Antibacterial activity of essential oils against periodontal pathogens: a qualitative systematic review

Abstract

Periodontal diseases are among the most common infectious diseases that lead to the destruction of periodontal tissues. Anaerobic gram-negative bacteria (Aggregatibacter actinomecetemcomitans, Porphyromonas gingivalis, Fusobacterium nucleatum...) isolated from periodontal lesions, have been shown to be related to the onset and progression of periodontal disease. Given the incidence of periodontitis, increased resistance of oral bacteria to antibiotics and adverse effects of some antibacterial agents currently used in dentistry, there is a need for alternative products that are safe and effective, for prevention and treatment of these diseases. Essential oils considered traditional medicines are viewed as good alternatives. In Morocco, a wide producer of essential oils, the high prevalence of aggressive periodontitis, related to virulent periodontal bacteria isolated from pockets in Moroccan adolescents and because of the reasons evoked above, the search of a new natural agent has become a necessity. In this qualitative systematic review, the virulence and increased antibiotic resistance of periopathogens, involved in periodontitis, will be exposed, justifying the use of alternative natural agents such as essential oils-based. Studies that have investigated the efficacy of such plant-derived medicines on periodontal pathogens will be described and discussed.

Full text

Copyright © 2012 APIDPM Santé tropicale. Tous droits réservés.
Antibacterial activity of essential oils against periodontal
pathogens : a qualitative systematic review
L. LAKHDAR¹, M. HMAMOUCHI², S. RIDA³, O. ENNIBI¹
1. Dpt of Periodon-
tology, Faculty of
Dentistry, Mohammed V
University, Rabat,
Morocco
2. Dpt of medical
biology, Faculty of
Medicine and pharmacy,
Rabat, Morocco
3. Faculty of Dentistry,
Rabat, Morocco
Keywords :
Biofilms,
periodontal,
pathogens,
essential oils
Mots-clés :
Biofilms,
parodontal,
pathogènes,
huiles essentielles
• O.S.T. - T.D.J
Décembre/December 2012, Vol..35, N°140 •
Abstract
Periodontal diseases are among the most common infectious diseases that lead to the destruction of
periodontal tissues. Anaerobic gram-negative bacteria (
Aggregatibacter actinomecetemcomitans,
Porphyromonas gingivalis, Fusobacterium nucleatum
…) isolated from periodontal lesions, have been
shown to be related to the onset and progression of periodontal disease. Given the incidence of perio-
dontitis, increased resistance of oral bacteria to antibiotics and adverse effects of some antibacterial
agents currently used in dentistry, there is a need for alternative products that are safe and effective,
for prevention and treatment of these diseases. Essential oils considered traditional medicines are
viewed as good alternatives. In Morocco, a wide producer of essential oils, the high prevalence of
aggressive periodontitis, related to virulent periodontal bacteria isolated from pockets in Moroccan
adolescents and because of the reasons evoked above, the search of a new natural agent has become
a necessity. In this qualitative systematic review, the virulence and increased antibiotic resistance of
periopathogens, involved in periodontitis, will be exposed, justifying the use of alternative natural
agents such as essential oils-based. Studies that have investigated the efficacy of such plant-derived
medicines on periodontal pathogens will be described and discussed.
Résumé
Activité antibactérienne des huiles essentielles contre les pathogènes parodontaux :
revue qualitative systématique
Les maladies parodontales sont parmi les maladies infectieuses les plus communes, qui entraînent la
destruction des tissus parodontaux. Aujourd’hui, il est bien établi que les bactéries anaérobies gram
négatif (A
ggregatibacter actinomecetemcomitans, Porphyromonas gingivalis, Fusobacterium
nucleatum
…), isolées à partir des lésions parodontales, sont liées à l’apparition et la progression de la
maladie parodontale. Compte tenu de l’incidence des parodontites, de la résistance croissante des bac-
téries orales aux antibiotiques et des effets secondaires de certains agents antibactériens fréquemment
utilisés en dentisterie, la recherche d’un nouvel agent thérapeutique alternatif, efficace et sur, pour la
prévention et le traitement de ces maladies, s’impose. Les huiles essentielles, utilisées en médecine
traditionnelle, peuvent être considérées comme une bonne alternative thérapeutique.
Au Maroc, grand producteur d’huiles essentielles, en raison de la haute prévalence des parodontites
agressives causées par des bactéries parodontales virulentes, isolées à partir de poches parodontales
chez des adolescents marocains, et pour toutes les raisons évoquées ci-dessus, la recherche d’un nou-
vel agent naturel est devenue une nécessité.
Dans cette revue de littérature de type qualitative systématique, seront exposées, la virulence et la
résistance accrue des pathogènes parodontaux impliqués dans les parodontites, justifiant l’utilisation
de tels agents à base d’huiles essentielles. Seront également décrites et discutées, des études
démontrant l’efficacité de ces médicaments à base de plantes sur les bactéries parodontopathogènes.

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
Periodontitis is infectious and inflammatory
disease affecting tooth-supporting tissues,
causing alveolar bone loss and connective
tissue destruction. The Primary etiologic agent
is dental biofilm, defined as a complex micro-
bial community composed of oral bacteria
organized in supra and subgingival biofilm.
The supragingival biofilm is attached to the
tooth surface and can be removed by mecha-
nical plaque control by daily tooth brushing
and interproximal cleaning devices. The nature
of subgingival biofilm is more complex with
both a tooth-associated and tissue-associated
biofilm separated by loosely bound or plank-
toni
c cells, containing different complex spe-
cies of virulent periopathogens. Therefore,
controlling the development of subgingival
biofilm seems to be more difficult because of
limited access of the areas colonized (cement,
periodontal pocket) and the virulence of patho-
gens within biofilm. The mechanical plaque
control is not properly practiced by most
individuals (1, 2, 3). They particularly concen-
trate on the solid surfaces of the mouth, which
provide an excellent surface for the growth of
biofilm but not the only source of bacteria colo-
nizing tooth surfaces (4). Therefore, the
adjunct use of antimicrobial agents might be
beneficial and help to reduce the accumulation
of subgingival biofilm on soft tissue surfaces of
the oral cavity, which are often hard to reach
areas by mechanical plaque control procedures.
Chemical agents such as chlorhexidine, cetyl-
pirinidium chloride, fluorides… have been used
to inhibit bacterial growth on oral surfaces.
Their prolonged use as adjuncts to mechanical
plaque control can cause side effects such as
tooth staining, taste alteration… In addition to
the development of antimicrobial resistance of
organisms in biofilm and the risk of oral cancer
associated with the alcohol content of mouth-
wash formulations.
In the last decades, the use of natural products
like essential oils as antibacterial agents is
increasing in medicine and dentistry. The
search of antimicrobial activity of essential oils
on subgingival biofilm, particularly on perio-
dontal bacteria, has been the subject of several
research studies all over the world.
In Morocco, one of the main producer countries
of essential oils, many researches and trials
have been accomplished on the safety and
antimicrobial activity of Moroccan plant extracts
and essential oils (5-10). However, their
antibacterial activity on periodontal pathogens
has been less studied. We are actually
searching, by in vitro trials, the antibacterial
activity of Moroccan essential oils on these
anaerobic organisms.
The objective of this qualitative systematic
review is to discuss the antibacterial activity of
essential oils on subgingival biofilm, particularly
on periodontal bacteria characterized by their
high complexity and therapeutic resistance.
Properties and
complexity of subgingival biofilm
The subgingival biofilm is a section of dental
plaque growing in subgingival environment. It
consists of a complex mixture of gram-nega-
tive, anaerobic bacteria and includes motile
species (11). Thus, the bacterial composition
and properties of this part of biofilm is different
from those of supragingival plaque. Access to
the oral cavity is limited, favoring anaerobic
development, limiting intraoral abrasion or sali-
vary host defense components. Nutrients are
available from the gingival crevicular fluid,
which increases in gingival inflammation. In
contrast to the supragingival biofilm, as long as
it is not disorganized by mechanical debride-
ment, the microorganisms are inaccessible to
antimicrobial agents and host defense particu-
larly phagocytozing leucocytes (PMNLs, macro-
phages) (12).
The subgingival biofilm is composed of tooth-
associated plaque, attached to the root surfa-
ce. This zone is an extension of the biofilm
• Antibacterial activity... •
39
Introduction

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
found above the gingival margin and may be
quite similar in bacterial composition. A second
zone, epithelial cell-associated biofilm, can be
observed lining the epithelial surface of the
periodontal pocket. A less dense zone of orga-
nisms, in the depths of pocket, unattached,
“loosely attached”, or as planktonic cells, may
be observed. This region consists of motile spe-
cies, predominantly various sizes and forms of
spirochetes (13). These zones, tooth-associated
and epithelial cell associated regions, as well as
the zone of non attaching motile organisms,
probably differ markedly in physiological state,
bacterial composition and their response to dif-
ferent antimicrobial agents. At the 1996 world
Workshop in Periodontics (14, 15), these spe-
cies were designated as periodontal pathogens:
Aggregatibacter actinomycetemcomitans, Por-
phyromonas gingivalis
and
Bacteroides forsy-
thus
. They were strongly associated with perio-
dontal disease status, disease progression and
unsuccessful therapy.
A. actinomycetemcomitans
and
P. gingivalis
are
considered to be exogenous and transmissible
periopathogens, while
B. forsythus
is regarded
as endogenous and opportunistic (American
Academy of Periodontology 1996). Other spe-
cies such as
F. nucleatum, Campylobacter
rectus, P. intermedia, P. nigrescens, Eubac-
terium nodatum, P. micros
and various spiroche-
tes also have a causative role in periodontal
diseases, but of less importance (16). Recently,
viruses including cytomegalovirus, Epstein-Barr
virus, papillomavirus and herpes simplex virus
have been proposed to be implicated in causing
periodontal diseases, possibly by changing the
host response to the local subgingival micro-
biota (17–21, 22, 23, 24).
SOCRANSKY, HAFFAJEE et al. (25) have descri-
bed specific associations among bacterial spe-
cies organized as complexes within subgingival
biofilm. Six complexes were recognized, includ-
ing the actinomyces, a yellow complex (
Strep-
tococcus sanguis, S. oralis, S. mitis, S. gordonii
and
S. intermedius
), a green complex (Capno-
cytophaga species,
Campylobacter concisus,
Eikenella corrodens
and
Actinobacillus actino-
mycetemcomitans
serotype a), a purple com-
plex (
Veillonella parvula
and
Actinomyces
odontolyticus
), an orange complex (
Fusobacte-
rium nucleatum/periodonticum subspecies,
Prevotella intermedia, Prevotella nigrescens
and
Peptostreptococcus micros, Eubacterium noda-
tum, Campylobacter rectus, Campylobacter sho-
wae, Streptococcus constellatus
and
Campylo-
bacter gracilis
) and red complex (
Bacteroides
forsythus, Porphyromonas gingivalis
and
Trepo-
nema denticola
). KOLENBRANDER et al. (26)
indicated that each strain of oral bacteria has
a defined set of coaggregation partners.
Certain complexes are observed together more
frequently than others in subgingival biofilm.
For example, it is rare to observe red complex
species without members of the orange
complex. Otherwise, members of the Actinomy-
ces, yellow, green and purple complexes are
unlikely found with members of the red
complex or even the red and orange complexes
(27). This cell to cell recognition is known as
coaggregation (13). Otherwise, within subgin-
gival biofilm, microorganisms show different
serotypes with different virulence such as
Aggregatibacter actinomycetemcomitans
.
Recent studies (28-32), realized in Morocco,
have shown the involvement of the JP2 clone
of
Aggregatibacter actinomycetemcomitans
in
aggressive periodontitis, particularly in perio-
dontal attachment loss, in young Moroccan
patients. All these factors emphasize the com-
plexity of subgingival dental plaque.
Antimicrobial resistance of
periopathogens in biofilm
It has been recognized that the indiscriminate
use of antimicrobials can lead to the develop-
ment of resistant bacteria. However, the
mechanisms of resistance to antimicrobials of
organisms growing in biofilm are not entirely
• Antibacterial activity... •
40

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
clear.
Antibiotics have been and continue to be the
only effective treatment of periodontal infec-
tions caused by periodontal bacteria in biofilm.
However, sufficient evidence exists that anti-
biotic resistance has increased in the perio-
dontal flora over the last decades (33). Recent
studies have found that periodontal micro-orga-
nisms, in patients with periodontal infections,
exhibit moderate susceptibilities to clindamycin,
metronidazol and amoxicillin (34, 35), probably
because of the widespread use of these anti-
biotics. Other earlier studies showed a resis-
tance of periodontal flora to penicillin and tetra-
cycline (36, 37).
For many years, it has been shown that orga-
nisms growing in biofilm are more resistant to
antimicrobial agents than the same species
growing in a planktonic state (13). There are
many factors that influence the increased resis-
tance of organisms in biofilms to antibiotics,
such : types of species, antibiotic molecules,
biofilms growing in different habitat … (27).
Slower rate of growth of bacterial species in
biofilm makes them less susceptible to many
antibiotics (38, 39). It appears to be one
important mechanism of resistance. Also, other
parameters, such: nutritional status, tempera-
ture, pH and prior exposure to subeffective
concentrations of antimicrobial agents, can
cause varied response to antibiotics within a
biofilm (40, 41, 42).
Antibiotic resistance may be classified into 3
groups: intrinsic, mutational and acquired resis-
tance due to the horizontal acquisition of gene-
tic material from other bacteria (33). This
acquisition of a genetic element that encodes
antibiotic resistance, from another micro-orga-
nism, is the most common process by which
antibiotic resistance is disseminated. The stable
structural properties and close proximity of the
bacterial cells within the biofilm appears to be
an excellent environment for horizontal gene
transfer, which can lead to the spread of anti-
biotic resistance genes amongst the biofilm
inhabitants (43). For these reasons, there is a
need for alternative natural agents such as
essential oils. Many studies have investigated
the efficacy of such plant-derived medicines on
periodontal pathogens.
Effect of essential oils
on periodontal bacteria
Several studies (45-53) have shown the effica-
cy of a considerable number of essential oils on
periodontal bacteria (table 1).
• Antibacterial activity... •
41
Essential oil Periopathogens Tested
Minimum Inhibitory
Concentrations (MIC)
Studies
Satureja hortensis L. Aa, Pg, Pm, Tf, Fn, Pi, Pn
<0,125 μl/ml
Salvia fruticosa M. Aa, Pg, Pm, Tf, Fn, Pi, Pn
8 μl/ml
Lavandula stoechas L. Aa, Pg, Pm, Tf, Fn, Pi, Pn
4 μl/ml
Myrtus communis L. Aa
2-1 μl/ml
Pg
0,25-2 μl/ml
Pm
0,5-2 μl/ml
Tf
0,25 μl/ml
Fn
0,25-0,5 μl/ml
Pi
2 μl/ml
Pn
1-2 μl/ml
Juniperus communis L.
sarriette commune *
Aa, Pg, Pm, Tf, Fn, Pi, Pn
4 μl/ml
Gursoy et al 2009 (44)
Table 1 : Studies showing antimicrobial activity (MIC) of some essential oils on periodontal pathogens

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
• Antibacterial activity... •
42
Table 1 : Suite
Essential oil Periopathogens Tested
Minimum Inhibitory
Concentrations (MIC)
Studies
Menthol, eucalyptol
En
16/128 μg/ml
Thymol
Tf
64/ 128 μg/ml
Listerine ®
Prevotella species
256/512 μg/ml
Pg, fusobacterium species
campylobacter species
Citrus oil
Pg
1 mg/ml Mizrahi et al 2006 (46)
Essential oil of
Cryptomeria japonica
A a, Fn, Pi, Pg
0,025- 0,05 mg/ml Cha JD et coll 2007 (47)
Aa
0,8 mg/ml
Fn
0,025 mg/ml
Pi
0,025 mg/ml
Pg
0,1 mg/ml
Linalool-rich essential
Croton cajucara *
Pg
31,2 μg/ml Alviano et al 2005 (49)
Essential oil of
Artemisia
lavandulaefolia
Obligate anaerobic bacteria
0.025 to 0.05 mg/mL Cha JD et al 2005 (50)
Leptospermum scoparium
oil
manuka*
Aa, Fn, Pg
0,03%
Aa
0,25-0,5 %
Pg
0,13- 0,25 %
Fn
0,06%
Aa
0,50%
Pg
0,25-0,5 %
Fn
0,13- 0,25 %
Aa
0,50%
Pg
0,5- 1 %
Fn
0,50%
Aa
0,50%
Pg
0,5- 1 %
Fn
0,50%
Melaleuca alternifolia
Aa, capnocytophaga, Ec,
fusobacterium spp, Pi
0,003- 2%
Hammer KA. et coll 2003
(52)
Haffajee AD. et coll 2008
(45)
Essential oil of
Artemisia feddei
Cha JD et al 2007 (48)
Takarada K. et coll 2004
(51)
Melaleuca alternifolia
oil
tea tree *
Eucalyptus radiata
oil
eucalyptus *
Lavandula officilalis
oil
lavandula *
Romarinus officilalis
oil
romarinus *

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
However, the susceptibility of a given orga-
nism to essential oils depends on numerous
factors; the most important ones are the pro-
perties of the essential oil and the micro-
organism itself (54).
As described in table 1, there are specific MICs,
for each type of periodontal bacteria tested,
related to different essential oils used. Some of
these MICs values seem to be interesting,
showing stronger antibacterial activity of some
essential oils in comparison with Antibiotics. In
fact, essential oil of
Satureja hortensia
(44)
(table 1) showed MIC<0,125 μl/ml for
A.
actinomycetemcomitans
, demonstrating higher
efficacy in comparison with some Antibiotics,
such as Doxycycline, Ampicillin/sulbactam and
Azithromycin (MIC=1 μl/ml, 0,75 μl/ml, 3 μl/ml)
tested against oral strains of
A. actinomyce-
temcomitans
(55).
Divergent results, found in the studies describ-
ed above, may be explained by the differences
between the types and numbers of bacterial
isolates tested in each study, and the methods
used, including the criteria for determining
MICs. Also, recent isolates may exhibit an
increased resistance against the antimicrobial
compounds, which possibly derives from their
recent interactions with host cells (56).
The mechanism of action of essential oils on
bacteria cells is not entirely understood.
Membrane disruption by the lipophilic consti-
tuents may be involved (57). The hydrophobi-
city, important property of essential oils and
their constituents, enables them to partition in
the lipids of bacterial cell membrane and mito-
chondria thus disturbing the structures and
making them more permeable (58). Otherwise,
the susceptibility of bacteria to any mouthrinses
depends on their growing form; planktonic or
biofilm forms. In fact, FINE et al (59) demons-
trated that mouthwashes, especially essential-
oil containing mouthrinse, kill almost all orga-
nisms in the planktonic form, while effects
on
the biofilm forms of the organisms were more
variable. This study supports the observation
that resistance to antimicrobial agents is
• Antibacterial activity... •
43
Table 1 : Suite
Essential oil Periopathogens Tested
Minimum Inhibitory
Concentrations (MIC)
Studies
Aa, Pg
0,11%
Pa
0,20%
Fn
> 0,6 %
Peppermint oil
Obligate anaerobe : Fn, Pi, Pg,
Pa, Pb, Sa, Pn, Tv
0,1- 0,3 %
Capnophilic microaerophiles :
Aa, cap, Ec
Sage oil
Fn, Pi, Pg, Pa, Sa, Pn, Tv, Aa,
cap, Ec
0,06-0,2 %
Thymol
Pn, Tv, Aa, Pg, Sa, Ec, Pa
0,02-0,03 %
Eugenol
Pn, Tv, Aa, Pg, Sa, Ec, Pa
0,05-0,14 %
Australian tea tree oil
Shapiro et al 1994 (53)
*: plant family, ®: commercial product, Aa :
Aggregatibacter actinomycetemcomitans
, Fn:
Fusobacterium nucleatum
, Pi:
Prevotella intermedia,
Ec:
Eikenella corrodens
, En:
Eubacterium nodatum
, Tf:
Tannerella forsythia
, Pg:
Porphyromonas gingivalis
, Pa:
Peptostreptococcus
anaerobius
, Pb:
Prevotella buccae
, Pn:
Prevotella nigrescens
, Sa:
Selenomas artemidis
, Td:
Treponema denticola
, Tv:
Treponema vincentil
,
Cap:
capnocytophaga

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• O.S.T. - T.D.J • Décembre/December 2012 Vol..35, N°140 •
affected by biofilm formation.
Therefore, the use of essential oil mouthrinses
may have benefits on plaque reduction (60-
6
8) affecting bacteria growing in supragingival
biofilm, but also the subgingival microbiota,
reducing the levels of total anaerobes, through
the disruption of the contiguous supragingival
plaque (69, 70, 71). However, essential mouth-
washes penetrate the subgingival area only
minimally. The crevicular fluid outflow would
dilute the subgingivally applied antiseptics
within minutes (72). Thus, the use of mouth-
rinse cannot be expected to provide a thera-
peutic benefit in the treatment of periodontitis
(73). Even in subgingival application, the effect
of an antiseptic on periodontitis has not been
demonstrated (74). It may however, partially
reach the subgingival bacteria, (with a mean
penetration of 70% on the total pocket depth)
and inflamed tissues that are otherwise
inaccessible (75, 76).
It has been showed that long term use of an
essential oil mouthwash is microbiologically
safe, with no change in the bacterial composi-
tion of supragingival plaque (77), and no
evidence of antimicrobial resistance (78). But
the data on the single therapeutic efficacy of
mouthwashes on periodontitis are scarce.
Despite their antimicrobial activity against a
wide spectrum of bacteria, essential oils may
also exert a cytotoxic effect, which depends on
the diversity of major and minor constituents
present in the essential oil. In fact, DUSAN et
al. (79) showed both antimicrobial activity and
detrimental effect on human cells for thyme oil,
and in contrast, no cytotoxic effect for its
component thymol as well as greatly-reduced
abitility to inhibit visible growth of the chosen
pathogen, with the doses used (80).
Conclusion
As demonstrated by examples in this review,
there is considerable evidence that essential
oils have strong antibacterial activity against
periodontal pathogens. However, numerous
factors can modify this efficacy, including the
complexity of subgingival biofilm, the consti-
tuents and doses used of essential oils and the
method of administration of the antiseptic
agent (mouthrinse, subgingival irrigation…).
Therefore, in order to develop these natural
products into solutions or gels for subgingival
irrigation, further studies are required to esta-
blish whether they offer therapeutic or preven-
tive benefits for periodontitis. In particular,
studies with adequate statistical power, blind-
ing, standardization of purified compounds, and
quality control would be for great value.
Today, Listerine
®
is the only commercial essen-
tial oil-based product recognized and the most
studied (81-85). However, its antibacterial
activity on periodontal bacteria is controversial.
Thus, our research team is currently investigat-
ing a novel antiseptic agent containing Moroc-
can essential oils by testing their activity on
periodontal pathogens in vitro and in vivo.
• Antibacterial activity... •
44
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