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O.S.T. - T.D.

J
Dcembre/December 2012, Vol..35, N140

Antibacterial activity of essential oils against periodontal


pathogens : a qualitative systematic review
L. LAKHDAR, M. HMAMOUCHI, S. RIDA, O. ENNIBI

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.

1. Dpt of Periodontology, 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

Rsum
Activit antibactrienne des huiles essentielles contre les pathognes parodontaux :
revue qualitative systmatique
Les maladies parodontales sont parmi les maladies infectieuses les plus communes, qui entranent la
destruction des tissus parodontaux. Aujourdhui, il est bien tabli que les bactries anarobies gram
ngatif (A ggregatibacter actinomecetemcomitans, Porphyromonas gingivalis, Fusobacterium
nucleatum), isoles partir des lsions parodontales, sont lies lapparition et la progression de la
maladie parodontale. Compte tenu de lincidence des parodontites, de la rsistance croissante des bactries orales aux antibiotiques et des effets secondaires de certains agents antibactriens frquemment
utiliss en dentisterie, la recherche dun nouvel agent thrapeutique alternatif, efficace et sur, pour la
prvention et le traitement de ces maladies, simpose. Les huiles essentielles, utilises en mdecine
traditionnelle, peuvent tre considres comme une bonne alternative thrapeutique.
Au Maroc, grand producteur dhuiles essentielles, en raison de la haute prvalence des parodontites
agressives causes par des bactries parodontales virulentes, isoles partir de poches parodontales
chez des adolescents marocains, et pour toutes les raisons voques ci-dessus, la recherche dun nouvel agent naturel est devenue une ncessit.
Dans cette revue de littrature de type qualitative systmatique, seront exposes, la virulence et la
rsistance accrue des pathognes parodontaux impliqus dans les parodontites, justifiant lutilisation
de tels agents base dhuiles essentielles. Seront galement dcrites et discutes, des tudes
dmontrant lefficacit de ces mdicaments base de plantes sur les bactries parodontopathognes.

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Mots-cls :
Biofilms,
parodontal,
pathognes,
huiles essentielles

Antibacterial activity...

Introduction

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 microbial 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 mechanical 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 planktonic cells, containing different complex species 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 pathogens within biofilm. The mechanical plaque
control is not properly practiced by most
individuals (1, 2, 3). They particularly concentrate on the solid surfaces of the mouth, which
provide an excellent surface for the growth of
biofilm but not the only source of bacteria colonizing 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, cetylpirinidium 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 mouthwash 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 periodontal 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-negative, 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 salivary 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 debridement, the microorganisms are inaccessible to
antimicrobial agents and host defense particularly phagocytozing leucocytes (PMNLs, macrophages) (12).
The subgingival biofilm is composed of toothassociated plaque, attached to the root surface. This zone is an extension of the biofilm

O.S.T. - T.D.J Dcembre/December 2012 Vol..35, N140

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Antibacterial activity...

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 organisms, in the depths of pocket, unattached,
loosely attached, or as planktonic cells, may
be observed. This region consists of motile species, 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 different antimicrobial agents. At the 1996 world
Workshop in Periodontics (14, 15), these species were designated as periodontal pathogens:
Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis and Bacteroides forsythus. They were strongly associated with periodontal 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 species such as F. nucleatum, Campylobacter
rectus, P. intermedia, P. nigrescens, Eubacterium nodatum, P. micros and various spirochetes 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 microbiota (1721, 22, 23, 24).
SOCRANSKY, HAFFAJEE et al. (25) have described specific associations among bacterial species organized as complexes within subgingival
biofilm. Six complexes were recognized, including the actinomyces, a yellow complex (Streptococcus sanguis, S. oralis, S. mitis, S. gordonii
and S. intermedius), a green complex (Capno-

40

cytophaga species, Campylobacter concisus,


Eikenella corrodens and Actinobacillus actinomycetemcomitans serotype a), a purple complex ( Veillonella parvula and Actinomyces
odontolyticus), an orange complex (Fusobacterium nucleatum/periodonticum subspecies,
Prevotella intermedia, Prevotella nigrescens and
Peptostreptococcus micros, Eubacterium nodatum, Campylobacter rectus, Campylobacter showae, Streptococcus constellatus and Campylobacter gracilis) and red complex (Bacteroides
forsythus, Porphyromonas gingivalis and Treponema 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 Actinomyces, 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 subgingival 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 periodontal attachment loss, in young Moroccan
patients. All these factors emphasize the complexity of subgingival dental plaque.
Antimicrobial resistance of
periopathogens in biofilm
It has been recognized that the indiscriminate
use of antimicrobials can lead to the development of resistant bacteria. However, the
mechanisms of resistance to antimicrobials of
organisms growing in biofilm are not entirely

O.S.T. - T.D.J Dcembre/December 2012 Vol..35, N140

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Antibacterial activity...

clear.
Antibiotics have been and continue to be the
only effective treatment of periodontal infections caused by periodontal bacteria in biofilm.
However, sufficient evidence exists that antibiotic resistance has increased in the periodontal flora over the last decades (33). Recent
studies have found that periodontal micro-organisms, in patients with periodontal infections,
exhibit moderate susceptibilities to clindamycin,
metronidazol and amoxicillin (34, 35), probably
because of the widespread use of these antibiotics. Other earlier studies showed a resistance of periodontal flora to penicillin and tetracycline (36, 37).
For many years, it has been shown that organisms 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 resistance 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, temperature, 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 resistance due to the horizontal acquisition of genetic material from other bacteria (33). This
acquisition of a genetic element that encodes
antibiotic resistance, from another micro-organism, 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 antibiotic 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 efficacy of a considerable number of essential oils on
periodontal bacteria (table 1).

Table 1 : Studies showing antimicrobial activity (MIC) of some essential oils on periodontal pathogens

Essential oil

Periopathogens Tested

Minimum Inhibitory
Concentrations (MIC)

Satureja hortensis L.

Aa, Pg, Pm, Tf, Fn, Pi, Pn

<0,125 l/ml

Salvia fruticosa M.

Aa, Pg, Pm, Tf, Fn, Pi, Pn

8 l/ml

Lavandula stoechas L.

Aa, Pg, Pm, Tf, Fn, Pi, Pn

4 l/ml

Myrtus communis L.

Aa
Pg
Pm
Tf
Fn
Pi
Pn
Aa, Pg, Pm, Tf, Fn, Pi, Pn

2-1 l/ml
0,25-2 l/ml
0,5-2 l/ml
0,25 l/ml
0,25-0,5 l/ml
2 l/ml
1-2 l/ml
4 l/ml

Juniperus communis L.
sarriette commune *

O.S.T. - T.D.J Dcembre/December 2012 Vol..35, N140

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Studies
Gursoy et al 2009 (44)

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Antibacterial activity...

Table 1 : Suite

Periopathogens Tested

Minimum Inhibitory
Concentrations (MIC)

Menthol, eucalyptol

En

16/128 g/ml

Thymol

Tf

64/ 128 g/ml

Prevotella species
Pg, fusobacterium species
campylobacter species

256/512 g/ml

Pg

1 mg/ml

A a, Fn, Pi, Pg

0,025- 0,05 mg/ml

Essential oil of
Artemisia feddei

Aa
Fn
Pi
Pg

0,8 mg/ml
0,025 mg/ml
0,025 mg/ml
0,1 mg/ml

Cha JD et al 2007 (48)

Linalool-rich essential
Croton cajucara *

Pg

31,2 g/ml

Alviano et al 2005 (49)

Obligate anaerobic bacteria

0.025 to 0.05 mg/mL

Cha JD et al 2005 (50)

Aa, Fn, Pg

0,03%

Aa
Pg
Fn

0,25-0,5 %
0,13- 0,25 %

Eucalyptus radiata oil


eucalyptus *

Aa
Pg
Fn

0,50%
0,25-0,5 %
0,13- 0,25 %

Lavandula officilalis oil


lavandula *

Aa

0,50%

Pg

0,5- 1 %

Fn

0,50%

Aa

0,50%

Pg

0,5- 1 %

Fn

0,50%

Aa, capnocytophaga, Ec,


fusobacterium spp, Pi

0,003- 2%

Essential oil

Listerine

Citrus oil
Essential oil of
Cryptomeria japonica

Essential oil of Artemisia


lavandulaefolia

Leptospermum scoparium oil


manuka*
Melaleuca alternifolia oil
tea tree *

Romarinus officilalis oil


romarinus *

Melaleuca alternifolia

42

Studies
Haffajee AD. et coll 2008
(45)

Mizrahi et al 2006 (46)


Cha JD et coll 2007 (47)

Takarada K. et coll 2004


(51)

0,06%

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Hammer KA. et coll 2003


(52)

Antibacterial activity...

Table 1 : Suite

Periopathogens Tested

Minimum Inhibitory
Concentrations (MIC)

Aa, Pg

0,11%

Pa

0,20%

Fn

> 0,6 %

Peppermint oil

Obligate anaerobe : Fn, Pi, Pg,


Pa, Pb, Sa, Pn, Tv
Capnophilic microaerophiles :
Aa, cap, Ec

0,1- 0,3 %

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 %

Essential oil
Australian tea tree oil

Studies
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

However, the susceptibility of a given organism to essential oils depends on numerous


factors; the most important ones are the properties of the essential oil and the microorganism 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 l/ml for A.
actinomycetemcomitans, demonstrating higher
efficacy in comparison with some Antibiotics,
such as Doxycycline, Ampicillin/sulbactam and
Azithromycin (MIC=1 l/ml, 0,75 l/ml, 3 l/ml)
tested against oral strains of A. actinomycetemcomitans (55).
Divergent results, found in the studies described 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 constituents may be involved (57). The hydrophobicity, important property of essential oils and
their constituents, enables them to partition in
the lipids of bacterial cell membrane and mitochondria 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) demonstrated that mouthwashes, especially essentialoil containing mouthrinse, kill almost all organisms 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

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Antibacterial activity...

References

affected by biofilm formation.


Therefore, the use of essential oil mouthrinses
may have benefits on plaque reduction (6068) 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 mouthwashes penetrate the subgingival area only
minimally. The crevicular fluid outflow would
dilute the subgingivally applied antiseptics
within minutes (72). Thus, the use of mouthrinse cannot be expected to provide a therapeutic 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 composition 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 constituents 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 establish whether they offer therapeutic or preventive benefits for periodontitis. In particular,
studies with adequate statistical power, blinding, standardization of purified compounds, and
quality control would be for great value.
Today, Listerine is the only commercial essential 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 investigating a novel antiseptic agent containing Moroccan essential oils by testing their activity on
periodontal pathogens in vitro and in vivo.

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