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Antibacterial activity of essential oils against periodontalpathogens : a qualitative systematic review

L. LAKHDAR, M. HMAMOUCHI, S. RIDA, O. ENNIBI1. 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-cls :Biofilms,parodontal,pathognes,huiles essentielles

O.S.T. - T.D.J

Dcembre/December 2012, Vol..35, N140

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.

RsumActivit 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 (Aggregatibacter 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 bac-

tries 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 laprvention 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 nou-

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

Periodontitis is infectious and inflammatory

disease affecting tooth-supporting tissues,

causing alveolar bone loss and connectivetissue 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-tonic 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 ofbiofilm 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 severalresearch 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 theseanaerobic 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 andcomplexity of subgingival biofilm

The subgingival biofilm is a section of dentalplaque 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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found above the gingival margin and may be

quite similar in bacterial composition. A second

zone, epithelial cell-associated biofilm, can beobserved 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. actinomycetemcomitansand P. gingivalisare

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. microsand 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 (1721, 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 Actinobacil lus actino-

mycetemcomitansserotype a), a purple com-plex (Veillonella parvula and Ac tinomyces

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 gingivalisand Trepo-

nema denticola). KOLENBRANDER et al. (26)

indicated that each strain of oral bacteria hasa 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 ascoaggregation (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 ofperiopathogens 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


40


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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).


41

Essential oil Periopathogens TestedMinimum Inhibitory

Concentrations (MIC)Studies

Satureja hortensis L. Aa, Pg, Pm, Tf, Fn, Pi, Pn


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42

Table 1 : Suite

Essential oil Periopathogens Tested Minimum InhibitoryConcentrations (MIC)

Studies

Menthol, eucalyptol En 16/128 g/ml

Thymol Tf 64/ 128 g/ml

Listerine Prevotella species 256/512 g/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 g/ml Alviano et al 2005 (49)

Essential oil ofArtemisia

lavandulaefolia

Obligate anaerobic bacteria 0.025 to 0.05 mg/mL Cha JD et al 2005 (50)

Leptospermum scopariumoil

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 alternifoliaoil

tea tree *

Eucalyptus radiataoil

eucalyptus *

Lavandula officilalisoillavandula *

Romarinus officilalisoil

romarinus *


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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 0,6 %

Peppermint oil Obligate anaerobe : Fn, Pi, Pg,

Pa, Pb, Sa, Pn, Tv

0,1- 0,3 %

Capnophilic microaerophiles :

Aa ca Ec

Sage oil Fn, Pi, Pg, Pa, Sa, Pn, Tv, Aa,

ca 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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affected by biofilm formation.

Therefore, the use of essential oil mouthrinses

may have benefits on plaque reduction (60-

68) 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 noevidence 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-reducedabitility 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, andquality 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.


44

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