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Eur J Oral Sci 2020; 1–11 © 2020 The Authors.

© 2020 The Authors. Eur J Oral Sci published by John Wiley & Sons Ltd
DOI: 10.1111/eos.12745 European Journal of
Printed in Singapore. All rights reserved
Oral Sciences

Review article
Effect of essential oils on oral Dorota Dobler , Frank Runkel,
Thomas Schmidts
Institute of Bioprocess Engineering and

halitosis treatment Pharmaceutical Technology, Technische


Hochschule Mittelhessen - University of
Applied Sciences, Giessen, Germany

Dorota Dobler, Institute of Bioprocess


Dobler D, Runkel F, Schmidts T. Effect of essential oils on oral halitosis treatment. Engineering and Pharmaceutical Technology,
Eur J Oral Sci. 2020; 00: 1–11. © 2020 The Authors. Eur J Oral Sci published by Technische Hochschule Mittelhessen -
John Wiley & Sons Ltd University of Applied Sciences, Wiesenstr. 14,
D-35390 Giessen, Germany
Halitosis is a very common condition which may affect up to 30% of the popula-
tion. In about 90% of the cases, halitosis originates in the mouth due to inadequate E-mail: Dorota.Dobler@lse.thm.de
plaque control, periodontal disease, dry mouth, faulty restorations, and in particular
due to excessive bacterial growth. Oral malodor is mainly caused by a microbial Key words: essential oils; halitosis; sulfur-
degradation of amino acids into volatile, bad-smelling gases (volatile sulfur com- reducing bacteria
pounds – VSCs). Management of oral malodor is directed primarily at managing This is an open access article under the
and reducing the VSC-producing bacteria count as well as masking the odor. Essen- terms of the Creative Commons Attribution
tial oils have been used for this purpose in traditional medicine for centuries. In the License, which permits use, distribution and
present review, data on the antimicrobial activity of essential oils against relevant reproduction in any medium, provided the
oral VSC-producing bacteria are compiled and compared. Additionally, other posi- original work is properly cited.
tive aspects of essential oils with regard to oral odor are considered. Accepted for publication October 2020

Halitosis is a general term used to define an unpleasant the data, the most common bacteria occurring in hali-
or offensive odor emanating from the mouth, which tosis patients are Porphyromonas gingivalis, T. forsythia,
originates from oral or non-oral sources (1,2). It is a Fusobacterium nucleatum, Prevotella intermedia and
very common problem and moderate chronic halitosis Treponema denticola (9,10). Furthermore, it is observed
affects up to 50% of the population independent of that persons with T. forsythia in their saliva have a
periodontal diseases (3). In about 90% of the cases, higher level of VSCs in their breath compared to sub-
halitosis originates in the mouth due to inadequate pla- jects without these bacteria (9). The other species that
que control, periodontal disease, dry mouth, faulty produces VSCs and is found only in persons with hali-
restorations, and in particular due to excessive bacterial tosis is Solobacterium moorei (10). However, no obvious
growth. Oral malodor is mainly caused by a microbial association between halitosis and any specific bacterial
degradation of amino acids into volatile, bad-smelling genus has been found. Halitosis may therefore be more
gases (volatile sulfur compounds – VSCs), such as the result of complex interactions between several bac-
hydrogen sulfide (H2S), methyl mercaptan, dimethyl terial species (5,11).
sulfide, dimethyl disulfide, and sulfur dioxide (1). Due
to the topography of the tongue, the anaerobic bacte-
rial groups especially favor colonization of the tongue
Treatment of halitosis using essential oils
and thus play an important role in oral malodor forma-
tion (4,5). Although oral malodor is not directly caused Among the methods for treatment of halitosis are prod-
by periodontal disease, it has been suggested that peri- ucts that (i) chemically and mechanically reduce the
odontal disease contributes to an increased tongue number of microorganisms, (ii) mask the odor, and (iii)
coating and higher production of volatile sulfur com- chemically neutralize VSCs (12). The most effective
pounds (6). Among the cultivable oral bacteria, the method is the reduction of VSC-producing bacteria. In
most active producers of hydrogen sulfide in vitro are recent years, there has been a growing interest in the
Treponema denticola, Porphyromonas gingivalis, Porphy- research and development of new antimicrobial agents
romonas endodontalis, Prevotella intermedia, and Bac- from natural sources. Essential oils are of special inter-
teroides loescheii (7). Other bacterial species associated est as they are a mixture of multifarious chemical sub-
with periodontal disease, such as Enterobacteriaceae, stances that belong to different chemical families,
Tannerella forsythia, Centipeda periodontii, Eikenella including terpenes, aldehydes, alcohols, esters, pheno-
corrodens, and Fusobacterium periodonticum, also have lics, ethers, and ketones (13). The antimicrobial impact
a high capability to generate VSCs in vitro (7,8). In of essential oils and their chemical components has
recent years, VSC-producing bacteria have become been investigated by several research groups in the past
quantifiable using polymerase chain reaction. Based on (14,15). The antibacterial activity of essential oils seems
2 Dobler et al.

to be mainly achieved by the destruction of the cell Table 1


membrane. Increased membrane permeability may lead Summary of published MIC values of essential oils tested on
to a loss of vital intracellular components such as pro- several VSCs producing bacteria strains
teins, sugars, ATP and DNA, while decreasing the pro-
duction of ATP and thereby leading to cell damage Bacterial MIC value µg/ml
accompanied by leakage of electrolytes (16,17). In gen- Essential oil strain (reference number)
eral, gram-negative bacteria are more resistant to essen- Aloysia gratissima P. gingivalis 125 (27)
tial oils than gram-positive bacteria (18). Commonly F. nucleatum 125 (27)
used essential oils are thyme oil, eucalyptus oil and Aloysia triphylla P. gingivalis 250 (27)
peppermint oil. Accordingly, a number of mouth-rins- F. nucleatum 125 (27)
ing solutions based on essential oils are available. The Alpinia speciose P. gingivalis 125 (27)
best known is Listerine, which contains eucalyptol F. nucleatum 125 (27)
Artemisia Capillaris P. gingivalis 200 (76)
(0.092%), menthol (0.042%), methyl salicylate F. nucleatum 100 (76)
(0.060%) and thymol (0.064%) as active ingredients. P. intermedia 25 (76)
Eucalyptol acts as an antibacterial and anti-fungal Artemisia feddei P. gingivalis 100 (75)
agent, thymol has antiseptic properties, and menthol is F. nucleatum 25 (75)
known for its local anesthetic and counterirritant activ- P. intermedia 25 (75)
ity. Multiple studies confirmed the positive effect of Lis- Baccharis P. gingivalis 125 (27)
dracunculifolia F. nucleatum 125 (27)
terine as a treatment for halitosis (19–23).
Callitris glaucophylla P. gingivalis 2000 (80)
Although many studies highlight the antimicrobial (White cypress oil)
activity of essential oils against oral bacteria, investiga- Chrysanthemum P. gingivalis 100 (77)
tions mostly focus on non-VSC-producing species such indicum F. nucleatum 200 (77)
as Staphylococcus spp. In the present review, data on P. intermedia 200 (77)
the antimicrobial activity of several essential oils Cinnamomum P. gingivalis 630 (67), 6.25 (68), 2000
zeylanicum (80), 250 (27), 250 (83)
against relevant oral VSC-producing bacteria are com-
(Cinnamon oil) F. nucleatum 420 (67), 250 (27), 125
piled and compared. Table 1 summarizes the minimum (83)
inhibitory concentration (MIC) values of essential oils S. moorei 414 (69)
tested on several VSC-producing bacteria which are Commiphora myrrha P. gingivalis 250 (83)
described in the literature. Additionally, other positive F. nucleatum 250 (83)
aspects of essential oils with regard to oral odor are S. moorei 6250 (69)
taken into account. These include anti-inflammatory Coriandrum sativum P. gingivalis 125 (27)
(Coriander oil) F. nucleatum 15 (27)
and antioxidant properties as well as the potential S. moorei 1350 (69)
impact on relevant clinical parameters linked to mouth Croton cajucara P. gingivalis 31.2 (82)
health status and gingival inflammation: plaque index Cryptomeria japonica P. gingivalis 25 (74)
(PI) and gingival index (GI). F. nucleatum 50 (74)
P. intermedia 50 (74)
Cymbopogon citratus P. gingivalis 55–110 (61), 4000 (80),
(Lemongrass oil) 50 (27), 220 (84), 133
Mentha oil (62)
F. nucleatum 250 (27)
Mints (Mentha spp.) are medicinal herbs that are val- Cymbopogon martini P. gingivalis 250 (27)
ued worldwide in traditional medicines for their antimi- F. nucleatum 125 (27)
crobial and antioxidant properties. They are also odor- Cymbopogon P. gingivalis 250 (27)
masking agents, as menthol and menthyl acetate are winterianus F. nucleatum 125 (27)
Cyperus articulatus P. gingivalis 250 (27)
responsible for a pungent and refreshing odor. There-
F. nucleatum 250 (27)
fore Mentha extracts are extensively used in oral Elyonurus muticus P. gingivalis 250 (27)
hygiene products, mouth fresheners, toothpastes, and F. nucleatum 250 (27)
chewing gums. The most widely used herb of this group Eugenia P. gingivalis 160 (70), 100 (71), 2000
is Mentha piperita. The main components of the oil are caryophyllata (80), 2 (85)
menthol, isomenthone, limonene, iso-menthanol, men- (Clove oil) F. nucleatum 80 (70), 100 (71), 1 (85)
thyl acetate, b-pinene, and a-pinene (24). P. intermedia 100 (71), 2 (85)
Eugenia florida P. gingivalis 125 (27)
Despite the common use of mint oil in oral hygiene F. nucleatum 125 (27)
products, only a few studies have investigated its Eugenia uniflora P. gingivalis 250 (27)
antimicrobial activity against oral bacteria. In general, F. nucleatum 125 (27)
it has been shown that the antimicrobial activity of Eucalyptus globulus P. gingivalis 2270–4545 (47), 280 (55),
mint oils against gram-positive bacteria is higher com- (Eucalyptus oil) 1000 (83)
pared to gram-negative bacteria (24,25). F. nucleatum 1180–2270 (47), 1140
(55), 1000 (83)
The MIC values of peppermint oil against different
Ficus deltoidea P. gingivalis 630 (81)
VSC-producing bacteria are found to be between 62.5 F. nucleatum 630 (81)
and 2,800 µg ml 1, although large differences were Juniperus communis L. P. gingivalis 3460 (40)
found between existing studies (26,27) (see Table 1). (Juniper oil) F. nucleatum 3460 (40)
Using the disc diffusion method, peppermint oil showed P. intermedia 3460 (40)
Effect of essential oils on halitosis 3

Table 1 Continued Table 1 Continued

Bacterial MIC value µg/ml Bacterial MIC value µg/ml


Essential oil strain (reference number) Essential oil strain (reference number)

Ledum S. moorei 1.56 (69) Thujopsis dolabrata P. gingivalis 1000 (80)


groenlandicum (Asunaro oil)
(Labrador tea) Thymus vulgaris P. gingivalis 32 (43), 500 (83)
Lavandula stoechas P. gingivalis 4400–8800 (47), 3520 (Thyme oil) F. nucleatum 500 (83)
(Lavender oil) (40) S. moorei 1470 (69)
F. nucleatum 2200 (47), 3520 (40) Ziziphus joazeiro P. gingivalis 250 (27)
P. intermedia 3520 (40) F. nucleatum 250 (27)
Lippia alba (leaves) P. gingivalis 6.25 (86), 250 (27) Chlorhexidine P. gingivalis 3 (88), 4 (80), 8 (26), 15
F. nucleatum 800 (86), 125 (27) (27)
Lippia sidoides P. gingivalis 250 (27) F. nucleatum 8 (26), 15 (27)
F. nucleatum 125 (27) P. intermedia 3 (88)
Leptospermum P. gingivalis 275 (47) P. endodentalis 3 (88)
scoparium (Manuka F. nucleatum 275 (47) a
oil) Multiple isolates were tested.
Melaleuca alternifolia P. gingivalis 1140–4390 (47), 61 (46),
(Tea tree oil) 966 (29) a higher antimicrobial activity against P. gingivalis than
F. nucleatum 527 (47), >5270 (29)
spearmint oil and many other essential oils (28), and
P. intermedia 26–880a (48)
P. endodentalis 61 (46), 220–880a (48) the antimicrobial activity was only exceeded by tea tree
Fusobacterium 2200–17,560a (48) and cinnamon oils. Another study showed a higher
spp. antimicrobial activity of sage oil in comparison to pep-
S. moorei ≥ 5 (49) permint oil (29). Antimicrobial activity of mint oil
Mentha pipperita P. gingivalis 62.5 (26), 2000 (29), 250 against Streptococcus mutans, another oral pathogenic
(Peppermint oil) (27)
bacterium, has been observed by several research
F. nucleatum 1000 (26), 2000 (29), 250
(27) groups (26,28,30). In contrast, CHAUDARI et al.
S. moorei 2810 (69) observed no activity against this strain (31). This dis-
T. denticola 1000 (29) crepancy probably points to various compositions of
Mikania glomerata P. gingivalis 500 (27) available essential oils. The minimum bactericidal con-
F. nucleatum 250 (27) centrations (MBCs) of other mint plants of the family
Myrtus communis L. P. gingivalis 220 (40), 880–7040a (41), Lamiaceae, i.e., kitchen mint and Japanese mint,
(Myrtle oil) 125–62.5a (39)
F. nucleatum 220–440 (40)
against P. gingivalis were found as 821 and
P. intermedia 1760 (40) 6,537 µg ml 1, respectively (32).
Ocimum americanum P. gingivalis 350 (87), >4450 (62) Furthermore, components of the essential oils from
F. nucleatum 700 (87) Mentha spp. can significantly retard biofilm formation
P. intermedia 350 (87) and thereby decrease the number of bacteria that pro-
Ocimum basilicum P. gingivalis >4450 (62) duce VSCs (33–35).
Ocimum sanctum L. P. gingivalis >4450 (62)
The main component of Mentha (menthol) seems to
Origanum majorana S. moorei 1400 (69)
(Sweet marjoram) be the major constituent responsible for the bioactivity
Orthosiphon P. gingivalis 1250 (81) of mint oil, whereas other terpenes in the essential oils
stamineus F. nucleatum 1250 (81) display some synergistic effects (36).
Pistacia atlantica P. gingivalis 11,380 (78) Peppermint oil can also increase salivation, which
Kurdica has positive effects since a dry mouth may intensify hal-
Romarinus officialis P. gingivalis 4540–9080a (47), 1000
itosis (37).
(Romarinus oil) F. nucleatum 4405 (47)
Salvia officinalis P. gingivalis 600 (29)
(Sage oil) F. nucleatum 800 (29)
S.
T.
moorei
denticola
5740 (69)
2000 (29)
Myrtus communis oil (myrtle oil)
Salvia fruticose M. P. gingivalis 7300 (40) The pharmacological activities of myrtle oil (Myrtus
F. nucleatum 7300 (40) communis), including its anti-inflammatory, antimicro-
P. intermedia 7300 (40)
Satureja hortensis oil P. gingivalis <113 (40)
bial, antioxidant, and hypoglycemic properties, have
(Summer savory F. nucleatum <113 (40) been widely investigated. The major components are a-
oil) P. intermedia <113 (40) pinene, limonene, 1,8-cineole, 4-terpineol, a-terpineol,
T. forsythia <113 (40) and linalool (38).
Satureja montana S. moorei 1400 (69) As shown in Table 1, myrtle oil exhibits a strong
(Winter savory oil) antimicrobial activity on several tested oral pathogens.
Siparuna guianenses P. gingivalis 62 (27)
The MIC values for several VSC-producing bacteria
F. nucleatum 62 (27)
Syzygium P. gingivalis 250 (27), 6.25 (72) are found between 62.5 and 7,040 µg ml 1 (39,40).
aromaticum F. nucleatum 250 (27) Using the disc diffusion assay, the antimicrobial activity
of myrtle oil was compared for different P. gingivalis
4 Dobler et al.

strains. All tested isolates of P. gingivalis (n = 20) were Table 2


sensitive to 125 µg ml 1 of myrtle oil, while 66.6% of Summary of published MIC values of main components of
P. gingivalis isolates were resistant to concentrations up essential oils for several VSC-producing bacterial strains.
to 62.5 lg ml 1 (39). Moreover, P. gingivalis is less sen-
sitive to myrtle oil than S. mutans. In another study, Bacterial MIC value
considerably higher values up to >7,000 lg ml 1 were Substance strain lg ml 1 (reference number)
found (41). 1,8-Cineole P. gingivalis 6400 (75)
(eucalyptol)
F. nucleatum 3200 (75)
P. intermedia 1600 (75)
Thymus oil (thyme oil) a-Pinene P. gingivalis 1600 (74), 800 (77)
Thyme possesses various beneficial effects due to its F. nucleatum 1600 (74), 3200 (77)
P. intermedia 400 (74), 800 (77)
antiseptic, carminative, antimicrobial, and antioxidative a-Terpineol P. gingivalis 200 (75), 100–400 (101)
properties. Commercially available thyme oils are F. nucleatum 400 (75), 100–400 (101)
mostly derived from the species Thymus zygis or Thy- P. intermedia 200 (75), 400 (101)
mus vulgaris. The main compounds of this oil are the b-Caryopyllene P. gingivalis 400 (75), 630 (81)
natural terpenoid thymol and its isomer carvacrol (42). F. nucleatum 12800 (75), 630 (81)
Several studies have shown the antimicrobial activity P. intermedia 800 (75)
Bomeol P. gingivalis 800 (75)
of thyme oil and its single components against oral
F. nucleatum 200 (75)
pathogen bacteria (29,43). As shown in Table 1, MIC P. intermedia 200 (75)
values for VSC-producing bacteria were found ranging Carvacrol P. gingivalis 70 (102), 2400 (103)
between 32 and 1,470 lg ml 1 (43,44). The MIC value F. nucleatum 30 (102), 2400 (103)
of the main component of thyme oil, thymol, for P. intermedia 125 (45)
P. gingivalis was found as 300 lg ml 1 (29,44) and for Camphor P. gingivalis 6400 (75)
F. nucleatum 6400 (75)
P. intermedia as 125 lg ml 1 (45) (see Table 2). How-
P. intermedia 1600 (75)
ever, no direct comparison between thyme oil and thy- Cinnamaldehyde P. gingivalis 0.3 (67), 0.33 (68)
mol is possible, due to different methods used in the F. nucleatum 0.3 (67)
selected studies. P. intermedia 125 (45)
The antimicrobial activity of thyme oil in comparison Citral P. gingivalis 210 (62)
to lavender oil, tea tree oil, peppermint oil, and eugenol Citronellal P. gingivalis 640 (62)
oil was evaluated using four common oral pathogens: Cuparene P. gingivalis 4000 (80)
Eugenol P. gingivalis 5.13 (72), 100 (71), 800 (67),
Staphylococcus aureus, Enterococcus fecalis, 1250 (81), 600 (29), 3180 (62)
Escherichia coli and Candida albicans (37). In general, F. nucleatum 100 (71), 800 (67), 1250 (81)
the MIC values of thyme oil were significantly higher P. intermedia 100 (71), 250 (45)
compared to those of peppermint oil and eugenol oil, Geraniol P. gingivalis 1110 (62)
indicating a lower antimicrobial activity. However, no Germacrene D P. gingivalis 1250 (81)
VSC-producing bacteria were tested. F. nucleatum 1250 (81)
Linalool P. gingivalis 100–800* (101), 4290 (62)
F. nucleatum 100–200* (101)
P. intermedia 200–1600* (101)
Melaleuca alternifolia oil (tea tree oil) Macrocarpal P. gingivalis 0.5–5 (57), 0.2–0.39* (104)
F. nucleatum 100 (57), 0.78–6.25* (104)
The essential oil of Melaleuca alternifolia (Myrtaceae), P. intermedia 1–10 (57), 0.39–1.56* (104)
known as tea tree oil, has been valued in medicine for Sabinene P. gingivalis 50 (74)
F. nucleatum 800 (74)
many years. Tea tree oil mainly contains terpinen-4-ol,
P. intermedia 200 (74)
c-terpinene, and a-terpinene (about 70% to 90% of the Terpinen-4-ol P. gingivalis 400 (75), 600 (102)
oil as a whole). The oil exhibits strong antimicrobial F. nucleatum 200 (75), 600 (102)
properties and is often used in the superficial treatment P. intermedia 200 (75)
of skin infections. Thujopsene P. gingivalis 500 (80)
It has been shown that the essential oil of Melaleuca Thymol P. gingivalis 300 (29)
alternifolia can inhibit strong oral bacterial growth and P. intermedia 125 (45)
VSC production (46,47). The MIC values were found *Multiple isolates were tested.
to range between 26 and above 17,000 lg ml 1
(Table 1), whereas MBC values were reported at
4,390 lg ml 1 (46–48). Some studies could even show strains (48). Time kill experiments performed in this
an antimicrobial activity of tea tree oil exceeding the study demonstrated a rapid killing of S. mutans and
activity of chlorhexidine. Additionally, M. alternifolia Lactobacillus rhamnosus after 30 s treatment with as lit-
significantly reduces the production of H2S by P. gingi- tle as 0.5% of tea tree oil. FORRER et al. determined the
valis and the H2S and methyl mercaptan (CH3SH) antimicrobial activity of tea tree oil in combination
levels of P. endodontalis. HAMMER et al. determined an with a-bisabolol and found that tea tree oil was potent
in vitro activity of Melaleuca alternifolia oil against 161 against S. moorei at concentrations of 5% and 0.5%,
isolates of oral bacteria including some VSC-producing efficiently killing the bacteria even after a short
Effect of essential oils on halitosis 5

incubation time (49). Furthermore, the combination of In vivo experiments, using toothpaste containing
0.1% a-bisabolol plus 0.05% tea tree oil could increase eucalyptus oil, confirmed the antibacterial activity as
antimicrobial activity compared to the single compo- well as inhibition of dental biofilm formation (33). Fur-
nents. Besides its antimicrobial activity, tea tree oil thermore, SATO et al. demonstrated that 0.3% eucalyp-
showed significant adhesion-inhibiting effects on P. gin- tus-extract-containing chewing gum significantly
givalis in vitro (47). This effect suggests that tea tree oil inhibited plaque accumulation in comparison to a con-
might suppress the biofilm formation. trol chewing gum without eucalyptus extract in human
All of these studies suggest that tea tree oil may be volunteers (56).
an effective active ingredient in antiseptic mouth rinses. Besides the native oil, the antimicrobial activity of
Thus, several studies assessing the effects of tea tree oil selected components of eucalyptus oil has been tested
on oral bacteria as well as plaque formation in vivo in some studies (57,58). However, only a few studies
have been conducted (50,51). A tea tree oil-containing were performed using oral bacteria. The effect of
mouthwash was effective in decreasing salivary bacterial macrocarpals, which are phloroglucinol derivatives con-
counts for a short period of time. However, it neither tained in eucalyptus leaves, on periodontopathic bacte-
reduced the clinical parameters (PI and plaque area) ria, especially P. gingivalis, were tested (57). The
nor the vitality of the plaque flora significantly (50). growth of all tested oral bacteria was strongly inhib-
The same effects were obtained using a tea tree oil-con- ited. The MIC values of macrocarpals were 10–1,000
taining gel (51). However, decreased gingival inflamma- times lower than for native eucalyptus oil (see Table 2).
tion, despite a lack of a significant decrease in plaque Additionally, macrocarpals inhibited P. gingivalis Arg-
scores, indicates its anti-inflammatory rather than and Lys-specific proteinases. This resulted in an inhibi-
antibacterial activity (51). A significant decrease in the tion of the binding behaviour towards saliva-coated
full mouth bleeding score, as an index value of active hydroxyapatite beads, suggesting that macrocarpals
inflammation, along with the GI using mouth rinse also attenuate P. gingivalis adherence. In contrast, the
containing tea tree oil was also found in a clinical study antimicrobial activity of the main component of euca-
performed by SALVATORI et al. (52). The effect was even lyptus oil (eucalyptol) is lower than the activity of
better compared to a mouthwash containing 0.12% native oil (58).
chlorhexidine. Another study compared mouthwashes
containing tea tree oil (0.2%), garlic (2.5% solution),
or chlorhexidine (0.12%), by determining levels of
S. mutans and other oral microorganisms in saliva sam-
Cymbopogon citratus oil (lemongrass oil)
ples upon usage of the different products (53). Signifi- Lemongrass oil (Cymbopogon citratus) is a volatile oil
cant reduction in viable counts after application of tea obtained from lemongrass leaves. Lemongrass oil is
tree oil was found. Additionally, in contrast to usually made up of citral at an average of 65%–80%,
chlorhexidine, a further reduction of bacteria was and citral is a natural mixture of geranial and neral
observed after a period of 5 wk of use. (59). Lemongrass oil has antibacterial, anti-fungal,
Some studies also report adverse effects of the use of antioxidant, antiseptic, astringent, anti-inflammatory,
mouthwashes containing tea tree oil, such as a burning analgesic, antipyretic, and carminative properties.
sensation and a stinging and unpleasant taste (53,54). The antimicrobial activity of lemongrass oil against
However, it is possible that those effects could be oral bacteria has been determined in several studies (60–
attributed to the alcohol of the mouthwashes (54). 62). The MIC values against VSC-producing bacteria
were reported to range between 55 and 4,000 lg ml 1
(see Table 1). An in vitro time kill study showed that
C. citratus oil rapidly reduced viable numbers of P. gin-
Eucalyptus globulus oil (eucalyptus oil)
givalis (62). In another study, the antimicrobial activity
Eucalyptus oil is extracted from the leaves of the euca- against common VSC-producing microorganisms of
lyptus tree (Eucalyptus globulus) native to Australia. lemongrass oil, and a lemongrass mouth rinse containing
The main group of constituents of eucalyptus oil are 1% lemongrass oil, was compared with chlorhexidine
monoterpenes such as eucalyptol (1,8-cineole), a-pinene digluconate, using a broth micro-dilution assay and the
and d-limonene. Eucalyptus oil has antibacterial and disc diffusion method (61). In this study, lemongrass oil
freshening properties, and is therefore often used in was effective against A. actinomycetemcomitans and
mouthwashes and chewing gums. P. gingivalis, but less effective against S. mutans. Using a
Several studies confirm the antimicrobial activity of mouth rinse containing lemongrass, lower MIC and
eucalyptus oil against oral bacteria including VSC-pro- MBC values were found than for pure lemongrass oil
ducing strains (47,55). The reported MIC values for and a chlorhexidine digluconate solution. However, the
several VSC-producing bacteria are between 280 and mouth rinse contained an additional 0.003% of a flavor
4,540 lg ml 1 (see Table 1) (47,55). The MIC values of mixture containing menthol, peppermint oil, anise oil,
eucalyptus oil are found to be higher than for manuka and vanilla in ethanol. These compounds can enhance
oil, tea tree oil, romarinus oil, and comparable with the activity of lemongrass oil by synergistic effects. In
those reported for lavendula oil (47). The lower antimi- contrast, the inhibition zone of the lemongrass mouth
crobial activity of eucalyptus oil in comparison to tea rinse was smaller than that of lemongrass oil alone, and
tree oil was confirmed by PARK & YOON (28). of chlorhexidine digluconate. This discrepancy was
6 Dobler et al.

explained by different diffusion of the formulation in the Clove oil


agar. An in vivo study using this mouth rinse showed
that it can significantly reduce VSC production in the Several studies have shown that the essential oil of the
oral cavity (61). Eugenia caryophyllata (clove) leaf and its main compo-
Double-blinded clinical trials have been conducted to nent eugenol has an antibacterial activity against VSC-
check the efficacy of lemongrass oil as a mouthwash in producing bacteria. However, there are significant dif-
comparison to a 0.2% chlorhexidine mouthwash (63). ferences between the data described in the literature.
The lemongrass oil mouthwash group showed a higher The MIC values for oral bacteria were found ranging
reduction in the PI score and the GI than the chlorhex- between 1 and 2,000 lg ml 1 (see Table 1) (70–72). A
idine group. The higher reduction in the GI score was similar antimicrobial activity was found for clove oil
probably due to the antioxidant and anti-inflammatory and its main compound, eugenol, against all tested
effect of lemongrass oil. These properties can be also strains of F. nucleatum, P. gingivalis and P. intermedia,
utilized in the prevention and treatment of periodonti- whereas another active compound, b-caryophyllene,
tis, where application of lemongrass oil mouthwash showed a significantly lower activity (71).
leads to an increased level of thiol antioxidants (64). Furthermore, E. caryophyllata oil suppressed the
Moreover, lemongrass oil can be an effective anti- adhesion of bacteria and disrupted biofilm formation at
plaque agent by reducing the adherence of cells and concentrations ranging from 0.63 to 5.0 mg ml 1 (73).
thereby having an inhibitory effect on biofilm forma-
tion (65). A reduction of biofilm formation up to
99.8% could be shown for S. mutans at a concentration Other essential oils
of 0.5 % v/v C. citratus oil (62). Another in vitro study
showed that application of lemongrass oil mouthwash Apart from the oils described above, many other essen-
(0.25% and 0.5% solutions) results in better plaque tial oils have been tested with regard to oral bacteria
reduction compared to a solution containing chlorhexi- (47). Manuka oil and tea tree oil had the strongest
dine (66). antibacterial activity compared to eucalyptus oil, lavan-
dula oil, and romarinus oil against P. gingivalis and
F. nucleatum (47). Additionally, they have shown a sig-
nificant adhesion-inhibiting activity against P. gingi-
Cinnamomum zeylanicum oil (cinnamon valis. In another study, the antimicrobial efficacy of
oil) Satureja hortensis L. (summer savory), Salvia fruticosa
Cinnamon oil, obtained from the Cinnamomum zeylan- M. (sage), Lavandula stoechas L. (lavender), Myrtus
icum plant, has been successfully used in traditional communis L., and Juniperus communis L. (juniper)
medicine for decades. Cinnamaldehyde has been identi- essential oils was compared (40). S. hortensis L. essen-
fied as the major component of cinnamon oil in con- tial oil was the most effective, showing inhibitory activ-
centrations of up to 80% (67). ity against all tested VSC-producing bacteria. However,
The antimicrobial activity of cinnamon oil against S. hortensis L. essential oil had no anti-biofilm activity
oral bacteria is described in several studies (67,68). The against most tested periodontal bacteria (40).
MIC values of the native oil were compared to MIC The essential oil of Cryptomeria japonica exhibited con-
values of its main component, cinnamaldehyde (67). siderable inhibitory effects against several VSC-producing
The antimicrobial activity of cinnamaldehyde against bacteria at MIC values ranging from 25 to 50 lg ml 1
P. gingivalis and F. nucleatum (MIC = 0.3 lg ml 1) (74). In another publication the same research team pub-
(see Table 2) was significantly higher than the activity lished MIC values for Artemisia feddei oil ranging between
of cinnamon oil (MIC = 630 and 420 lg ml 1, respec- 25 and 100 lg ml 1 (75). Comparable results were
tively). A similar trend was found for P. gingivalis in obtained for Artemisia capillaris oil (76). Furthermore, the
another study. However, the MIC values determined antimicrobial activity of all of these oils is similar to the
for cinnamon oil were significantly lower, at activity of ampicillin with regard to P. intermedia. How-
6.25 lg ml 1 (68). Additionally, in both studies, the ever, the main components of these oils, such as a-pinene,
increased translucency of S. mutans, P. gingivalis and sabinene, a-terpineol, terpinen-4-ol, camphor, and 1,8-ci-
F. nucleatum cells after an exposure to cinnamon oil neole, have a lower antimicrobial activity than the native
was explained as the destruction of the bacterial cell oils, pointing to a synergistic effect of all components.
membrane (67,68). In another study, the antimicrobial Similar synergistic effects are found for the essential oil of
activity of cinnamon oil against S. moorei was found to Chrysanthemum indicum (77). The published MIC values
be superior to all other tested essential oils, such as of this essential oil for P. gingivalis, F. nucleatum, and
peppermint, sage, or thyme oils (69). In the same study, P. intermedia range between 100 and 200 lg ml 1 (see
a reduced biofilm growth even below MIC values was Table 1) and are thereby lower than those seen for the sin-
observed. However, cinnamaldehyde had no effect on gle components of the oil as well as the antibiotics ampi-
the established biofilm mass, whereas the preformed cillin and gentamicin.
biofilm mass was inhibited by the native oil (68). Fur- The essential oils from coriander, Labrador tea,
thermore, cinnamon oil inhibited the ability of sweet marjoram, thyme, and winter savory exhibited a
S. moorei to produce H2S in vitro even at concentra- MIC of 1.56 mg ml 1 and a MBC of 3.13 mg ml 1 for
tions below the MIC value (69). S. moorei (69). Essential oils from balsam fir, myrrh,
Effect of essential oils on halitosis 7

peppermint, and sage were less effective, with MIC and of the oils used. Only a few studies with this research
MBC values ≥3.13 and ≥6.25 mg ml 1, respectively topic have been published. Most of them are related to
(69). Listerine products, and have been summarized by HAAS
Pistacia atlantica Kurdica essential oil demonstrated et al. (89). This systematic review demonstrated that
an antimicrobial effect against P. gingivalis as well as mouthwashes containing essential oils, used as adju-
significant wound healing effect due to a reduction of vants to mechanical oral hygiene, are more efficient
the lipid peroxidation, thus improving collagen synthe- than mechanical oral hygiene alone. Furthermore, Lis-
sis (78). terine has been shown to be highly effective against oral
The antimicrobial efficacy of various concentrations malodor due to its antimicrobial action (90). Moreover,
of chamomile oil and turmeric oil against P. gingivalis Listerine products with essential oils were more efficient
was assessed via the disc diffusion test (79). Both oils than cetylpyridinium chloride (89). The irritation poten-
were less effective than eucalyptus oil and tea tree oil. tial of an essential oil-containing mouth rinse (Listerine
The antibacterial effect of forty-eight selected plant Antiseptic) was found to be minimal (91).
essential oils against P. gingivalis was evaluated with Another study has been performed using a mouth-
the MIC and MBC assay (80). Ten samples showed an wash containing essential oils of lemon and mint. Sig-
inhibitory activity, whereas asunaro oil nificant differences between the control mouthwash
(MIC = 1 mg ml 1) and cypress oil (0.5 mg ml 1) were (mouthwash without essential oils) and the test mouth-
selected as the two most effective essential oils. Further- wash were found regarding the PI, bleeding on probing,
more, four active compounds were isolated. Among GI, BANA test results, and organoleptic examination
them, thujopsene was the most effective with values, confirming the hypothesis that the essential oils
MIC = 0.5 mg ml 1. in the tested formulation had a beneficial clinical effect
The antimicrobial activity of the essential oils of on halitosis (92).
Orthosiphon stamineus Benth and Ficus deltoidea Jack, A mixture of tea tree (Melaleuca alternifolia), pepper-
containing b-caryophyllene as the main component, mint (Mentha piperita), and lemon oil (Citrus limon)
against P. gingivalis and F. nucleatum has been com- has been used to treat oral malodor in 32 intensive care
pared (81). The MIC values of Ficus deltoidea oil were unit patients (93). The level of oral malodor was signifi-
similar to the MIC values of b-caryophyllene, whereas cantly lower 5 min after the essential oil treatment ses-
the activity of Orthosiphon stamineus oil was lower, sion, even though the first decrease of VSCs was
probably due to a lower concentration of b-caryophyl- detected after 1 h. These data indicate that besides
lene. However, these essential oils showed no inhibition antimicrobial activity, components of essential oils can
on bacterial biofilms. Furthermore, the combination of act as masking agents.
both oils with amoxicillin at concentrations of 1 9 and The effect of a mouth rinse, consisting of the essen-
2 9 MIC values demonstrated an additive antibacterial tial oils Cymbopogon flexuosus, Thymus zygis and Ros-
effect. marinus officinalis (Parodolium), was tested in a
The antimicrobial activity of Croton cajucara oil and randomized clinical trial against oral pathogen bacteria
its main component linalool has been tested against in patients with generalized moderate chronic periodon-
P. gingivalis (82). The oil activity was found compara- titis (94). A significant decrease of T. denticola, F. nu-
ble with the activity of chlorhexidine, but linalool cleatum, T. forsythia, and P. micra was determined
showed no measurable activity. This result suggests that after 3 months of use.
although linalool is a major component of the essential The antimicrobial activity of the mouthwash
oil from C. cajucara, it is not responsible for its Salviathymol N, containing 1% of essential oils (Euca-
antibacterial effects. lyptus globulus oil, Foeniculum vulgare oil, camphor,
The activity of several less common essential oils on Mentha piperita oil, menthol, Rosmarinus officinalis oil,
oral biofilms has been tested by BERSAN et al. (27). Salvia officinalis oil) in comparison to that of a mouth-
Most of the essential oils presented a moderate to wash containing 0.12% w/v chlorhexidine, was tested
strong antimicrobial activity against the oral pathogens. using experimental microorganisms including F. nuclea-
The essential oil of Coriandrum sativum inhibited all tum (95). This study showed that the chlorhexidine
oral species at the lowest MIC values, whereas Cyperus solution had a higher antibacterial effect against the
articulates exhibited the best ability to control biofilm tested organisms than Salviathymol, which exhibited
formation. moderate antibacterial effects.

Mouth hygiene products containing several Antimicrobial activity and synergism


essential oils between oil components
Mouthwashes and toothpastes containing essential oils The reactivity of an essential oil depends on the nature,
are common oral hygiene products. Their aim is to the composition, and the orientation of its functional
reduce oral bacteria and to decrease oral odor by groups. Usually, the chemical characterization of many
masking. Most of these products contain more than essential oils reveals the presence of only two or three
one essential oil. However, most of these products have major components at a fairly high concentration (20%–
not yet been investigated with regard to the efficiency 80%), compared to other components present in trace
8 Dobler et al.

amounts. Thus, the biological properties of the essential eucalyptus oil and peppermint oil show a significantly
oils are determined mostly by their major components. lower antimicrobial activity. It has been shown that
Among the essential oil constituents, the phenolic organisms growing in biofilms are more resistant to
compounds have been found to possess major antimi- antimicrobial agents than the same species growing in a
crobial activities (96). The hydroxyl group of phenol planktonic state. However, biofilm formation seems to
interacts with the cell membrane, causing leakage of be one of the main challenges in the treatment of hali-
cellular components, a change in fatty acids and phos- tosis. Several studies have shown that the inhibition of
pholipids, and an influence on genetic material synthe- biofilm formation by essential oils is due to an attenua-
sis. Similarly to phenolic compounds, the site of action tion of bacterial growth. Although chlorhexidine is
of the terpenes is the cell membrane. They permeate mostly used for the elimination of oral bacteria, essen-
through the membrane, causing a swelling and an inhi- tial oils have several other benefits regarding the treat-
bition of respiratory enzymes (97). The MIC values of ment of halitosis. These particularly include their anti-
some common compounds have been compiled in inflammatory and odor-masking properties. Therefore,
Table 2. mouthwashes containing essential oils are more effec-
However, as shown above, compounds in essential tive for the treatment of halitosis.
oils can interact and cause synergistic, additive, indiffer- Most of the studies presented were performed
ent, or antagonistic effects. In recent years, many stud- in vitro. The bactericidal effects seen in vitro may not
ies have investigated combinations of essential oils and necessarily be transferred to an in vivo application,
their components with the aim to increase their efficacy e.g., using a mouthwash solution. Due to the presence
(98,99). However, there are only a few studies per- of unpredictable amounts of saliva as well as exogenous
formed on VSC-producing bacteria. Nevertheless, simi- protein in the oral cavity, the activity of essential oils
lar mechanisms can be expected as for other gram- might be influenced. Therefore, clinical trials are
negative pathogens. The synergism could be due to the required to determine the in vivo efficacy and to inves-
increase of one of three factors which determine the tigate optimal oil concentrations and compositions.
antimicrobial property of essential oil components: Essential oils are natural products and thereby not
their lipophilic properties, the potency of their func- synthesized de novo following existing protocols.
tional groups, and their aqueous solubility by either Therefore, their chemical composition strongly
compound of a paired combination (98). depends on several factors, such as seasonal variation,
Synergistic effects on the growth inhibition of gram- harvesting time and procedure, the age of a plant and
negative bacterium E. coli has been found for thymol/ the selected part of the plant used for extraction of
eugenol, thymol/carvacrol, carvacrol/eugenol, car- the oil (105). This might contribute to the partially
vacrol/linalool, carvacrol/menthol, menthol/thymol, contradictory results from the existing studies. How-
eugenol/linalool, and eugenol/cinnamaldehyde combi- ever, not all observed differences can be explained in
nations (45,98,99). Eugenol and thymol are believed to this way. Thus, different methods, such as different
work synergistically, with thymol disrupting and disin- media, different cultivation conditions, and different
tegrating the outer membrane of gram-negative species inoculum sizes can also have an impact on the out-
and allowing eugenol to access the cytoplasm and come. A further explanation for the differences in the
destroy enzymes (99). The synergism between eugenol MIC values published for a single compound could
and cinnamaldehyde is probably caused by the different be related to the different sensitivity of strains of one
protein target sites of the two compounds: eugenol species against the tested inhibitory compounds. Sev-
inhibits the enzymatic activity while cinnamaldehyde eral studies demonstrated that MIC values for a sin-
interferes with the action of amino acid decarboxylases gle compound can be found to differ by several
(100). The absence of synergistic effects observed orders of magnitude. Therefore, a direct comparison
between linalool and menthol, lacking an aromatic of data, obtained by various research groups, is not
ring, suggests that the aromatic ring may significantly possible in most cases.
contribute to synergism (98). When using essential oils, several safety aspects
must be taken into account. These include the allergic
and toxic potential as well as patient compliance. Lim-
ited data are available on the safety and toxicity of
Discussion the described oils. Studies have shown that many
Several in vitro and in vivo studies have investigated essential oils could be toxic at higher doses and also
the effect of herbal essential oils in treating dental dis- cause skin irritation at higher concentrations (106).
eases, including halitosis. In this context the strong The spectrum of reported skin reactions to essential
antimicrobial activity of several oils against VSC-pro- oils include allergic contact dermatitis, irritant contact
ducing bacteria could be shown. Some studies could dermatitis, phototoxic reactions and contact urticaria
even show that the effect of essential oils is superior to (107). These allergic reactions arise from certain con-
that of the commonly used chlorhexidine solution stituents, e.g., benzyl alcohol, cinnamyl alcohol, euge-
(shown in Table 1). Based on the published literature, nol, iso-eugenol, hydroxycitronellal, geraniol, and
the highest antimicrobial activities are described for many others. However, the use of low concentrations
cinnamon oil, clove oil, lemongrass oil, myrtle oil, and of essential oils showed hardly any negative side
summer savory oil, whereas the commonly used effects.
Effect of essential oils on halitosis 9

Most essential oils have a strong smell. This fra- 10. HARASZTHY VI, ZAMBON JJ, SREENIVASAN PK, ZAMBON MM,
grance is often used to mask mouth odor. However, GERBER D, REGO R, PARKER C. Identification of oral bacte-
rial species associated with halitosis. J Am Dent Assoc 2007;
not all fragrances are considered pleasant by patients. 138: 1113–1120.
Thus, oils with a camphoraceous odor, such as eucalyp- 11. DONALDSON AC, MCKENZIE D, RIGGIO MP, HODGE PJ,
tus oil or tea tree oil, are less accepted than citral- or ROLPH H, FLANAGAN A, BAGG J. Microbiological culture
menthol-containing oils, such as lemongrass oil or pep- analysis of the tongue anaerobic microflora in subjects with
permint oil. Therefore, most antimicrobial oral prod- and without halitosis. Oral Dis 2005; 11(Suppl 1): 61–63.
12. DE GEEST S, LALEMAN I, TEUGHELS W, DEKEYSER C, QUIRY-
ucts contain a mix of several essential oils. In this way, NEN M. Periodontal diseases as a source of halitosis: a review
a pleasant smell with the desired antimicrobial activity of the evidence and treatment approaches for dentists and
can be achieved. dental hygienists. Periodontol 2000 2016; 71: 213–227.
13. SWAMY MK, AKHTAR MS, SINNIAH UR. Antimicrobial prop-
erties of plant essential oils against human pathogens and
their mode of action: an updated review. Evid Based Comple-
ment Alternat Med 2016; 2016: 3012462.
Conclusion 14. CHOUHAN S, SHARMA K, GULERIA S. Antimicrobial activity
of some essential oils-present status and future perspectives.
As described in this review, there is considerable evi- Medicines 2017; 4: 58.
dence that essential oils have the potential to be further 15. INOUYE S, TAKIZAWA T, YAMAGUCHI H. Antibacterial activity
developed as preventive or therapeutic agents for the of essential oils and their major constituents against respira-
treatment of halitosis. However, there is a need to con- tory tract pathogens by gaseous contact. J Antimicrob Che-
mother 2001; 47: 565–573.
duct further research to establish their safety and effi- 16. CUI H, ZHANG X, ZHOU H, ZHAO C, LIN L. Antimicrobial
cacy before including them in common clinical practice. activity and mechanisms of Salvia sclarea essential oil. Bot
Presently, the composition of oral products seems Stud 2015; 56: 16.
based more on traditional use than on clinical data. 17. LAKEHAL S, MELIANI A, BENMIMOUNE S, BENSOUNA S, BENRE-
BIHA F, CHAOUIA C. Essential oil composition and antimicro-
There are only a few studies which include clinical data
bial activity of Artemisia herba–alba Asso grown in Algeria.
regarding an effective treatment of halitosis using essen- Med Chem 2016; 6: 435–439.
tial oils contained in mouth rinses or toothpastes. 18. TROMBETTA D, CASTELLI F, SARPIETRO MG, VENUTI V, CRIS-
TANI M, DANIELE C, SAIJA A, MAZZANTI G, BISIGNANO G.
Acknowledgements – Open access funding enabled and organized Mechanisms of antibacterial action of three monoterpenes.
by Projekt DEAL. Antimicrob Agents Chemother 2005; 49: 2474–2478.
19. VLACHOJANNIS C, CHRUBASIK-HAUSMANN S, HELLWIG E, AL-
Conflicts of interest – The authors declare that they have no con- AHMAD A. A Preliminary investigation on the antimicrobial
flicts of interest. This research received no specific grant from any activity of listerine(R), its components, and of mixtures
funding agency in the public, commercial, or non-profit sectors. thereof. Phytother Res 2015; 29: 1590–1594.
No funding was accepted for this study, and no ethical approval 20. FINE DH, FURGANG D, SINATRA K, CHARLES C, MCGUIRE A,
was required. KUMAR LD. In vivo antimicrobial effectiveness of an essen-
tial oil-containing mouth rinse 12 h after a single use and 14
days’ use. J Clin Periodontol 2005; 32: 335–340.
21. KATO T, IIJIMA H, ISHIHARA K, KANEKO T, HIRAI K, NAITO
Y, OKUDA K. Antibacterial effects of Listerine on oral bacte-
References ria. Bull Tokyo Dent Coll 1990; 31: 301–307.
22. FORNELL J, SUNDIN Y, LINDHE J. Effect of listerine on dental
1. SPIELMAN AI, BIVONA P, RIFKIN BR. Halitosis. A common plaque and gingivitis. Scand J Dent Res 1975; 83: 18–25.
oral problem. N Y State Dent J 1996; 62: 36–42. 23. GORDON JM, LAMSTER IB, SEIGER MC. Efficacy of Listerine
2. ZALEWSKA A, ZATONSKI M, JABLONKA-STROM A, PARADOWSKA antiseptic in inhibiting the development of plaque and gin-
A, KAWALA B, LITWIN A. Halitosis - a common medical and givitis. J Clin Periodontol 1985; 12: 697–704.
social problem. A review on pathology, diagnosis and treat- 24. TYAGI AK, MALIK A. Antimicrobial potential and chemical
ment. Acta Gastroenterol Belg 2012; 75: 300–309. composition of Mentha piperita oil in liquid and vapour
3. AYLIKCI BU, COLAK H. Halitosis: from diagnosis to manage- phase against food spoiling microorganisms. Food Control
ment. J Nat Sci Biol Med 2013; 4: 14–23. 2011; 22: 1707–1714.
4. DEBOEVER EH, LOESCHE WJ. Assessing the contribution of 25. AL-BAYATI FA. Isolation and identification of antimicrobial
anaerobic microflora of the tongue to oral malodor. J Am compound from Mentha longifolia L. leaves grown wild in
Dent Assoc 1995; 126: 1384–1393. Iraq. Ann Clin Microbiol Antimicrob 2009; 8: 20.
5. SEERANGAIYAN K, VAN WINKELHOFF AJ, HARMSEN HJM, ROS- 26. GREENBERG M, URNEZIS P, TIAN M. Compressed mints and
SEN JWA, WINKEL EG. The tongue microbiome in healthy chewing gum containing magnolia bark extract are effective
subjects and patients with intra-oral halitosis. J Breath Res against bacteria responsible for oral malodor. J Agric Food
2017; 11: 36010. Chem 2007; 55: 9465–9469.
6. SATO H, OHKUSHI T, KAIZU T, TSUNODA M, SATO T. A study 27. BERSAN SMF, GALVAO LCC, GOES VFF, SARTORATTO A, FIG-
of the mechanism of halitosis occurrence in periodontal UEIRA GM, REHDER VLG, ALENCAR SM, DUARTE RMT,
patients. Bull Tokyo Dent Coll 1980; 21: 271–278. ROSALEN PL, DUARTE MCT. Action of essential oils from
7. PERSSON S, EDLUND MB, CLAESSON R, CARLSSON J. The for- Brazilian native and exotic medicinal species on oral bio-
mation of hydrogen sulfide and methyl mercaptan by oral films. BMC Complem Altern Med 2014; 14: 451.
bacteria. Oral Microbiol Immunol 1990; 5: 195–201. 28. PARK C, YOON H. Antimicrobial activity of essential oil
8. GOLDBERG S, CARDASH H, BROWNING H 3rd, SAHLY H, against oral strain. Int J Clin Prev Dent 2018; 14: 216–221.
ROSENBERG M. Isolation of Enterobacteriaceae from the 29. SHAPIRO S, MEIER A, GUGGENHEIM B. The antimicrobial
mouth and potential association with malodor. J Dent Res activity of essential oils and essential oil components towards
1997; 76: 1770–1775. oral bacteria. Oral Microbiol Immunol 1994; 9: 202–208.
9. KRESPI YP, SHRIME MG, KACKER A. The relationship 30. GALVAO ~ LCDC, FURLETTI VF, BERSAN SMF, DA CUNHA MG,
between oral malodor and volatile sulfur compound-produc- RUIZ ALTG, DE CARVALHO JE, SARTORATTO A, REHDER
ing bacteria. Otolaryng Head Neck 2006; 135: 671–676. VLG, FIGUEIRA GM, TEIXEIRA DUARTE MC, IKEGAKI M, DE
10 Dobler et al.

ALENCAR SM, ROSALEN PL. Antimicrobial activity of essen- 51. SOUKOULIS S, HIRSCH R. The effects of a tea tree oil-contain-
tial oils against streptococcus mutans and their antiprolifera- ing gel on plaque and chronic gingivitis. Aust Dent J 2004;
tive effects. Evid Based Complement Alternat Med 2012; 49: 78–83.
2012: 751435. 52. SALVATORI C, BARCHI L, GUZZO F, GARGARI M. A comparative
31. CHAUDHARI L, JAWALE BA, SHARMA S, SHARMA H, KUMAR study of antibacterial and anti-inflammatory effects of mou-
C, KULKARNI PA. Antimicrobial activity of commercially thrinse containing tea tree oil. Oral Implantol 2017; 10: 59–70.
available essential oils against Streptococcus mutans. J Con- 53. GROPPO FC, RAMACCIATO JC, SIMOES RP, FLORIO FM, SAR-
temp Dent Pract 2012; 13: 71–74. TORATTO A. Antimicrobial activity of garlic, tea tree oil, and
32. KRAIVAPHAN P, AMORNCHAT C, MANEEPITSAMAI Y. Bacterici- chlorhexidine against oral microorganisms. Int Dent J 2002;
dal effects of three mint essential oils on Porphyromonas 52: 433–437.
gingivalis in planktonic and biofilm cells. Res J Med Plant 54. VAZQUEZ JA, ZAWAWI AA. Efficacy of alcohol-based and
2013; 7: 100–106. alcohol-free melaleuca oral solution for the treatment of flu-
33. RASOOLI I, SHAYEGH S, ASTANEH S. The effect of Mentha spi- conazole-refractory oropharyngeal candidiasis in patients
cata and Eucalyptus camaldulensis essential oils on dental with AIDS. HIV Clin Trials 2002; 3: 379–385.
biofilm. Int J Dent Hyg 2009; 7: 196–203. 55. BOULEKBACHE ML, GRENIER D, BEY OSSZ, HARKAT ML,
34. TUTAR U, CELIK C, KARAMAN I, ATAS M, HEPOKUR C. Anti- RIGOU P, ALLALOU H, MADANI K. Chemical composition,
biofilm and antimicrobial activity of Mentha pulegium L antioxidant capacity, and antibacterial activity of essential
essential oil against multidrug-resistant Acinetobacter bau- oils of leaves of Eucalyptus globulus plant. Clin Exp Phar-
mannii. Trop J Pharm Res 2016; 15: 1039–1046. macol 2017; 7: 67.
35. RASOOLI I, SHAYEGH S, TAGHIZADEH M, ASTANEH SD. Phy- 56. SATO S, YOSHINUMA N, ITO K, TOKUMOTO T, TAKIGUCHI T,
totherapeutic prevention of dental biofilm formation. Phy- SUZUKI Y, MURAI S. The inhibitory effect of funoran and
tother Res 2008; 22: 1162–1167. eucalyptus extract-containing chewing gum on plaque forma-
36. ISCAN G, KIRIMER N, KURKCUOGLU M, BASER KH, DEMIRCI tion. J Oral Sci 1998; 40: 115–117.
F. Antimicrobial screening of Mentha piperita essential oils. 57. NAGATA H, INAGAKI Y, YAMAMOTO Y, MAEDA K, KATAOKA
J Agric Food Chem 2002; 50: 3943–3946. K, OSAWA K, SHIZUKUISHI S. Inhibitory effects of macro-
37. THOSAR N, BASAK S, BAHADURE RN, RAJURKAR M. Antimi- carpals on the biological activity of Porphyromonas gingi-
crobial efficacy of five essential oils against oral pathogens: valis and other periodontopathic bacteria. Oral Microbiol
An in vitro study. Eur J Dent 2013; 7: S71–S77. Immunol 2006; 21: 159–163.
38. MULAS M, MELIS RAM. Essential oil composition of myrtle 58. HENDRY E, WORTHINGTON T, CONWAY BR, LAMBERT P.
(Myrtus communis) leaves. J Herbs Spices Med Plants 2011; Antimicrobial efficacy of eucalyptus oil and 1, 8-cineole
17: 21–34. alone and in combination with chlorhexidine digluconate
39. FANI MM, KOHANTEB J, ARAGHIZADEH A. Inhibitory activity against microorganisms grown in planktonic and biofilm cul-
of Myrtus communis oil on some clinically isolated oral tures. J Antimicrob Chemother 2009; 64: 1219–1225.
pathogens. Med Princ Pract 2014; 23: 363–368. 59. TAJIDIN E. Chemical composition and citral content in
40. GURSOY UK, GURSOY M, GURSOY OV, CAKMAKCI L, KONO- lemongrass (Cymbopogon citratus) essential oil at three
NEN E, UITTO VJ. Anti-biofilm properties of Satureja horten- maturity stages. Afr J Biotechnol 2012; 11: 2685–2693.
sis L. essential oil against periodontal pathogens. Anaerobe 60. GOYAL R, ANAND M. Antibacterial effect of lemongrass oil
2009; 15: 164–167. on oral microoganisms: an in vitro study. J Pharm Sci Innov
41. HEDAYATI A, KHOSROPANAH H, BAZARGANI A, ABED M, 2013; 2: 41–43.
EMAMI A. Assessing the antimicrobial effect of the essential 61. SATTHANAKUL P, TAWEECHAISUPAPONG S, PAPHANGKORAKIT J,
oil of myrtus communis on the clinical isolates of porphy- PESEE M, TIMABUT P, KHUNKITTI W. Antimicrobial effect of
romonas gingivalis: an in vitro study. Jundishapur J Nat lemongrass oil against oral malodour micro-organisms and
Pharm Prod 2013; 8: 165–168. the pilot study of safety and efficacy of lemongrass mou-
42. AMIRI H. Essential oils composition and antioxidant proper- thrinse on oral malodour. J Appl Microbiol 2015; 118: 11–17.
ties of three thymus species. Evid Based Complement Alternat 62. WONGSARIYA K, LOMARAT P, BUNYAPRAPHATSARA N, SRISUKH
Med 2012; 2012: 728065. V, CHOMNAWANG MT. Evaluation of Thai spice essential oils
43. FANI M, KOHANTEB J. In vitro antimicrobial activity of thy- and their active compounds for anti-cariogenic activity and
mus vulgaris essential oil against major oral pathogens. Evid mechanism of action. J Essent Oil Bear Pl 2014; 17: 1064–
Based Complement Altern Med 2017; 22: 660–666. 1074.
44. SHAPIRO S, GUGGENHEIM B. The action of thymol on oral 63. DANY SS, MOHANTY P, TANGADE P, RAJPUT P, BATRA M.
bacteria. Oral Microbiol Immunol 1995; 10: 241–246. Efficacy of 0.25% lemongrass oil mouthwash: a three arm
45. DIDRY N, DUBREUIL L, PINKAS M. Activity of thymol, car- prospective parallel clinical study. J Clin Diagn Res 2015; 9:
vacrol, cinnamaldehyde and eugenol on oral bacteria. Pharm ZC13–ZC17.
Acta Helv 1994; 69: 25–28. 64. ANAND KM, GOYAL R, BHAT GS, KAMATH S, AGGARWAL M,
46. GRAZIANO TS, CALIL CM, SARTORATTO A, FRANCO GC, BHANDARKAR MA, MAHIMA BS, SUKREETH S. Antioxidant
GROPPO FC, COGO-MULLER K. In vitro effects of Melaleuca property of a novel lemongrass oil mouth wash: an experi-
alternifolia essential oil on growth and production of volatile mental study. Recent Res Sci Technol, 2011; 3.
sulphur compounds by oral bacteria. J Appl Oral Sci 2016; 65. TAWEECHAISUPAPONG S, AIEAMSAARD J, CHITROPAS P, KHUN-
24: 582–589. KITTI W. Inhibitory effect of lemongrass oil and its major
47. TAKARADA K, KIMIZUKA R, TAKAHASHI N, HONMA K, OKUDA constituents on Candida biofilm and germ tube formation. S
K, KATO T. A comparison of the antibacterial efficacies of Afr J Bot 2012; 81: 95–102.
essential oils against oral pathogens. Oral Microbiol Immunol 66. ANAND KM, BHAT GS, PENTAPATI CK, GOYAL R. Antiplaque
2004; 19: 61–64. efficacy of lemongrass oil mouthwash – an in-vitro study.
48. HAMMER KA, DRY L, JOHNSON M, MICHALAK EM, CARSON Glob J Med Res 2012; 12.
CF, RILEY TV. Susceptibility of oral bacteria to Melaleuca 67. ZAMIRAH Z-A, SHAHIDA M-S, FADZILAH A, ABDUL M, WAN
alternifolia (tea tree) oil in vitro. Oral Microbiol Immunol AIDA WAN M, IBRAHIM J. Anti-bacterial activity of cinnamon
2003; 18: 389–392. oil on oral pathogens. Open Conf Proc J 2013; 4: 12–16.
49. FORRER M, KULIK EM, FILIPPI A, WALTIMO T. The antimi- 68. WANG Y, ZHANG Y, SHI YQ, PAN XH, LU YH, CAO P.
crobial activity of alpha-bisabolol and tea tree oil against Antibacterial effects of cinnamon (Cinnamomum zeylan-
Solobacterium moorei, a Gram-positive bacterium associated icum) bark essential oil on Porphyromonas gingivalis.
with halitosis. Arch Oral Biol 2013; 58: 10–16. Microb Pathog 2018; 116: 26–32.
50. ARWEILER NB, DONOS N, NETUSCHIL L, REICH E, SCULEAN 69. LEBEL G, HAAS B, ADAM AA, VEILLEUX MP, LAGHA AB,
A. Clinical and antibacterial effect of tea tree oil–a pilot GRENIER D. Effect of cinnamon (Cinnamomum verum) bark
study. Clin Oral Investig 2000; 4: 70–73. essential oil on the halitosis-associated bacterium
Effect of essential oils on halitosis 11

Solobacterium moorei and in vitro cytotoxicity. Arch Oral 88. AMORIM CVGD, AUN CE, MAYER MPA. Susceptibility of
Biol 2017; 83: 97–104. some oral microorganisms to chlorhexidine and para-
70. LEE SK, TEOH EC, RAZALI M, ZAINAL-ABIDIN Z, MOHD-SAID monochlorophenol. Brazilian Oral Res 2004; 18: 242–246.
S. Antibacterial Activity of Clove Essential Oil on Anaerobic 89. HAAS AN, WAGNER TP, MUNIZ FWMG, FIORINI T, CAVAGNI
Oral Pathogens IADR Asia/Pacific Region (APR) Regional J, CELESTE RK. Essential oils-containing mouthwashes for
Meeting and Co-Annual Scientific Meeting of IADR Divi- gingivitis and plaque: Meta-analyses and meta-regression. J
sions. 2013. Dent 2016; 55: 7–15.
71. MOON S-E, KIM H-Y, CHA J-D. Synergistic effect between 90. PITTS G, PIANOTTI R, FEARY TW, MCGUINESS J, MASURAT T.
clove oil and its major compounds and antibiotics against The in vivo effects of an antiseptic mouthwash on odor-pro-
oral bacteria. Arch Oral Biol 2011; 56: 907–916. ducing microorganisms. J Dent Res 1981; 60: 1891–1896.
72. ZHANG Y, WANG Y, ZHU X, CAO P, WEI S, LU Y. Antibacte- 91. FISCHMAN SL, AGUIRRE A, CHARLES CH. Use of essential oil-
rial and antibiofilm activities of eugenol from essential oil of containing mouthrinses by xerostomic individuals: determi-
Syzygium aromaticum (L.) Merr. & L. M. Perry (clove) leaf nation of potential for oral mucosal irritation. Am J Dent
against periodontal pathogen Porphyromonas gingivalis. 2004; 17: 23–26.
Microb Pathog 2017; 113: 396–402. 92. SABAU R, ORMENISAN A, MONEA A, SZEKELY M, COSARCA A,
73. HANAFIAH RM, AZIZAN N, MOHD-SAID S, ZAINAL-ABIDIN Z. IONESCU TP, BERESESCU G, DALAI CE. Effect of essential oil
In-vitro inhibitory effect of Cinnamomum zeylanicum and mouthwash on halitosis. Rev Chim 2017; 68: 518–521.
Eugenia caryophyllata oils on multispecies anaerobic oral 93. HUR MH, PARK J, MADDOCK-JENNINGS W, KIM DO, LEE
biofilm. J Int Dent Medical Res 2019; 12: 411–417. MS. Reduction of mouth malodour and volatile sulphur
74. CHA JD, JEONG MR, JEONG SI, MOON SE, KIL BS, YUN SI, compounds in intensive care patients using an essential oil
LEE KY, SONG YH. Chemical composition and antimicrobial mouthwash. Phytother Res 2007; 21: 641–643.
activity of the essential oil of Cryptomeria japonica. Phy- 94. AZAD MF, SCHWIERTZ A, JENTSCH HFR. Adjunctive use of
tother Res 2007; 21: 295–299. essential oils following scaling and root planing -a randomized
75. CHA JD, JUNG EK, KIL BS, LEE KY. Chemical composition clinical trial. BMC Complement Altern Med 2016; 16: 171.
and antibacterial activity of essential oil from Artemisia fed- 95. AL‐BAYATY F, TAIYEB‐ALI T, ABDULLA M, B MAHMUD Z,
dei. J Microbiol Biotechnol 2007; 17: 2061–2065. MARA T, ALAM SELANGOR S, EHSAN D. Antibacterial effects
76. KIM K-H, KIM B-C, SHIN C-G, JEONG S-I, KIM H-J, JU Y-S. of Oradex, Gengigel and Salviathymol‐n mouthwash on den-
Susceptibility of oral bacteria to essential oil of Artemisia tal biofilm bacteria. Afr J Microbiol Res 2011; 5: 636–642.
capillaris thunb. Korean J Oriental Med 2004; 25: 121–128. 96. CEYLAN E, FUNG DYC. Antimicrobial activity of spices. J
77. JUNG E-K. Chemical composition and antimicrobial activity Rapid Meth Aut Mic 2004; 12: 1–55.
of the essential oil of Chrysanthemum indicum against oral 97. SIKKEMA J, WEBER FJ, HEIPIEPER HJ, DEBONT JAM. Cellular
bacteria. J Bacteriol Virol 2009; 39: 61–69. toxicity of lipophilic compounds - mechanisms, implications,
78. AZEEZ SH, GAPHOR SM. Evaluation of antibacterial effect and adaptations. Biocatalysis 1994; 10: 113–122.
against porphyromonas gingivalis and biocompatibility of 98. BASSOLE IHN, LAMIEN-MEDA A, BAYALA B, TIROGO S, FRANZ
essential oil extracted from the gum of Pistacia atlantica kur- C, NOVAK J, NEBIE RC, DICKO MH. Composition and
dica. Biomed Res Int 2019; 2019: 11. Antimicrobial Activities of Lippia multiflora Moldenke,
79. HANS VM, GROVER HS, DESWAL H, AGARWAL P. Antimicro- Mentha x piperita L. and Ocimum basilicum L. essential oils
bial efficacy of various essential oils at varying concentra- and their major monoterpene alcohols alone and in combi-
tions against periopathogen porphyromonas gingivalis. J nation. Molecules 2010; 15: 7825–7839.
Clin Diagn Res 2016; 10: ZC16–ZC19. 99. PEI RS, ZHOU F, JI BP, XU J. Evaluation of combined
80. WANG X, MITSUNAGA T, YAMAUCH K. Antibacterial activity antibacterial effects of eugenol, cinnamaldehyde, thymol, and
of selected essential oils against streptococcus sobrinus and carvacrol against E. coli with an improved method. J Food
porphyromonas gingivalis. J Pharm Sci Emerg Drugs 2016; 4. Sci 2009; 74: M379–383.
81. AZIZAN N, MOHD SAID S, ZAINAL ABIDIN Z, JANTAN I. Com- 100. WENDAKOON CN, SAKAGUCHI M. Combined effect of sodium
position and antibacterial activity of the essential oils of chloride and clove on growth and biogenic amine formation
orthosiphon stamineus benth and ficus deltoidea jack against of enterobacter aerogenes in mackerel muscle extract. J Food
pathogenic oral bacteria. Molecules 2017; 22: 2135. Prot 1993; 56: 410–413.
82. ALVIANO WS, MENDONCA-FILHO RR, ALVIANO DS, BIZZO 101. PARK SN, LIM YK, FREIRE M, CHO E, JIN D, KOOK JK. Antimi-
HR, SOUTO-PADRON T, RODRIGUES ML, BOLOGNESE AM, crobial effect of linalool and a-terpineol against periodonto-
ALVIANO CS, SOUZA MM. Antimicrobial activity of Croton pathic and cariogenic bacteria. Anaerobe 2012; 18: 369–372.
cajucara Benth linalool-rich essential oil on artificial biofilms 102. MAQUERA-HUACHO PM, TONON CC, CORREIA MF, FRANCIS-
and planktonic microorganisms. Oral Microbiol Immunol CONI RS, BORDINI EAF, MARCANTONIO E, SPOLIDORIO DMP.
2005; 20: 101–105. In vitro antibacterial and cytotoxic activities of carvacrol
83. BARDAJI DKR, REIS EB, MEDEIROS TCT, LUCARINI R, and terpinen-4-ol against biofilm formation on titanium
CROTTI AEM, MARTINS CHG. Antibacterial activity of com- implant surfaces. Biofouling 2018; 34: 699–709.
mercially available plant-derived essential oils against oral 103. CIANDRINI E, CAMPANA R, FEDERICI S, MANTI A, BATTISTELLI
pathogenic bacteria. Nat Prod Res 2016; 30: 1178–1181. M, FALCIERI E, PAPA S, BAFFONE W. In vitro activity of Car-
84. KHONGKHUNTHIAN S, SOOKKHEE S, OKONOGI S. Antimicrobial vacrol against titanium-adherent oral biofilms and plank-
activities against periodontopathogens of essential oil from tonic cultures. Clin Oral Investig 2014; 18: 2001–2013.
lemon grass (Cymbopogon citratus (DC.) Stapf.). J Nat Sci 104. OSAWA K, YASUDA H, MORITA H, TAKEYA K, ITOKAWA H.
2008; 8. Macrocarpals H, I, and J from the leaves of eucalyptus glob-
85. ALI HS, KAMAL MM, MOHAMED SB. In vitro clove oil activity ulus. J Nat Prod 1996; 59: 823–827.
against periodontopathic bacteria. J Sci Tech 2009; 10: 1–7. 105. BARRA A. Factors affecting chemical variability of essential
86. JUIZ PJ, LUCCHESE AM, GAMBARI R, PIVA R, PENOLAZZI L, oils: a review of recent developments. Nat Prod Commun
DI CIANO M, UETANABARO AP, SILVA F, AVILA-CAMPOS MJ. 2009; 4: 1147–1154.
Essential oils and isolated compounds from Lippia alba 106. HAMMER KA, CARSON CF, RILEY TV, NIELSEN JB. A review
leaves and flowers: antimicrobial activity and osteoclast of the toxicity of Melaleuca alternifolia (tea tree) oil. Food
apoptosis. Int J Mol Med 2015; 35: 211–217. Chem Toxicol 2006; 44: 616–625.
87. THAWEBOON S, THAWEBOON B, OCIMUM AMERICANUM L. 107. TISSERAND R, YOUNG R. 5 - The skin. In: TISSERAND R,
Essential oil exhibits antimicrobial activity against oral bac- YOUNG R, eds. Essential oil safety, 2nd edn. St. Louis:
teria related to periodontal disease. Adv Mat Res 2014; Churchill Livingstone, 2014; 69–98.
1025–1026: 755–759.

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