<i>Helicobacter Pylori</i> and Periodontal diseases: An update and proposal of a multidisciplinary clinical protocol

doi:10.4236/ojst.2013.36053

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Open Journal of Stomatology, 2013, 3, 318-322 OJST

http://dx.doi.org/10.4236/ojst.2013.36053 Published Online September 2013 (http://www.scirp.org/journal/ojst/)

Helicobacter Pylori and Periodontal diseases: An update

and proposal of a multidisciplinary clinical protocol

Sophie Marbaix1, Assem Soueidan1, Maya Romani2, Guillaume Campard1, Gilles Amador3,

Zahi Badran1

1Department of Periodontology (Inserm U791/UIC Odontologie/CHU de Nantes), Faculty of Dental Surgery, Nantes, France

2Department of Family medicine, American University of Beirut-Medical Centre, Beirut, Lebanon

3Department of Dental public health, Faculty of Dental Surgery (CHU de Nantes), Nantes, France

Email: [email protected]

Received 13 June 2013; revised 14 July 2013; accepted 1 August 2013

which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Helicobacter Pylori has been closely linked to chronic

gastritis, peptic ulcers and increased risk of gastric

carcinoma. Oral cavity, in particular dental plaque in

periodontal pockets, may be a possible reservoir har-

boring H. Pylori, and may therefore be involved in the

gastric reinfection by the bacterium, even after triple

therapy regimen. This report is an update of scientific

data showing the potential localization of H. Pylori in

the oral cavity of periodontitis patients. A multidisci-

plinary clinical protocol combining full-mouth disin-

fection and triple therapy is also suggested. This pro-

tocol could permit to enhance oral H. Pylori eradica-

tion.

Keywords: Periodontal; Triple Therapy; Full-Mouth

Disinfection

1. INTRODUCTION

Periodontal diseases are inflammatory chronic diseases

affecting teeth supportive tissues, and have infectious

bacterial etiology. It is initiated by oral bacterial biofilms

developing on dental roots. Early stage of the disease is

gingivitis, and is characterized by gingival inflammation

(swelling, redness, bleeding···). Individually susceptible

patients could develop Periodontitis, which implies al-

veolar bone loss and periodontal pockets formation

around affected teeth (Figure 1). Periodontopathogenic

bacteria (PB) are mainly anaerobic, Gram negative

strains developing subgingivally in periodontal pockets.

This subgingival environment is particularly favorable

for the survival and proliferation of non-aerobic strains.

Also, many locations in the oral cavity (OC), such as the

dorsum of the tongue are oxygen-poor sites. Helico-

Figure 1. Periodontitis affecting teeth supportive

tissues.

bacter Pylori (HP), as a gram-negative, microaerophilic,

spiral-shaped bacterium; could find adequate conditions

for colonization and proliferation in the OC. HP has been

implicated in the etiology of gastritis and peptic ulcers.

Its presence is also a risk factor for gastrointestinal can-

cers. Human infection by this pathogen could involve an

oral route, and the OC is an anatomical region with a

potential to harbor HP, in particular dental plaque (oral

biofilm).

Thus, it seems conceivable that oral health status and

different gingival clinical conditions may have an effect

on the presence of HP in oral biofilms, hence influencing

the process of HP gastric infection or reinfection [1,2] .

Many reports found that HP could colonize the healthy

OC or the subgingival periodontal pockets area. The lat-

ter could eventually serve as a bacterial reservoir. Ac-

cording to Savita et al. [3], subjects with periodontitis

harbor a number of HP significantly higher than subjects

without periodontitis. Also, reinfection of the gastroin-

testinal tract by HP from dental plaque could occur after

proper eradication regimen. Triple therapy (TT) has been

successfully used to eradicate gastric HP. TT is the most

common first line treatment recommended for H. Pylori

OPEN ACCESS

S. Marbaix et al. / Open Journal of Stomatology 3 (2013) 318-322 319

eradication, it consists of a proton pump inhibitor (PPI)

(lansoprazole 30 mg twice daily, omeprazole 20 mg twice

daily, pantoprazole 40 mg twice daily, rabeprazole 20 mg

twice daily) plus amoxicillin 1 gram twice daily and

clarithromycin 500mg twice daily for 7 to 14 days. Met-

ronidazole (500 mg twice daily) can be substituted for

amoxicillin in penicillin-allergic patients. A longer dura-

tion of treatment (14 versus 7 days) may be more effective

in curing infection, but this remains controversial. TT is

currently considered the gold standard reaching an eradi-

cation rate up to 80% [1,4]. However, in many cases, HP

is not completely eliminated after a single treatment, and

the recurrence of the HP infection has been well-docu-

mented [5]. Therefore, the OC has been suspected to be a

common source for reinfection of the stomach [2,6]. In

fact, bacteria developing in biofilm configuration (such

as in dental plaque) are much more resistant to antibiot-

ics than freely circulating bacteria [7].

Full mouth disinfection (FMD) is a periodontal clini-

cal protocol, combining mechanical antibacterial therapy

(scaling/root planning of dental roots) and antiseptic re-

gimen (chlorhexidine) to obtain PB eradication [8,9].

The mechanical debridement of all teeth is performed

within 24 h, in order to eradicate rapidly PB present in

dental biofilms, and thus preventing reinfection of treated

sites. Also, the adjunction of a systemic antibiotic pre-

scription to FMD (amoxicillin/metronidazole or azithro-

mycin) has been found to successfully enhance clinical

outcomes [10-12].

This article focuses on the specific association of

periodontal status and oral HP in the published scientific

literature. The rationale of considering periodontitis as a

risk factor for HP infections/reinfection will also be dis-

cussed, with an emphasis on the eventual clinical impli-

cations of this assumption. Finally, we suggest the merg-

ing of both FMD and TT regimen, in order to enhance

periodontal therapy outcome as well as eradication of HP.

2. HELICOBACTER PYLORI AND

PERIODONTAL DISEASES

2.1. Helicobacter Pylori in Periodontally Ill and

Healthy Patients

Several studies have evaluated the correlation between

the prevalence of HP and periodontal diseases. Conflict-

ing results could be observed in the literature, this could

be attributed to the diversity of the studied populations,

sample collection methods, and the specificity of the

methods used for HP detection [2,13]. Although it may

affect the presence of HP in dental plaque, few studies

have separately investigated supra and subgingival plaque,

which corresponds to different microenvironments when

availability of nutrients, oxygen and host mechanisms

are considered [14].

Souto et al. [2] performed a full-mouth clinical ex-

amination (six sites per tooth) to determine periodontal

health status and examined subjects with no history of

gastric symptoms, their results showed a higher preva-

lence of HP in subgingival biofilm of subjects with pe-

riodontitis compared to individuals with periodontal

health (50% versus 11% respectively), suggesting that

periodontal pockets and inflammation may favor HP

colonization. Another study by Riggio and Lennon [15]

examined the presence of H. Pylori in subgingival plaque

(sites with periodontal pocket depth ≥5 mm) of perio-

dontitis patients with no symptoms of gastritis or peptic

ulcer disease. This study found that 38% of subjects with

deep periodontal pockets were positive for HP. Conse-

quently, the authors concluded that subgingival plaque in

individuals presenting periodontitis may function as a

reservoir for HP.

Gebara et al. [14], found that more than 26% of HP

was detected in the OC of periodontitis patients (all posi-

tive for gastric HP), periodontitis and gingivitis showed a

high prevalence; however, no control group with healthy

patients were included. Al Asqah et al. [13] found that

periodontitis patients had a significantly higher percent-

age of HP in subgingival plaque samples in comparison

to periodontally healthy controls (79% versus 43% re-

spectively). Other studies failed to detect HP in the sub-

gingival plaque [16,17] or found no association between

periodontal status and the prevalence of the bacterium in

OC [18].

2.2. Relation between Gastric Infection and

Periodondal Disease

Umeda et al. [19] showed that more than 40 % of pa-

tients with history of gastritis or peptic ulcers had perio-

dontal pockets (>4 mm). Bruce et al. (54) found that

periodontal pockets ≥5 mm are associated with increased

odds of HP seropositivity. Also, a large epidemiological

investigation performed over 10,000 subjects [20], found

a positive link between HP associated gastric infection

and periodontal diseases. The latter may facilitate the HP

oro-gastric transmission and colonization of the bacteria

in the digestive tract. Also, periodontitis microenviron-

ment conditions could be favorable for HP multiplication,

thus increasing sufficiently to cause gastric infection

[21,22].

On the other hand, many studies [23-25] failed to es-

tablish a positive correlation between periodontal disease

and gastric infection.

3. TRIPLE THERAPY AND ORAL

HELICOBACTER PYLORI

3.1. Effect of Triple Therapy on Oral HP

It is still unclear whether TT affects HP in dental plaque.

Song et al. [26] found plaque samples negative for HP

S. Marbaix et al. / Open Journal of Stomatology 3 (2013) 318-322

320

only in patients who had recently been treated with TT.

But many reports, found a persistent oral HP after TT

[27-29]. More recently, a meta-analysis [30] confirmed

the close relationship between HP infection in the OC

and the stomach, and concluded that oral HP is more

difficult to eradicate than gastric HP and it may be a

source of reinfection. On the other hand, Umeda et al.

[19] reported that subjects with periodontal pockets re-

tained HP in the OC even after eradication of the bacte-

rium from the stomach. Similarly, Gebara et al. [1]

showed that 60% of subjects with periodontal disease

were still positive for HP DNA in their OC, whereas only

10% were positive in the stomach after triple therapy. In

a same way, Zarik et al. [5] revealed that 3 months after

triple therapy in the group of participants who did not

harbor HP in periodontal pockets, the eradication rate

was 87.4%. In contrast, the group positive for HP in the

subgingival plaque exhibited a significantly lower rate of

eradication (47.6%). Also, polyantibiotic systemic ther-

apy was considerably less efficient in the eradication of

HP from periodontal pockets, compared with its elimina-

tion in the stomach (33% and 87% respectively).

3.2. Effect of Periodontal Therapy on Prevention

of Gastric Helicobacter Pylori Recurrence

Few studies investigated the effect of periodontal therapy

on eradication of gastric HP. Zarik et al. [5], evaluated

the effectiveness of periodontal treatment and TT in

achieving complete elimination of gastric HP infection.

Participants positive for HP in the subgingival biofilm,

who had undergone basic periodontal therapy and a TT

regimen, showed a higher elimination rates compared to

the group who underwent TT alone (77.3% and 47.6%

respectively), thus suggesting that systemic antibiotic

polytherapy alone is not as effective in preventing the

reappearance of gastric HP in subjects positive for the

oral form of HP. A meta-analysis [31] concluded that

periodontal therapy reduces the relative risk of persis-

tence of gastric HP by 63%. Similar results were found

in a study with a two years follow-up [32].

Recently, a case series of 9 patients [33], investigated

whether full mouth ultrasonic debridement can eradicate

persistent oral HP after TT. Periodontal debridement was

able to eradicate HP from 88.3% of patients with gingi-

vitis, while it failed in eradicating the bacteria from the

OC of periodontitis group. Within the limits of this case

series, a single session of oral hygiene instruction com-

bined with full mouth periodontal debridement seemed to

promote a positive effect in eradicating HP only from

supragingival sites.

4. CLINICAL MULTIDISCIPLINARY

MANAGEMENT PROPOSAL

Actual consensus in Periodontology suggests that antibi-

otic regimen should be started immediately after me-

chanical periodontal treatment [34]. Thus, a complete

elimination of calculus and disorganization of bacterial

biofilms must be achieved prior to any antibiotic therapy

in order to disrupt the biofilm configuration forming a

barrier to antibiotic molecules. For periodontal treatment

we suggest a full mouth disinfection (FMD) approach, as

described in the periodontal literature [9]. The FMD con-

sists of a total scaling/mechanical debridement of teeth

root surfaces. An antiseptic irrigation of the pockets, the

dorsum of the tongue and the tonsils is also performed

[8]. The whole procedure should be finalized in one ses-

sion (or two sessions within 24 h). Immediately after

FMD, an antibiotic regimen (+ antiseptic chlorhexidine

mouth-washes/oral gels) has been found to significantly

enhance periodontal outcome [10]. A combination of

amoxicillin/metronidazole is the most tested combina-

tion after FMD [11]. On the other hand, clarithromycin

has shown an excellent availability in the gingival area

[35]. Hence, the antibiotic regimen in TT could substitute

periodontal prescription as soon as the mechanical treat-

ment is accomplished. This approach could enhance PP

and HP elimination (in the OC and the gastric tract). In

fact, the antibiotics used to eradicate HP are also effi-

cient against the anaerobic PB. Hence, the merging of the

periodontal FMD protocol and the TT (Figure 2) permits

to treat both pathologies in an optimal manner, and could

significantly boost oral HP eradication.

For maintaining long-term results, routine dental/peri-

odontal supportive therapy and daily oral hygiene pro-

cedures should be performed without interruption [6].

5. CONCLUSION

Although contradictory results are found in the scientific



Oral h

iene instructions

 Tooth brushing, interdental plaque removal, tongue scrapping

Full mouth disinfection(1 or 2 sessions

erformed in 24 h)

 Mechanical scaling/root planning (or ultrasonic debridement)

 Subgingival chlorhexidine irrigation

 Tongue disinfection with chlorhexidine gel

Tri

le the ra

+2 weeks chlorhexidine mouthwashes

 Starting immediately following the last session of full mouth

disinfection

Periodontal full mouth disinfection is immediately followed by triple

therapy regimen and antiseptic regimen, in order to enhance the eradi-

cation of periodontopathogenic bacteria as well as oral/gastric H. Py-

lori.

Figure 2. Multidisciplinary clinical protocol.

S. Marbaix et al. / Open Journal of Stomatology 3 (2013) 318-322 321

literature, many reports have associated periodontal dis-

ease (periodontal pockets formation) to an increased

prevalence of oral HP. Its bacterial load is increased by

periodontal disease and periodontal pockets formation.

The assumption that subgingival oral biofilm could act as

a suitable reservoir for HP is plausible and supported by

consistent evidence from preliminary clinical trials. The

presence of oral HP in patients with periodontal disease

(Periodontitis and gingivitis) may cause refractoriness of

gastric infection to triple therapy alone [5,31].

The mechanisms that confer the ability of HP to es-

cape systemic treatment are not well understood, but

there is evidence indicating that biofilms provide de-

fense from the host immunological response and the ac-

tion of antimicrobials agents [36]. Hence, antimicrobials

cannot be efficient if the biofilm is not mechanically

disrupted [37] shortly prior to prescription. The subgin-

gival dental biofilm is particularly suspected, due to the

favorable micro-ecological conditions provided by the

periodontal pockets. The biofilm is known to provide

protection from the host’s immunological response, and

bacteria growing in biofilms exhibit high resistance to

antimicrobial agents [5]. We therefore suggest a simple

multidisciplinary clinical management protocol, merging

the triple therapy to periodontal mechanical treatment

and chemical antiseptic disinfection. A joint coordination

between the periodontist and the gastroenterologist is a

perquisite for the success of this treatment regimen.

Adopting this protocol has two objectives; treating pe-

riodontal disease and enhancing the efficacy of the anti

HP therapy.

On the other hand, it should be considered that the ef-

ficacy of non-surgical treatment modalities is related to

the pocket depth. Hence, surgical periodontal procedures

like open flap debridement could be needed in some

cases to eliminate deep bacterial biofilms potentially har-

boring HP [33]. To our knowledge, no research has been

conducted in this field.

In conclusion, the efficacy of the combined proposed

protocol should be investigated in future controlled, ran-

domized clinical trials. If confirmed, it could be inte-

grated in the standard clinical management of HP infec-

tions.

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