Is There a Relation Betw RA and Perio

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J Clin Periodontol 2000; 27: 267272 Copyright C Munksgaard 2000

Printed in Denmark . All rights reserved

ISSN 0303-6979

F. Mercado1, Roderick I. Marshall1,

Alexander C. Klestov2 and

Is there a relationship betweenP. Mark Bartold11Department of Dentistry, University ofQueensland, 2Rheumatology Department,rheumatoid arthritis andRoyal Brisbane Hospital, Australia

periodontal disease?

Mercado F, Marshall RI, Klestov AC, Bartold PM: Is there a relationship between

rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000; 27: 267272.

C Munksgaard, 2000.

Abstract

Aim: The aim of this study was to determine whether there is a relationshipbetween disease experience of rheumatoid arthritis and periodontal disease.Methods: 1412 individuals attending the University of Queenslands School ofDentistry were assessed for the prevalence of periodontal disease and rheuma-toid arthritis. Analysis of data obtained from a self-reported health questionnaireand dental records was carried out and included: number of individuals referredfor advanced periodontal care (test group); number of individuals attending forroutine dentistry; determination of rheumatoid arthritis, cardiovascular diseaseand diabetes mellitus through self-reporting and assessment of prescription medi-cations; assessment of periodontal disease through assessment of existing oralradiographs.Results: In patients referred for periodontal treatment, the prevalence of self-reported rheumatoid arthritis was 3.95% which is significantly higher than thatseen in patients not referred for periodontal treatment (0.66%) and also that

reported in the general population (1%). Of those referred patients with rheu-matoid arthritis, 62.5% had advanced forms of periodontal disease. These resultswere mirrored in the results of the self-reported prevalence of cardiovascular diseaseand diabetes mellitus which was consistent with the published higher prevalencein periodontal patients.

Key words: periodontal disease; rheumatoidConclusions: Based on data derived from self-reported health conditions, and notarthritis; inflammation; self-reported health

withstanding the limitations of such a study, we conclude that there is good evi-questionnaire

dence to suggest that individuals with moderate to severe periodontal disease areat higher risk of suffering from rheumatoid arthritis and vice versa. Accepted for publication 14 June 1999

Periodontal disease is an all-en-compassing term relating to the de-structive inflammatory disorders of thehard and soft tissues surrounding teeth.All forms of inflammatory periodontaldisease are associated with a constel-lation of bacteria, predominantlyGram-negative anaerobic or facultativespecies present on tooth root surfacesas a biofilm. Long-term plaque ac-cumulation induces chronic inflam-mation of the periodontal tissues,which may lead to destruction of theattachment of the periodontal ligament

and the adjacent bone (Page et al.1977). By this stage, simple removal ofthe irritants is no longer sufficient topermit unconditional and complete re-generation of the damaged tissues. Ulti-mately, if untreated, the affected teethbecome loose and may be lost if the dis-ease continues to be active.

Recent studies have shown that peri-odontal disease may be related to anumber of systemic diseases includingan increased incidence of atheroscler-osis, coronary heart disease, myocardialinfarction and stroke (De Stefano 1993,

offenbacher 1996, Beck et al. 1996,Haraszthy et al. 1998). Periodontal dis-ease is also known to be a major com-plication of diabetes (Yalda et al. 1994)and management of periodontal diseaseresults in better controlled diabetes(Miller et al. 1992).

In addition to the above well docu-mented examples, a number of otherchronic conditions of altered connectivetissue metabolism, hormone imbalanceand altered immune function have like-wise been associated with increased riskof periodontal disease (Bartold 1991).


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268 Mercado et al.

Of these, rheumatoid arthritis is of par-ticular interest since it is a chronic in-flammatory disease which demonstratesremarkably similar patterns of soft andhard tissue destruction to those noted inchronic periodontitis (Snyderman et al.1982). Although the aetiologies of these

diseases are distinctly separate, theunderlying pathological processes are ofsufficient similarity to warrant consider-ation of the hypothesis that individualsat risk of developing rheumatoid ar-thritis may also be at risk of developingperiodontitis, or vice versa. Indeed,should an individual have a particularsystemic predisposition towards alteredimmune function or altered connectivetissue metabolism (for example, geneticpolymorphisms leading to altered neu-trophil function, specific HLA pheno-types consistent with poor immune de-

fence, or altered expression of cytokinessuch as IL-1), then the potential for sus-ceptibility to multiple diseases related tosuch functions is possible.

Therefore, the primary aim of thispreliminary study was to test the hypo-thesis that individuals with periodontaldisease would have a higher prevalenceof rheumatoid arthritis than those indi-viduals without periodontal disease.The secondary aim was to test thehypothesis that those individuals withrheumatoid arthritis would have ahigher prevalence of advanced forms of

periodontal destruction, than patientswith periodontal disease but withoutrheumatoid arthritis. We chose to carryout this initial study on the basis ofdata collated from self-reported healthquestionnaires recognising the limi-tation of such data but needing prelimi-nary data to indicate whether a largerand more detailed study to investigatethis issue is warranted.

Methodology

Prior to commencement of this study

approval had been obtained from theHuman Ethics Committee of the Uni-versity of Queensland. A total of 1412subjects ages 2070 were included in thestudy (see Table 1 for subject distri-

Table 1. Distribution and ages of cohort

studied

Periodontitis Control

group group

no. subjects: 809 603

mean age (year s) 44.32 42.28

bution). The subjects were all patientsattending the University of QueenslandDental School for dental treatment.Within the study, two groups were iden-tified. The periodontitis group (PG)were derived from studying the recordsof 809 consecutive individuals referred

for periodontal treatment. The remain-der, were the general group (GG) andconsisted of 603 consecutive individualsattending a clinic for general dentaltreatment (other than referred peri-odontal treatment).

The prevalence and severity of peri-odontitis was ascertained from thedocumentation in each subjects dentalrecords and assessment of past dentalradiographs using the modified Hugo-son and Jordan (1982) classification(Table 2).

To determine the prevalence of rheu-

matoid arthritis, the patients dentalrecords were obtained and the latestmedical-dental questionnaires wereevaluated. To be identified as sufferingfrom rheumatoid arthritis, the patientsmust not only have self reported thepresence of such a condition but alsohave had the prescription of a medi-cation consistent with such a conditiondocumented (medication included vari-ous NSAIDs, methotrexate, etc.). As-sessments of the records for the pres-ence of cardiovascular disease and dia-betes mellitus were also noted in the PG

group since these two systemic con-ditions have been well documented fortheir association with periodontitis andthus would provide a measure of valid-ity to the rheumatoid arthritis data. Foran individual to be included in thesegroups not only must they have self-re-ported the presence of such a conditionbut they must also have, in their rec-ords, documentation of the prescriptionof a medication consistent with the

Table 2. Modified Hugoson and Jordan classification for periodontal disease

Perio 0 no discernible radiographic evidence of bone loss

Perio 1 (mild) proximal bone loss reaching at most 1/3 of normal bone height

Perio 2 (moderate) proximal bone loss between 1/3 and 2/3 of normal bone height

Perio 3 (severe) proximal bone loss more than 2/3 of normal bone height

Table 3. Distribution of rheumatoid arthritis in a periodontitis population

Rheumatoid arthritis No rheumatoid arthritis Totals

P2-P3 20 (2.4%) 340 (42.0%) 360 (44.5%)

P0-PI 12 (1.5%) 437 (54.1%) 449 (55.5%)

Totals 32 (4.0%) 777 (96%) 809 (100%)

presence of cardiovascular disease ordiabetes mellitus.

Following collection of the data, t-test analyses were used to determinedifferences in the prevalence of peri-odontitis and rheumatoid arthritis, inthe cohorts studied using the same test,

the difference in the prevalence of mod-erate to severe periodontitis in individ-uals with rheumatoid arthritis was alsoevaluated against those without rheu-matoid arthritis.

Results

The prevalence of rheumatoid arthritisin the periodontitis group (PG) was3.95% which was significantly greaterthan that found in the general group(GP) 0.66% (p0.05) The overall preva-lence of rheumatoid arthritis, is shown

in Fig. 1. Among the 36 subjects whoreported to have rheumatoid arthritisand were taking the prescribed medi-cations, 33 (92%) had radiographic evi-dence of moderate to severe alveolarbone loss (P1, P2 or P3).

The prevalence of moderate to severeperiodontitis (P2-P3) in the peri-odontitis group (PG) (44.5%) was, asexpected, much greater than in the gen-eral group (0.1%). Within the PGgroup, as shown in Fig. 2 and Table 3,20 out of 32 (62.5%) of the patientswith rheumatoid arthritis suffered from

advanced forms of periodontal destruc-tion (P2 or P3). Only of those withoutrheumatoid arthritis, 340 out of 777(43.8%) suffered from more advancedforms of periodontal disease. Thus, pa-tients with rheumatoid arthritis weremore likely (p0.05) to have moderateto severe bone loss (P2 or P3) thanmilder forms of disease (P0 or P1).

To test the validity of using self-re-ported information, we also determined


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Rheumatoid arthritis and periodontal disease 269

Fig. 1. Prevalence of disease in various populations. The prevalence of rheumatoid arthritis

(RA) cardiovascular disease (CVD) and diabetes mellitus (DM) was monitored in the peri-

odontitis group (PG) and general group (GG). Data from previously published studies are

included for comparison.

Fig. 2. Prevalence of periodontal disease in individuals with rheumatoid arthritis (RA) cardio-

vascular disease (CVD) and diabetes mellitus (DM). The prevalence for zero to mild (P0-P1)

and moderate to severe periodontitis (P2-P3) is shown. The scoring system (P0-P3 is as de-

scribed in Table 2).

the prevalence of self-reported cardio-vascular disease (CVD) (14.2%) anddiabetes mellitus (DM) (6.1%) withinthe periodontal group. While thesevalues are somewhat higher than thosereported for the general population(Nathan 1993, Saskatchewan HeartHealth Program 1997), they are consist-ent with the reported prevalence ofthese conditions within a periodontalpopulation and is consistent with these

patients tending to have more systemicdiseases generally (Rees and Brasher1974, Peacock & Carson 1995).

Discussion

It is generally accepted that the preva-lence of advanced periodontitis in hu-man populations ranges between 515%(American Academy of Periodontology,1996). In the present study we report

that the prevalence of moderate to se-vere periodontitis is significantly elev-ated in individuals suffering from rheu-matoid arthritis (unadjusted relativerisk 4.7). In addition, the converse alsoholds true in that individuals referredfor periodontal treatment also appear

to have a higher prevalence of rheuma-toid arthritis compared to the generalpopulation (unadjusted relative risk1.5).

These findings are based on theanalyses of data obtained from self-re-ported health questionnaires and evalu-ation of oral radiographs. Althoughgathering information from healthquestionnaires results in data that areless reliable than those obtainedthrough laboratory/clinical examina-tions, this method is cost-effective andreliable enough to be used in epidemio-

logical and clinical studies (Ho et al.1997, Nery et al. 1987, Suomi et al.1975). Indeed a recent study has shownthat there are high levels of agreementbetween self-reported health conditionsand actual presence of the condition (kranged from 0.710.90) (Ho et al. 1997).Thus, such an approach is valid for apilot study before moving to more elab-orate and larger scale studies.

In an effort to test the validity of ourfindings we monitored the self-reportedprevalence of cardiovascular diseaseand diabetes mellitus. The prevalence of

both cardiovascular disease (CVD)(14.2%) and diabetes mellitus (DM)(6.1%) within the PG group, while con-sistent with other studies (11.623.5%for CVD and 4% for DM) (Rees &Brasher 1974, Brasher & Rees 1970,Peacock & Carson 1995), these valuesare far greater than the currently ac-cepted general population figures of 6%for cardiovascular disease (Saskat-chewan Heart Health Survey, 1997) and2.4% for diabetes mellitus (Nathan1993, National Diabetes Data Group,1985). As these published figures com-

pare favourably with the findings in thisstudy they offer a measure of validity tothis methodology (self-reporting) andtherefore to the self-reported rheuma-toid arthritis experience data collectedin this study.

The findings that 58% of the patientswho reported to have DM and 64.6%of patients with self-reported cardio-vascular disease had significant levels ofperiodontal bone loss (P2 or P3) werenot surprising since numerous studieshave shown that diabetes increases therisk of severe periodontitis and peri-


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270 Mercado et al.

Fig. 3. Possible interrelationships between rheumatoid arthritis and periodontal disease.

odontal disease progression approxi-mately 23 fold (Gross & Genco 1998)and that periodontal disease may be arisk factor for cardiovascular disease(Beck et al. 1996).

The observation that 3.9% of pa-tients in the study referred for manage-ment of periodontal disease had self-re-ported rheumatoid arthritis is particu-larly noteworthy. This is a very highprevalence compared to the 1% preva-lence reported in the normal population

(Arnett 1988). The additional findingthat 62.5% of the rheumatoid arthritispatients suffered from more advancedforms of periodontal destruction (P2 orP3) supports the hypothesis that notonly is there a higher prevalence ofrheumatoid arthritis amongst individ-uals referred for periodontal treatmentbut that those individuals with rheuma-toid arthritis have a greater prevalenceof advanced forms of periodontal dis-ease. The increased prevalence of rheu-matoid arthritis in the periodontitisgroup in this study suggests a possible

link between the manifestation of thesetwo chronic inflammatory diseases.

To date, only a few studies haveexamined the extent of the associationbetween RA and periodontal diseaseand, amongst these studies, the resultshave been conflicting (Helminen-Pak-kala 1971, Blair & Chalmers 1976,Kasser et al. 1997, Tolo et al. 1990). Thelack of uniformity in classifying thevarious forms of periodontal diseaseand rheumatoid arthritis in these

studies has made it difficult to comparethe above studies. In the present studywe have recognised that periodontitishas a variable expression with regardsto its severity. Therefore, by trying tocorrelate the experience of rheumatoidarthritis with moderately to advancedperiodontitis we believe we are gettingcloser to determining whether underly-ing systemic components may impacton the manifestation of these two dis-eases. If all forms of periodontal dis-ease (from very mild gingivitis to ad-vanced periodontitis) were to be in-

cluded (as has been the case in moststudies) then the likely correlation be-comes weaker due to a dilution of thepatient cohort with significant disease.

Since we have identified a possible re-lationship between rheumatoid arthritisand moderate to severe periodontitis we

propose that, in a proportion of thesepatients, a hitherto unidentified disable-ment or dysregulation of commonpathologic mechanisms operate in thesetwo chronic inflammatory diseases. In-deed, there are remarkable similaritiesin the pathogenesis of these two con-ditions at both the cellular and molecu-lar level (Fig. 3). Both conditions relyupon an initial competent surveillanceby neutrophils which if either insuf-ficient or over exuberant leads to earlytissue damage, subsequent recruitmentof lymphocytes, immunemediate pro-

tection, together with degradation ofthe tissues, the release of myriad cyto-kines, lymphokines and prostanoidpathways all point to a common under-lying regulatory mechanisms in thesetwo conditions despite their differingaetiology (Kornman et al. 1997, Reyn-olds et al. 1997, Offenbacher et al.1993).

In conclusion, while all of the studieslinking periodontal disease to varioussystemic diseases need further investiga-tion, the available data are becomingcompelling to indicate a significant re-

lationship between periodontal diseasein systemic health. This study highlightsthe potential for a relationship between2 of the most common and debilitatingchronic inflammatory conditions affect-ing humans and warrants further de-tailed investigation.

Zusammenfassung

Gibt es einen Zusammenhang zwischen rheu-

matoider Arthritis und marginaler Parodonti-

tis?

Das Ziel dieser Studie war es, einen mogli-

chen Zusammenhang zwischen dem Vorkom-men rheumatoider Arthritis und marginaler

Parodontitis festzustellen. 1412 Personen, die

die Zahnklinik der Universitat von Queens-

land aufsuchten, wurden auf marginale Paro-

dontitis und rheumatoide Arthritis unter-

sucht. Es wurde eine Auswertung von Daten

vorgenommen, die aus einem Befragungsbo-

gen mit Angaben der Patienten zur Gesund-

heit und zahnarztlichen Befundunterlagen

entstammten. Diese Daten umfaten: Zahl

der Personen, die zur weiterfuhrenden

Parodontaltherapie uberwiesen waren (Test-

gruppe), Zahl der Personen, die sich zur

Routinebehandlung vorstellten; Angabe


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Rheumatoid arthritis and periodontal disease 271

rheumatoider Arthritis, kardiovaskularer Er-

krankungen und Diabetes mellitus durch die

Patienten selbst und Erfassung verschriebe-

ner Medikamente; Beurteilung marginaler

Parodontitis aufgrund existierender Ront-

genbilder. Bei Patienten, die zur Parodontiti-

stherapie uberwiesen waren, lag die Prava-

lenz selbstgenannter rheumatoider Arthritis

bei 3.95%, was statistisch signifikant hoherlag als die Pravalenz bei den Patienten, die

nicht uberwiesen waren (0.66%) bzw. die Pra-

valenz die sich aus den Angaben einer durch-

schnittlichen Population ergab (1%). Von den

Patienten mit rheumatoider Arthritis litten

62.5% an fortgeschrittenen Formen der mar-

ginalen Parodontitis. Diese Ergebnisse spie-

gelten sich in den Angaben zur Pravalenz

kardiovaskularer Erkrankungen und Diabe-

tes mellitus wider, die bei Patienten mit mar-

ginaler Parodontitis hoher lag. Basierend auf

den Daten aus den Patientenangaben zur Ge-

sundheit kann die Schlufolgerung gezogen

werden, da Patienten mit moderater bis

fortgeschrittener Parodontitis ein erhohtes

Risiko haben, an rheumatoider Arthritis zuleiden und umgekehrt.

Resume

Existe-t-il une relation entre la polyarthrite

rhumatoide et la maladie parodontale?

Cette etude avait pour but de determiner

sil existe une relation entre latteinte de

polyarthrite rhumatode et de maladie pa-

rodontale. Chez 1412 sujets frequentant

lEcole Dentaire de lUniversite de Queens-

land, les prevalences de la maladie

parodontale et de la polyarthrite rhumato-

de ont ete determinees. Une analyse desdonnees obtenues en se basant sur un

questionnaire de sante rempli par les sujets

eux-memes, et a partir des fiches dentaires,

a ete pratiquee et comprenait: le nombre

de sujets adresses pour soins parodontaux

avances (groupe test), le nombre de sujets

sadressant pour des soins dentaires

ordinaires; enregistrement de la polyarthri-

te rhumatode, des maladies cardiovasculai-

res, et du diabete sucre, a partir des rensei-

gnements donnes par les sujets eux-memes,

et enregistrement des medicaments

prescrits; enregistrement de la maladie pa-

rodontale a partir des radiographies bucca-

les existant. Chez les patients adresses pour

traitement parodontal, la prevalence de lapolyarthrite rhumatode ressortant des in-

dications des patients etait de 3.95%, ce

qui est significativement plus eleve que ce

quon constatait chez les patients qui

netaient pas adresses pour traitement pa-

rodontal (0.66%), et plus eleve aussi que ce

qui ressortait des indications de la popula-

tion en general (1%). Parmi les patients

adresses et souffrant de polyarthrite

rhumatode, 62.5% presentaient des formes

avancees de maladie parodontale. Ces

resultats etaient le reflet des resultats de la

prevalence dont il etait rendu compte pour

les maladies cardiovasculaires et le diabete

sucre, en concordance avec lelevation de la

prevalence chez les patients parodontaux.

En se basant sur les donnees provenant des

informations fournies par les patients sur

leur sante, et en depit des limitations de ce

genre detude, on peut conclure quil existe

des preuves indiquant que les sujets

atteints de maladie parodontale moderee a

severe ont une risque plus eleve de souffrirde polyarthrite rhumatode et inversement.

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Address:

P. M. Bartold

Department of Dentistry

University of Queensland

Brisbane QLD 4000

Australia

Fax: (07) 3365 8135

e-mail: p.bartold/mailbox.uq.edu.au

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