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J Clin Periodontol 2008; 35 (Suppl. 8): 333–337 doi: 10.1111/j.1600-051X.2008.01278.

Periodontal diseases and health: Denis Kinane1 and Phillippe


Bouchard2 on behalf of group E of
the European Workshop on

Consensus Report of the Periodontologyn


1
Center for Oral Health and Systematic
Diseases, School of Dentistry, University of

Sixth European Workshop on Louisville, Louisville, KY, 40202, USA;


2
Department of Periodontology, Service of
Odontology, Hôtel-Diev Hospital, AP-HP,
Paris 7-Denis Diderot University, U.F.R. of

Periodontology Odontology, Paris, France

Kinane D, Bouchard P. Periodontal diseases and health: Consensus Report of the


Sixth European Workshop on Periodontology. J Clin Periodontol 2008; 35 (Suppl. 8):
333–337. doi: 10.1111/j.1600-051X.2008.01278.x.

Abstract
Introduction: The remit of this group was to update the knowledge base on
periodontal diseases and health.
Material and Methods: The literature was systematically searched and critically
reviewed in five specific topics.
Results: Prevalence of periodontitis: The data suggest a trend towards a lower
prevalence of periodontitis in recent years.
Adverse pregnancy outcome: The findings indicate a likely association between
periodontal disease and an increased risk of adverse pregnancy outcomes. There is no
evidence that treating periodontal disease decreases the rate of adverse pregnancy outcomes.
Prevalence and distribution of periodontal pathogens: Genetic analysis of bacteria
has demonstrated an unanticipated diversity within species. Carriage rates and
particular subsets of these species vary between ethnic groups. Few of these
differences can be related to differences in disease prevalence.
Diabetes mellitus: Evidence on the association supports the concept of increased
severity but not extent of periodontitis in subjects with poorly controlled diabetes. It is
inconclusive that periodontal treatment results in improved metabolic control.
Cardiovascular diseases: Evidence suggests that having periodontitis contributes to
Key words: cardiovascular; diabetes mellitus;
the total infectious and inflammation burden and may contribute to cardiovascular periodontitis; preterm birth; prevalence
events and stroke in susceptible subjects. The impact of periodontal therapy must be
further investigated. Accepted for publication 20 May 2008

Conflict of interest and source of


funding statement
Group E participants declare that they had
no conflict of interests.
The 6th European Workshop has been finan-
cially supported by an unrestricted education-
al grant from Straumann AG. The sponsor
had no impact on the program or on the
deliberations of the European Workshop.

n
D’Aiuto Francesco, UK; Hugoson Anders, Swe-
den; Kilian Mogens, Denmark; Kocher Thomas,
Germany; Loos Bruno, The Netherlands; Madia-
nos Phaebus, Greece; Norderyd Ola, Sweden;
Papapanou Panos, USA; Persson Rutger, Switzer-
land; Pihlström Bruce, USA; Rylev Mette, Den-
mark; Salvi Giovanni, Switzerland; Shapira Lior,
Israel; Wimmer Gernot, Germany.
r 2008 The Authors 333
Journal compilation r 2008 Blackwell Munksgaard
334 Kinane & Bouchard

The remit of this working group was to cally plausible pathways by which these diagnostic methodology in periodontal
update the existing knowledge base on effects may be mediated. These studies disease. This review identifies the very
the impact of periodontal disease on may span a broad spectrum of approaches limited number of studies that provide
health. Several published systematic including in vitro studies, in vivo prevalence data over time, and this data is
reviews from the 4th EAP Workshop mechanistic experimental animal studies, discussed in comparison with those stem-
formed the starting point for this update, human observational, prospective cohort ming from a few corresponding studies
and in addition, specific innovations not studies and intervention trials focusing on from countries outside Europe. The data
covered in previous workshops were specific biomarkers. Ultimately, rando- indicate a possible trend of a lower pre-
included. For this purpose, the literature mized controlled clinical trials (RCTs) valence of periodontitis in recent years.
was systematically searched and criti- examine the effect of specific interven-
cally reviewed. tions (with respect to time point, mode of
Consensus statements
Five manuscripts were produced on administration, intensity, etc.) on particu-
specific topics identified as areas where lar clinical outcomes or on validated and Limited data from selected populations in
advances in knowledge had been made widely accepted surrogate markers. Europe and the US points to a decrease in
in periodontal and general health and Clinical trials with a statistically sig- the prevalence of periodontal diseases.
which were deemed to be potentially nificant positive outcome are easy to These decreases are primarily in gingivi-
important in the future clinical practice. interpret and indicate that the tested tis and mild/moderate periodontitis. The
intervention is effective in favourably single study that allows a comparison
- Has the prevalence of advanced altering the adverse health outcome. If over time of the most severe forms of
periodontitis changed in Europe independently corroborated by addi- periodontitis demonstrates no change in
during the last 30 years? tional clinical trials, their findings are prevalence. However, this observation is
- A critical assessment of adverse interpreted as the ultimate proof that the confounded primarily by tooth loss and a
pregnancy outcome and perio exposure was causative of the condition. definitive statement on changes in pre-
dontal disease. However, clinical trials with non- valence of severe periodontitis over time
- Prevalence and distribution of significant outcomes are far more diffi- is not possible.
major periodontal pathogens cult to interpret. In situations where
worldwide. there are wide confidence intervals, the
Implications for practice
- Effects of diabetes mellitus on direction of the effect cannot be deter-
periodontal and peri-implant con mined with adequate precision, thus the Precise estimates of prevalence trends
ditions. Update on associations findings are inconclusive. over time are essential for the determina-
and risks. Repeated, independently carried out, tion of treatment needs, the identification
- Cardiovascular and periodontal negative clinical trials may ultimately of the determinants of change in preva-
disease. An update on the associa- point to the conclusion that the particular lence, and subsequent cost-effectiveness
tions and risks. adverse health outcome may not be analyses to appropriately allocate oral
positively modulated by means of the health care resources in order to achieve
Although the purpose was to produce specific intervention. Still, these studies maximal benefit for the population.
systematic reviews with meta-analyses do NOT provide proof that there is a lack
in all five manuscripts, the paucity and of a causal relationship between the
heterogeneity of the available clinical exposure and the outcome. Interventions Implications for research
research in some specific areas pre- may fail to have an effect on the outcome There is a need for additional studies
cluded this approach and favoured a under investigation due to a variety of using well-defined criteria that reflect
more narrative approach. reasons such as inappropriate timing, extent and severity across the entire range
Themes common to all of the inability to alter the exposure to a suffi- of periodontal conditions, so that the
reviewed topics emerged, which were cient extent and inadequate compliance. trends in prevalence can be defined with
deemed fundamentally important to the RCTs are ideally suited to assess the precision. Assessment of periodontal
accurate interpretation of study design, effectiveness of the intervention on a status should incorporate an evaluation
outcomes, interpretations and future disease outcome, change clinical prac- of dental status parallel to assessments
research. Among these we have identi- tice, and to inform public health policy. of inflammatory periodontal conditions
fied the following. They do not serve as a sole basis for as well as a documentation of possible
Causal inference is established incre- determining causality. changes in established risk factors.
mentally through a synthesis of data
stemming from different types of studies.
Epidemiologic studies (case–control, Has the Prevalence of Periodontitis A Critical Assessment of Adverse
cross-sectional and prospective cohort Changed During the Last 30 Years? Pregnancy Outcome and Periodontal
studies) are usually the first to generate (Hugosson & Norderyd 2008) Disease (Wimmer & Pihlstöm 2008)
association data between putative risk Conclusions Conclusions
factors (exposures) and adverse health
outcomes. Initially observed univariate This paper reviews global trends in the Despite wide efforts in the areas of
associations are subsequently examined change in prevalence of periodontitis prevention, diagnosis and therapy, the
in multivariate settings to adjust for over the last 30 years. The epidemiology incidence of preterm birth in most of the
potential confounders. Factors identified of periodontal disease is briefly reviewed countries has not reduced. Infections are
as independent exposures are examined together with the current classification considered to be one of the important
in additional studies to dissect biologi- system and the clinical and radiographic causes. Recently, oral infections have
r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
Periodontal diseases and health 335

attracted increasing interest. The objec- Existing evidence from a relatively dontal disease prevalence. Asian popu-
tive was to review the evidence for the small, single-centre RCT has shown no lations are regularly colonized with
association and risks between preterm advantage in use of adjunctive antimi- Aggregatibacter actinomycetemcomi-
low birth weight deliveries and crobial periodontal therapy to reduce tans serotype c with questionable patho-
periodontal diseases as well as the impact adverse pregnancy outcomes. genic potential. Conversely, the JP2
of periodontal therapy on pregnancy out- clone of A. actinomycetemcomitans has
comes. In order to identify studies for this enhanced virulence and causes signifi-
Implications for research
topic, a search in computerized databases cantly higher prevalence of aggressive
up to October 2007 was conducted. The Future observational and intervention periodontitis in adolescents whose des-
search was limited to clinical human studies should clearly define adverse cent can be traced back to the Mediter-
studies published in English. All levels pregnancy outcomes. For example, pre- ranean and western parts of Africa.
of available evidence were included. term birth and low birth weight should Some genetically distinct types of Por-
There was a clear heterogeneity between not be combined into one outcome phyromonas gingivalis are more asso-
the studies, concerning the definitions variable. ciated with disease than others, but
used for periodontal disease measure- Future observational and intervention additional work is required to relate
ment and for adverse pregnancy out- studies should clearly define periodontal this to clinical differences.
comes. In many papers, there was a disease exposure in terms of extent and Studies that take into account differ-
remarkable lack of adequate analysis severity of periodontal disease. ences linked to the genetics of both
for confounders, making it barely pos- Large sample prospective cohort stu- patients and potential pathogens are
sible to draw any solid conclusions. dies in various populations are needed in likely to give better insight into the
Although the findings indicate a likely order to determine whether and which aetiology of periodontal diseases.
association between periodontal disease type of periodontal diseases may have a
and an increased risk of adverse preg- causative role in adverse pregnancy out- Consensus statements
nancy outcomes, there is no conclusive come(s) and whether this role varies
evidence that treating periodontal dis- among different populations. Current evidence indicates that carriage
ease improves the rate of positive birth If large, prospective cohort studies rates of the periodontal pathogens
outcomes. It is recommended that establish a temporal relationship A. actinomycetemcomitans and P. gingi-
further studies including larger cohorts between maternal periodontal disease valis vary between ethnic groups.
and interventional trials, which clearly before or during pregnancy and adverse Some of these differences may be
define outcome and exposure measures pregnancy outcome(s), large sample, explained by differences in oral
and which adequately control for other multi-centre RCTs will be needed to hygiene, local patterns of antibiotic
confounders, be conducted. determine if appropriately timed and usage and other environmental factors.
delivered periodontal interventions Other differences seem to be related to
decrease adverse pregnancy outcome(s) host tropism resulting from long-term
Consensus statements in these populations. co-evolution rather than to differences
in geography and limited dissemination.
In certain study samples, periodontal dis-
Few of these differences can, with the
ease has been associated with adverse
Prevalence and Distribution of current information, be directly related
pregnancy outcome(s); this association
Principal Periodontal Pathogens to differences in periodontal disease
has not been shown in other populations.
Worldwide (Rylev & Kilian 2008) prevalence. The only well-documented
There is considerable heterogeneity and
exception is the JP2 clone of A. actino-
inconsistency in periodontal disease expo- Conclusions
mycetemcomitans, which has distinctly
sure definitions among studies of perio-
Detailed genetic analysis of bacteria has enhanced virulence and causes a signif-
dontal disease and adverse pregnancy
demonstrated an unanticipated genetic icantly higher prevalence of aggressive
outcome(s). There is considerable hetero-
diversity within species, which often periodontitis in adolescents whose
geneity in adverse pregnancy outcomes
reveals evolutionary lineages that are descent can be traced back to the Med-
reported in studies of periodontal disease
disproportionately associated with iterranean and western parts of Africa.
and adverse pregnancy outcome(s), for
infection. There is evidence that some Comprehensive genetic studies of
example: preterm birth, low birth weight,
evolutionary lineages of bacteria have bacteria associated with humans reveal
preterm birth and/or low birth weight,
adapted to particular ethnic groups. This striking differences in the pathogenic
foetal growth restriction, stillbirth, pre-
review analyses to what extent the potential of members of the same spe-
eclampsia, and late miscarriage.
observed differences in periodontal dis- cies. Recent information indicates that
There is no consistent evidence that
ease prevalence among ethnically or this applies to A. actinomycetemcomi-
treatment of periodontal disease
geographically distinct populations tans. There is strong evidence from
improves pregnancy outcome(s) across
may be explained by restricted host longitudinal cohort studies that the
populations.
adaptation of clones of principal perio- highly toxic JP2 clone of A. actinomy-
dontal pathogens. Carriage rates of sev- cetemcomitans has unique pathogenic
Implications for practice
eral putative periodontal pathogens and potential and is associated with initia-
particular subsets of these species vary tion of aggressive periodontal disease.
There is evidence that mechanical perio- between ethnic groups. Only individuals whose descent can be
dontal therapy administered in the sec- Few of these differences can, with the traced back to the Mediterranean and
ond trimester is safe and does not have limited information available, be western parts of Africa are susceptible
any adverse maternal or infant effects. directly related to differences in perio- to infection with the JP2 clone, a fact
r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
336 Kinane & Bouchard

that conceivably explains the observed Available evidence on the association Implications for practice
high prevalence of aggressive perio- between diabetes and periodontitis sup-
dontitis in African Americans, Arabs, ports the concept of increased severity The clinician should be aware of the
Berbers and individuals of Northwest but not extent of periodontitis in subjects bidirectional relationship between dia-
African descent, e.g. in Brazil. with poorly controlled diabetes. Subjects betes and periodontal disease and its
Conversely, the high prevalence of with controlled diabetes do not show an clinical ramifications for diagnosis and
A. actinomycetemcomitans serotype c in increase in the extent and severity of treatment.
Asian populations without pronounced periodontitis. Studies have demonstrated There is evidence that opportunistic
periodontitis suggests that at least in this that periodontitis is associated with poor screening for type II diabetes is effective
population some members of this sero- metabolic control and diabetes-related in the dental office, and thus oral care
type are non-pathogenic. More detailed complications. It is inconclusive that providers may play a role in the detec-
microbiological and prospective cohort periodontal treatment results in improve- tion of undiagnosed diabetes.
studies are required to associate parti- ments of metabolic control and of mar-
cular subsets of other bacteria with kers of systemic inflammation. No Implications for research
disease, health or particular ethnic evidence is available that improvement
groups. of metabolic control in diabetic subjects The effects of different modalities of
results in improved periodontal condi- periodontal therapy on glycaemic con-
tions in diabetic subjects with perio- trol need to be addressed in appropri-
Implications for practice ately powered and designed intervention
dontitis. Poorly controlled diabetes may
Knowledge of this phenomenon may be considered a risk factor for increased studies.
impact on the diagnosis and treatment severity of periodontal disease. The Additional studies should address the
of particular ethnic groups. effects of periodontal therapy on dia- association of periodontitis with the meta-
betic control and systemic inflammation bolic syndrome (a precursor of type II
are not proven beyond doubt and need to diabetes) and with gestational diabetes.
Implications for research The effects of diabetes on implant
be confirmed in large-scale RCTs.
As yet, we have no knowledge of the therapy and regenerative therapy should
host determinants of this bacterial trop- be addressed in appropriately powered
ism. Intervention studies are needed to and designed intervention studies.
further assess the clinical effects of Consensus statements
lowering the level or eliminating the
JP2 clone through treatment. Although Diabetes and periodontitis represent Cardiovascular and Periodontitis.
the JP2 clone confers high risk for common chronic diseases that may Update on the Associations and Risk
aggressive periodontitis, some non-JP2 have reciprocal influence. Interpretation (Persson & Persson 2008)
clones also confer risk and their con- of the available literature is hampered Conclusions
tribution should be elucidated. In future, by changing definitions of glycaemic
we should test for various clones and control and the prevalence and manage- Associations between periodontitis and
determine strategies for preventing ment of both diseases. cardiovascular diseases (CVDs) have
aggressive periodontitis, e.g., eradica- In terms of diabetes influencing been recognized. A literature review
tion or other means. periodontitis, available evidence on the since the previous European Workshop
association between diabetes and perio- on Periodontology has been conducted.
dontitis supports the concept of The lack of reliable epidemiological
Effects of Diabetes Mellitus on increased severity of periodontitis in data on disease prevalence makes it
Periodontal and Peri-Implant subjects with diabetes. Periodontal dis- difficult to assess the associations and
Conditions. Update on Associations ease in diabetes subjects is associated risks between periodontitis and CVD.
and Risks (Salvi et al. 2008) with age of onset, duration of diabetes, Data based on meta-analysis have sug-
Conclusions
poor metabolic control and diabetes- gested odds ratios between 1.1 and 2.2.
related complications. Subjects with The impact of periodontitis on serum
Diabetes mellitus and periodontal disease controlled diabetes show periodontal markers of inflammation such as CRP,
represent common chronic diseases that conditions comparable to those of the interleukin-6, plasminogen factors,
may have reciprocal influence. The objec- general population. Non-surgical and white blood cell counts, and on serum
tive was to review the evidence for the surgical periodontal therapies are lipids, brachial artery flow rate, intima
association between diabetes and perio- equally efficacious in diabetes subjects media thickness suggest that having
dontal disease and the impact of perio- with good glycaemic control compared periodontitis has a negative impact on
dontal therapy on diabetic status. A search with non-diabetes subjects. such CVD surrogates. There is evidence
of MEDLINE-PubMed was performed up In terms of periodontitis influencing that within 6 months following perio-
to and including December 2007. The diabetes, subjects with type I and type II dontal therapy, brachial artery flow rates
search was limited to clinical studies diabetes (Pima Indians) with severe improve. Following intensive perio-
published in English. Publications on ani- periodontitis have more diabetic com- dontal therapy, however, serum high-
mal studies were excluded. The selection plications than diabetes subjects with no sensitivity CRP values increase,
criteria included all levels of available periodontitis. It is inconclusive whether whereas brachial artery flow rate may
evidence: systematic reviews, RCTs, con- periodontal treatment results in temporarily decrease, suggesting that
trolled clinical trials, prospective and ret- improvements in metabolic control and medical consults before periodontal
rospective cohort studies and case reports. markers of systemic inflammation. treatment of subjects at high risk for
r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
Periodontal diseases and health 337

acute coronary syndrome or stroke lar events. Data suggest that periodontitis cal mechanisms whereby periodontal
should be performed. Tooth eradication elicits low-grade systemic inflammation. disease can mediate the risk for athero-
may also reduce the systemic inflamma- There is modest evidence to suggest that sclerosis and CVD events.
tory burden. Preventive periodontal care periodontal therapy lowers levels of ser- We need properly designed studies
may be the most important effort in um CRP; however, this finding is not assessing the immediate and long-term
reducing the risk for CVD by maintain- consistent across other biomarkers. impact of periodontal therapy on cardi-
ing healthy oral conditions. There is evidence that periodontal ovascular events or validated surrogate
Available evidence suggests that hav- therapy improves measures of endothe- markers of cardiovascular events. Well-
ing periodontitis contributes to the total lial function (endothelial dysfunction is designed prospective cohort studies may
infectious and inflammation burden and a very early marker of vascular disease). inform the design of large multicentred
may contribute to cardiovascular events There are still no published trials asses- RCTs to investigate the possible effect
and stroke in susceptible subjects. sing the impact of periodontal therapy on of periodontal therapy on CVD. The use
The impact of periodontal therapy the incidence of cardiovascular events. of validated surrogate markers for CVD
must be further investigated. would enhance the efficiency and cost-
Implications for practice
effectiveness of such RCTs.
Consensus statements
The clinician should be aware of the
Since the last similar systematic review potential relationship between CVD and
References
(4th EWP), a consistent positive but periodontal disease and its clinical rami-
weak association has been reported fications in periodontal management. Hugosson, A. & Norderyd, O. (2008) Has the
between periodontitis and increased prevalence of periodontitis changed during
future risk of cardiovascular events the last 30 years? Journal of Clinical Perio-
Implications for research dontology 35 (Suppl. 8), 338–345.
(MI, stroke). One meta-analysis reported
an odds ratio between 1.14 (CI 1.01– As suggested in the last EWP, prospec- Persson, R. & Persson, R. (2008) Cardiovascu-
lar and periodontitis: An update on the asso-
1.2) in prospective studies and 2.2 (CI tive multicentre cohort studies in differ-
ciations and risk. Journal of Clinical
1.6–3.1) in case controls and the second ent countries should be performed to Periodontology 35 (Suppl. 8), 362–379.
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tion of periodontitis in epidemiologic an exposure both with clinical, micro- of diabetes mellitus on periodontal and
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measures of sub-clinical carotid athero- and effect modifiers in the association assessment of adverse pregnancy outcome
sclerosis (intima media thickness: IMT), between these two diseases. In addition, and periodontal disease. Journal of Clinical
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r 2008 The Authors


Journal compilation r 2008 Blackwell Munksgaard

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