrobial activity $ 88.8%
using the disk diffusion method. O. libanoticum (whole plant) and Verbascum leptostychum
DC. (flower extracts) show 99.9% inhibition. Stronger antimicrobial activity was detected
in the methanol extract compared to the water extracts of the tested traditional medicinal
plants (
Barbour et al., 2004). The methanolic extract from O. libanoticum had a MIC of 1:2.5
against E. coli and a MIC of 1:3.5 against Shigella dysenteriae and Proteus species (
Barbour
et al., 2004
). O. libanoticum, Origanum majorana L., and Origanum vulgare L. also exhibit
antifungal activity (
El Gendy et al., 2015; Waller et al., 2017).
Thymbra spicata
To prevent multiplication of foodborne bacteria, leafy parts of plants such as thyme,
savory, and oregano are traditionally added to meat and food products to extend their
shelf life (
Sa
˘
g
˘
gdıc¸&O
¨
zcan, 2003). Hydrosols from 15 spices were tested for antibacterial
72 2. Plants used in Lebanon and the Middle East as Antimicrobials
Medicinal Plants as Anti-infectives
activity to study their potential as food preservatives, and only anise (Pimpinella anisum
L.), cumin (Cuminum cyminum L.), oregano (O. vulgare), summer savory (Satureja hortensis
L.), and black thyme (T. spicata) exhibited activity (
Sa
˘
gdıc¸&O
¨
zcan, 2003). T. spicata essen-
tial oils (75.5% carvacrol) exhibited stronger antibacterial activity compared to other
Lamiaceae species such as Origanum minutiflorum Schwarz & Davis (wild oregano;
endemic to Turkey), Satureja cuneifolia Ten. (wild savory), and O. onites (oregano). The anti-
bacterial activity may be primarily due to carvacrol and to the hydrocarbons (c-terpinene
and p-cymene) present in its essential oils. The essential oils from T. spicata were the most
active (among those tested) as seen using paper disc diffusion method where the 1/50
solution (in ethanol) inhibited most strains tested (
Baydar et al., 2004). Other studies show
antimicrobial activity of T. spicata decoction and hydrosols against different bacteria and
fungi (
Kivanc & Akgu
¨
l, 1988; O
¨
zcan & Boyraz, 2000; Sa
˘
gdıc¸&O
¨
zcan, 2003; Sa
˘
gdic¸, Ku¸sc¸u,
O
¨
zcan, & O
¨
zc¸elik, 2002; Saidi et al., 2012
). T. spicata is used as a “healthy plant” in
Lebanon due to its antimicrobial potential (
Bozkurt, 2006; Eruygur et al., 2017). It is rich
in phenolic compounds such as rosmarinic acid, carvacrol (
Stefanaki, Cook, Lanaras, &
Kokkini, 2018
), thymol, and flavonoids (Dorman, Bachmayer, Kosar, & Hiltunen, 2004;
Hanci, Sahin, & Yilmaz, 2003
). Eruygur et al. (2017) compared water extracts from leaves
and flowers of T. spicata (prepared as the traditional infusion me thod) with ethanol
extracts. Although ethanol extracted more compounds and had stronger antioxidant activ-
ity (mainly due to higher carvacrol content), the aqueous extract had more rosmarinic
acid content and wound-repair ability (
Eruygur et al., 2017). Both phenol and flavonoid
compounds are recognized for their antimicrobial activity; however, phenols seem to con-
tribute to stronger activity. A negative correlation was obtained using Spearman’s rho test
between minimal inhibitory concentration and the pres ence of these active compounds
after screening methanolic extracts of 21 medicinal plants in Spain (
Stankovi
´
c, Radi
´
c,
Blanco-Salas, Va
´
zquez-Pardo, & Ruiz-Te
´
llez, 2017). The methanol extracts of T. spicata
exhibited strong antimycobacterial activity against Mycobacterium tuberculosis (MIC 196 μg/
mL) and moderate activity against S. typhimurium, E. coli, S. epidermidis, and Enterobacter
aerogenes (
Askun, Tumen, Satil, & Ates, 2009). Crude methanol extracts of different plants
have higher antimicrobial activity than aqueous extracts as reported in the literature
(
Askun et al., 2009; Parekh, Jadeja, & Chanda, 2005). These extracts are rich in flavonoids,
alkaloids, glycosides, amino acids, phytosterols, tannins, triterpenoids, saponins, and ster-
oids (
Abdel-Wahhab et al., 2011; Kumar et al., 2009).
Myrtaceae
Eucalyptus species
The genus Eucalyptus belongs to the Myrtaceae family and consists of around 900 spe-
cies (
Gilles, Zhao, An, & Agboola, 2010; Tyagi & Malik, 2011). Eucalyptus is well known
worldwide as a source of fiber (for paper production) and for its medicinal properties
(
Luı
´
s et al., 2016). Its essential oils are known in folk medicine for their antifungal, antibac-
terial, analgesic, and antiinflammat ory properties (
Bussmann et al., 2010; Elaissi et al.,
2011; Mulyaningsih, Sporer, Zimmermann, Reichling, & Wink, 2010; Navarro, Villarreal,
Rojas, & Lozoya, 1996; Salari, Amine, Shirazi, Hafezi, & Mohammadypour, 2006; Silva
73Lebanese plants with antimicrobial activity
Medicinal Plants as Anti-infectives