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Periodontology 2000, Vol.

53, 2010, 28–44  2010 John Wiley & Sons A/S


Printed in Singapore. All rights reserved PERIODONTOLOGY 2000

Epidemiologic patterns of
chronic and aggressive
periodontitis
R Y A N T. D E M M E R & P A N O S N. P A P A P A N O U

The currently used definitions of chronic and patient, one quickly recognizes that appropriate
aggressive periodontitis were introduced at the 1999 assignment of this particular diagnosis by the clini-
World Workshop for the Classification of Periodontal cian – let alone by the epidemiologist – remains
Diseases and Conditions (2). This revised classifica- highly problematic.
tion system was intended to address a number of Nevertheless, use of the search terms Ôchronic
widely recognized shortcomings of the 1989 World periodontitisÕ or Ôaggressive periodontitisÕ in the
Workshop diagnostic scheme, according to which the PubMed database (as of July 2009) identified
majority of the pathologic periodontal conditions approximately 3300 and 1650 publications, respec-
were classified under the following three main tively. Interestingly, articles using the term Ôchronic
categories: ÔEarly Onset PeriodontitisÕ, ÔAdult Perio- periodontitisÕ covered a time span dating back to
dontitisÕ and ÔRefractory PeriodontitisÕ. The 1999 1948, while the earliest indexed article retrieved
Classification did indeed address some key deficien- using Ôaggressive periodontitisÕ as a keyword was
cies of the earlier system, including: (i) the lack of a also published in 1948, indicating that these terms
diagnostic category describing exclusively gingival have obviously been used in a variety of different
lesions; (ii) the dependence on knowledge about the contexts. Hence, given the substantial body of lit-
time of disease onset for distinguishing between erature using these terms, and in order to contrast
ÔEarly Onset PeriodontitisÕ and ÔAdult PeriodontitisÕ; with earlier reviews of the epidemiology of peri-
and (iii) the highly heterogeneous ÔRefractory Perio- odontitis that relied heavily on publications
dontitisÕ group, a term whose appropriate use re- employing terminology no longer in use (10, 40), we
quired prior knowledge of the volume and quality of decided to limit the present text to epidemiologic
therapy rendered, as well as of patient compliance. studies published over the past decade, anticipating
Nevertheless, although one of the explicitly expressed that they would have utilized the 1999 World
goals of the 1999 Classification was Ôto discard clas- Workshop nomenclature. For an overview of the
sification terminologies that were age-dependent or literature published prior to 1999, the reader is re-
required knowledge of rates of progressionÕ (5), the ferred to the earlier publications referred to above.
new system admittedly offered only limited sub- In our review, we first address some methodological
stantial improvement on either front. For example, considerations related to the assessment of chronic
one of the primary features of the newly introduced and aggressive periodontitis in epidemiologic stud-
ÔAggressive PeriodontitisÕ is Ôrapid attachment loss ies. We particularly address the issue of disease
and bone destructionÕ (33). With respect to age, Ôcir- onset and the impact of age in the determination of
cumpubertal onsetÕ continues to constitute a key diagnosis. Subsequently, we present current data on
feature of localized aggressive periodontitis, while the global prevalence of destructive periodontitis
generalized aggressive periodontitis is suggested to and its variability with respect to demographic
Ôusually affect persons under 30 years of age, but characteristics. Our review does not include the
patients may be olderÕ (33). Considering that another study of diagnosis-specific genetic and environ-
primary diagnostic feature of aggressive periodontitis mental risk factors for chronic or aggressive
is Ôfamilial aggregationÕ of the disease, a feature that is periodontitis, as these are dealt with in detail by
often impossible to ascertain upon examination of a Shapira et al. in this volume.

28
Epidemiologic patterns of chronic and aggressive periodontitis

higher the risk for invalid estimates when using a


Methodological issues – case partial-mouth methodology. Thus, there is consensus
definition that the best means of accurately assessing the
prevalence, extent and severity of periodontitis in an
Earlier reviews (10, 39, 40) have pointed out the lack epidemiologic study is by using a full-mouth clinical
of uniformity in the definition of periodontitis in examination (i.e. by using probing assessments at
epidemiologic studies and the resulting substantial multiple sites per tooth for all teeth present). There is
variability in the global prevalence estimates of the also a need to standardize additional sources of var-
disease that is caused by methodological inconsis- iation across studies, including probe tip dimensions
tencies alone. In fact, a recent methodological study and manual or pressure-sensitive devices and, most
has objectively quantified the influence of case defi- importantly, to use carefully calibrated clinical
nition on the prevalence of periodontitis by demon- examiners.
strating that periodontitis prevalence rates varied We want to draw the attention of the reader to the
from 14 to 65% when using six different case defi- fact that the methodological variability discussed
nitions among the same participants (14). Likewise, above relates solely to the definition of the Ôperio-
in a publication discussing the impact of using four dontitis caseÕ, irrespective of clinical diagnosis.
different classification systems to describe perio- As alluded to in the Introduction, the distinction
dontal conditions in adolescents (37), discrepancies between chronic periodontitis and aggressive
in periodontitis prevalence estimates of a factor of 10 periodontitis presents with additional complexity.
and a factor of 30 were noted for localized and gen- Although the primary clinical variables recorded for
eralized periodontitis, respectively. While it is well the assessment of either disease are identical, a dif-
accepted that the site-specific diagnosis of perio- ferential diagnosis between them must be made by
dontitis requires the combined presence of clinical contrasting the primary features of each disease, as
inflammatory signs (manifested as bleeding on described in the 1999 World Workshop consensus
probing), loss of connective tissue support (i.e. reports. However, none of the three primary features
attachment loss) and probably – but not necessarily – of aggressive periodontitis (systemically healthy pa-
an increase in probing depth, unequivocal thresholds tient; rapid attachment loss and bone destruction;
defining destructive disease or pathologic deepening familial aggregation) (33) are capable of consistently
of the gingival crevice have not been universally ac- facilitating a correct differential diagnosis in the set-
cepted. More importantly, the extent of the disease ting of an epidemiologic study: the first because it is
(i.e. the number or percentage of affected dental entirely nonspecific, the second because it requires at
units required to ascribe a diagnosis of ÔperiodontitisÕ least a pair of examination occasions, and the third
to a particular patient) has varied greatly. A recent because it is frequently difficult to ascertain without
systematic review of the definitions of periodontitis extensive interviewing and adequate verification.
used in epidemiologic studies (43) reported that the What appears to be a single feasible approach facili-
site-specific thresholds for increased probing depth tating the differential diagnosis between the two
have ranged from ‡3 mm to ‡6 mm, and those for diseases, in the setting of an epidemiologic study and
clinical attachment loss have ranged from ‡1 mm to according to the 1999 classification framework, is a
‡6 mm. The required number or percentage of diagnostic tool that would factor in the age of the
affected teeth or tooth surfaces exceeding the site- patient in the diagnostic decision-making process. In
specific thresholds to qualify a proband as a case has this context, it is important to realize that although
ranged from a minimum of one or more teeth (4) to the 1999 classification system abolished age as the
>30% of the sites in the dentition (48). primary classification criterion in the differential
Another important methodological consideration diagnosis of the different forms (and thus eliminated
pointed out earlier is the use of full-mouth vs. partial- the categories of Early Onset Periodontitis and adult
mouth examination protocols in the assessment of periodontitis), this should not be interpreted to sug-
periodontal conditions (18, 30–32). It is clear that the gest that age is to be disregarded from the diagnostic
validity of the estimates generated using a partial process. This is a point of paramount importance,
recording methodology will depend on the actual because an evaluation of the amount of supporting
prevalence and extent of periodontitis in the popu- periodontal tissue lost as a result of the disease in
lation in question and, consequently, on the age of relation to the duration of the exposure to the caus-
the subjects examined. The less prevalent and ⁄ or ative factors – reflected through the age of the indi-
extensive the disease in a particular population, the vidual subject – is frequently the sole means of

29
Demmer & Papapanou

ascertaining whether the disease is ÔaggressiveÕ based As discussed earlier, the attachment loss criteria
on a single examination. used in the Centers for Disease Control ⁄ American
However, utilization of a combined Ôattachment Academy of Periodontology definitions do facilitate a
loss in relation to ageÕ diagnostic tool for the differ- distinction between periodontitis and incidental
ential diagnosis between chronic periodontitis and attachment loss because they are applied exclusively
aggressive periodontitis in the setting of an epidem- to interproximal surfaces and require the presence of
iologic study requires the introduction of additional at least two affected teeth in the dentition. However,
criteria with respect to severity and extent. This is these definitions (i) do not incorporate any measure
essential for several reasons, which are discussed of current inflammatory status; and (ii) classify an
below. individual harboring as few as two 5-mm interprox-
First, the consensus reports of the 1999 World imal pockets into the Ômoderate periodontitisÕ
Workshop clarified that young individuals can also be category; therefore, they obviously increase the
affected by chronic periodontitis as a result of expo- probability for false-positive diagnoses. Interestingly,
sure to etiologic agents. Therefore, the maximum the authors of the report postulated that Ôfor the
amount of periodontal tissue loss in young individ- purposes of surveillance, there seems to be no reason
uals that can be considered as commensurate to the for separating chronic and aggressive periodontitisÕ
level of exposure to etiologic agents, with respect to (38), acknowledging that the proposed system is
its intensity and duration, and thus may be regarded incapable of distinguishing between the two forms of
as compatible with the diagnosis of chronic the disease.
periodontitis, needs to be defined. As will become evident by the systematic query of
Second, it is well recognized that attachment loss the recent literature described later, despite the
may frequently manifest itself in buccal tooth sur- extensive use of the terms ÔchronicÕ and ÔaggressiveÕ
faces of young subjects as a result of trauma caused periodontitis, no epidemiological studies explicitly
by faulty oral hygiene practices. Therefore, a dis- attempting to segregate between the two diagnoses
tinction between trauma-induced recession and have so far been carried out. Instead, the available
periodontitis is required. studies have aimed to describe the prevalence, extent
Third, attachment loss may develop at individual and severity of a single clinical pathologic condition,
teeth for reasons other than periodontitis or trauma, namely ÔperiodontitisÕ. Thus, in order to interpret the
including tooth malposition, advanced endodontic literature with respect to our assigned task, but also
lesions and tooth fractures. It is thus reasonable to as a basis for future studies that will attempt to dis-
propose that a reliable distinction between perio- tiguish between chronic periodontitis and aggressive
dontitis-induced attachment loss and incidental periodontitis, we propose an adaptation of the above
attachment loss resulting from different etiologies Centers for Disease Control ⁄ American Academy of
will require involvement of a minimum of two, Periodontology definitions to incorporate an assess-
nonadjacent tooth surfaces located on different teeth. ment of the loss of periodontal tissue in relation to
In a recent publication (38), a working group from age, as follows.
the Centers for Disease Control and the American In individuals £25 years of age, the presence of two
Academy of Periodontology introduced a new case or more interproximal, nonadjacent sites with
definition for use in population-based surveillance of attachment loss of ‡4 mm occurring at a minimum of
periodontitis. This clinical definition of periodontitis two different teeth and accompanied by bleeding on
in epidemiologic studies was based on a combination probing, will signify aggressive periodontitis. In
of probing depth and clinical attachment levels individuals between 26 and 35 years of age, a diag-
assessments as follows. nosis of aggressive periodontitis will require the
Severe periodontitis was characterized as the pres- presence of two or more interproximal, nonadjacent
ence of two or more interproximal sites with clinical sites with attachment loss of ‡6 mm occurring at a
attachment loss of ‡6 mm, not on the same tooth, minimum of two different teeth and accompanied by
and the presence of one or more interproximal sites bleeding on probing. In other words, our proposed
with a probing depth of ‡5 mm. criteria (i) define the maximum attachment loss that
Moderate periodontitis was defined as the presence may be considered as compatible with chronic
of two or more interproximal sites with clinical periodontitis as a function of the age of the examinee;
attachment loss of ‡4 mm occurring at two or more and (ii) incorporate a measure of current inflamma-
different teeth or two or more interproximal sites with tory status, expressed through bleeding on probing,
a probing depth of ‡5 mm, not on the same tooth. rather than a threshold for a deepened periodontal

30
Epidemiologic patterns of chronic and aggressive periodontitis

pocket. We consider the latter point as an advantage for a Classification of Periodontal Diseases and
over the Centers for Disease Control ⁄ American Conditions (33, 36). However, our initial screening of
Academy of Periodontology proposal because the published literature suggested a dearth of preva-
destructive disease with no concomitant deep pock- lence data based on the above definitions and
ets, reported to occur in some Asian and African diminished the potential for producing a meaningful
populations (6–8), will still be captured when using review. Conversely, this initial screening identified a
our proposed system. However, the above age- number of studies that reported prevalence data
adjusted approach will admittedly fail to facilitate the based on either the recently published joint Centers
differential diagnosis between severe chronic perio- for Disease Control ⁄ American Academy of Perio-
dontitis and aggressive periodontitis in a subject dontology definition (38) or on the extent and
older than 35 years of age. Access to disease-pro- severity of clinical attachment loss beyond specific
gression data derived from sequential examinations severity thresholds (i.e. from 3 to 6 mm). We there-
and ⁄ or confirmation of familial aggregation accord- fore decided to additionally include periodontitis
ing to the 1999 consensus report seem to be the only prevalence data based on these definitions. Although
way to distinguish between severe chronic perio- this approach is still not ideal for reviewing global
dontitis and aggressive periodontitis in older periodontitis prevalence data, it is a reasonable
patients, but the feasibility of such an approach in compromise that will facilitate a broader comparison
the setting of an epidemiologic study remains highly of data based on comparable definitions of peri-
questionable. odontitis.
We also feel that the secondary descriptors of Our initial screening of the literature focused on (i)
severity of chronic periodontitis (i.e. the terms ÔslightÕ, human studies; (ii) those published in the English
ÔmoderateÕ and ÔsevereÕ) that have been recom- language between 1 January 2000 [i.e. immediately
mended in the consensus report (36) may also benefit after the publication of the Consensus documents
from an age-adjustment. For example, an attachment (1)] and the date of the search (19 July 2009); and (iii)
loss of 5 mm affecting multiple interproximal sites in those that included in the title or abstract either of
a 30-year-old individual arguably represents a disease the words ÔperiodontalÕ or ÔperiodontitisÕ in addition
of different severity from that occurring in an 80- to either of the words ÔepidemiologyÕ or ÔprevalenceÕ
year-old patient, as it signifies an entirely different in addition to the word ÔpopulationÕ. Thus, the
prognosis with respect to tooth survival. In the latter complete PubMed search criteria were defined as
case, but not in the former case, this level of attach- follows: (((periodontal[Title ⁄ Abstract]) OR (peri-
ment loss is probably compatible with the retention odontitis[Title ⁄ Abstract])) AND ((epidemiology [Ti-
of the entire dentition throughout the patientÕs life. tle ⁄ Abstract]) OR (prevalence [Title ⁄ Abstract])))
Therefore, we suggest that an age-based adjustment AND (Ô2000Õ[Publication Date] : Ô2009 ⁄ 07 ⁄ 19Õ[Publi-
of severity may result in a more meaningful perio- cation Date]) AND (English[Language]) AND (popu-
dontal diagnosis, when used in epidemiologic studies lation[Title ⁄ Abstract]) AND (Humans[Filter])).
and, particularly, in the clinical setting. Systems de- This search strategy identified a total of 289 pub-
scribed previously that have used the amount of lications. All abstracts were reviewed and publica-
periodontal tissue support loss in relation to both the tions were excluded from further consideration for
root length of the particular tooth and the age of the the following reasons: (i) the manuscript did not
individual to define thresholds that seem to be present periodontitis prevalence data based on any of
incompatible with long-term tooth survival (49) may the definitions used in this review (i.e. the 1999
be useful in this context. International Classification Workshop criteria (33,
36), the Centers for Disease Control ⁄ American
Academy of Periodontology criteria (38) or the extent
Estimates of prevalence, severity of attachment loss beyond specific thresholds); (ii)
data arose from a highly selected population that
and extent severely limited the generalizability and representa-
tiveness of the data for the underlying population
Cross-sectional data
(e.g. studies exclusively of participants with type 2
As noted above, our original intent was to provide a diabetes); (iii) the study specifically excluded partic-
summary of published prevalence data for chronic ipants without periodontitis and thus precluded the
periodontitis and aggressive periodontitis based on calculation of prevalence estimates; and (iv) the re-
the definitions of the 1999 International Workshop sults were entirely duplicative of another publication

31
Demmer & Papapanou

from the same population. Using these additional participants tended to experience periodontitis of
restrictions, a total of 21 publications were consid- higher severity. Interestingly, Table 2 also indicates
ered eligible for final review. that, in France (11), mild periodontitis tended to be
We organized the data from the above studies into equally split between localized and generalized
three Tables. Table 1 presents prevalence estimates forms, whereas moderate and severe periodontitis
based on the Centers for Disease Control ⁄ American occurred more frequently in a generalized form than
Academy of Periodontology definitions (38). Table 2 in a localized form. The opposite trend was observed
uses the severity thresholds of the 1999 International in the Canadian data. The reasons for these patterns
Classification Workshop (5). Finally, Table 3 presents are unclear but are probably the consequence of ei-
estimates of periodontal disease according to extent ther differential tooth-extraction practices or differ-
and severity of clinical attachment loss. While Table 3 ential periodontal treatment availability in the two
does not allow for meaningful inferences on the source populations. In comparison to the French and
prevalence of chronic periodontitis vs. aggressive Canadian studies, the two reports from Brazil (16, 46)
periodontitis, it does allow for some level of stan- indicate a very high level of severe generalized
dardized comparison of periodontal destruction periodontitis, although these data are not represen-
across various populations and age and gender sub- tative of the entire Brazilian population.
groups. Only a single study fulfilling the inclusion criteria
Severe periodontitis prevalence estimates based on of our search presented data on aggressive perio-
the Centers for Disease Control ⁄ American Academy dontits (35). Specifically, this study examined perio-
of Periodontology definition (Table 1) ranged from dontal conditions among male and female Israeli
1% among 20–29-year-old participants in the Study army personnel who were between 18 and 30 years of
of Health in Pomerania report (27) to 39% among age, and reported a prevalence of localized aggressive
participants ‡65 years of age in the Erie County Study periodontitis of 4% while the prevalence of general-
(23). The substantial variation in these estimates was ized aggressive periodontitis was found to be 2%.
largely caused by the variation in age ranges of par- This surprising paucity of prevalence data for
ticipants included. In comparisons across relatively aggressive periodontitis is primarily because most
homogeneous age ranges, less variability is evident. studies initially identified using the term Ôaggressive
For example, when considering the prevalence of periodontitisÕ in their title or abstract were conducted
severe periodontitis among participants approxi- exclusively among participants who were determined
mately 40–50 years of age, estimates were 21% in to have the disease before enrollment. Therefore, true
Germany (27), and 16% (47), 28% and 32% (23) in prevalence estimates could not be determined based
various populations from the USA. However, varying on these reports. Likewise, case-control study designs
risk factor distributions and access to dental care were commonly utilized in the context of aggressive
across populations have certainly also contributed periodontitis, which also precluded the computation
beyond age to the overall variability in prevalence of valid prevalence estimates. As a result, the global
estimates. Notably, nationally representative esti- prevalence of aggressive periodontitis remains elu-
mates of severe periodontitis, according to the sive, which is reflective of the unresolved debate
Centers for Disease Control ⁄ American Academy of about its accurate definition. In order to mitigate this
Periodontology definitions in the general adult pop- lack of prevalence data on aggressive periodontitis,
ulation, were only available from the USA (15) and we attempted to bridge our aforementioned sug-
Australia (45) and show the respective prevalences to gested adaptation to the Centers for Disease
be 2% and 4%. Control ⁄ American Academy of Periodontology defi-
Using the 1999 International Workshop severity nitions using the currently available data as follows:
thresholds (Table 2), prevalence estimates for gen- (i) the criteria for our proposed definition of aggres-
eralized severe periodontitis ranged from 6 (12) to sive periodontitis among participants £25 years of
50% (46), and were highest (92%) for individuals age are met or exceeded by the Centers for Disease
‡70 years of age in a Brazilian cohort (46). The two Control ⁄ American Academy of Periodontology defi-
studies reporting prevalence estimates across all nition of moderate or severe periodontitis; and (ii)
three severity categories (11, 12) (Table 2) both indi- our proposed definition of aggressive periodontitis
cate that nearly all participants have some form of among participants 26–35 years of age most closely
periodontitis, although a substantial proportion of corresponds to the Centers for Disease Control ⁄
the periodontitis was mild in the French population American Academy of Periodontology definition of
(11). By contrast, the Canadian data (12) indicate that severe periodontitis. Using these approximations,

32
Table 1. Prevalence estimates based on qualifying studies using the Centers for Disease Control ⁄ American Academy of Periodontology Working Group definition
(15)

All Male participants Female participants


Examina-
Authors ⁄ Age (in tion None ⁄ Edentu- None ⁄ Edentu- None ⁄ Edentu-
Country n1 years) method Mild Moderate Severe lism Mild Moderate Severe lism Mild Moderate Severe lism
Holtfreter 3557 20–81 HM, 4 49% 33% 18% 12%2 46% 33% 21% NR 52% 33% 14% NR
et al. sites
587 20–29 88% 12% 1% NR 87% 12% 1% NR 88% 11% 1% NR
2009;
Germany; 745 30–39 66% 27% 7% NR 62% 28% 9% NR 70% 25% 5% NR
(SHIP)
(27) 714 40–49 37% 42% 21% NR 30% 45% 25% NR 44% 39% 17% NR
695 50–59 26% 43% 31% NR 21% 39% 41% NR 32% 47% 22% NR
544 60–69 20% 47% 33% NR 14% 45% 41% NR 26% 49% 26% NR
267 70–81 26% 44% 29% NR 21% 44% 35% NR 29% 45% 26% NR
Costa 340 30–45 FM, 4 sites 45% 41% 14% NR NR NR NR NR NR NR NR NR
et al.
2009;
Brazil
(14)
Slade 2999 15–90 FM, 3 sites 71% 25% 4% NR NR NR NR NR NR NR NR NR
et al.
2007;
Australia3
(NSAOH)
(45)
DÕAiuto 13677 17+ HM, 2 86% 12% 2% NR NR NR NR NR NR NR NR NR
et al. sites
2008;
USA3;
(NHANES
III)
(15)
Genco 1578 35–72 FM, 6 sites 19% 52% 30% NR 13% 51% 37% NR 30% 54% 19% NR
et al.
50 35–39 36% 60% 4% NR NR NR NR NR NR NR NR NR
2007;
USA; 630 40–54 24% 49% 28% NR NR NR NR NR NR NR NR NR
(MI-Perio
Study) 425 55–64 17% 54% 30% NR NR NR NR NR NR NR NR NR
(23)
Epidemiologic patterns of chronic and aggressive periodontitis

33
374 65+ 13% 55% 33% NR NR NR NR NR NR NR NR NR
34
Table 1. Continued

All Male participants Female participants

Examina-
Authors ⁄ Age (in tion None ⁄ Edentu- None ⁄ Edentu- None ⁄ Edentu-
Demmer & Papapanou

Country n1 years) method Mild Moderate Severe lism Mild Moderate Severe lism Mild Moderate Severe lism
Genco 1438 25–74 FM, 6 sites 27% 42% 31% NR 25% 40% 35% NR 31% 45% 25% NR
et al.
116 25–29 50% 40% 10% NR NR NR NR NR NR NR NR NR
2007;
USA; 277 30–39 38% 38% 24% NR NR NR NR NR NR NR NR NR
(Erie
County 383 40–54 24% 33% 32% NR NR NR NR NR NR NR NR NR
Study) 134 55–64 23% 45% 32% NR NR NR NR NR NR NR NR NR
(23)
215 65+ 15% 46% 39% NR NR NR NR NR NR NR NR NR
Taylor & 455 18–93 FM, 4 sites 64% 24% 12% NR 60% 22% 18% NR 66% 26% 8% NR
Borg-
105 18–25 89% 9% 2% NR NR NR NR NR NR NR NR NR
nakke
2007; 128 30–39 78% 20% 2% NR NR NR NR NR NR NR NR NR
USA (47)
129 40–54 56% 28% 16% NR NR NR NR NR NR NR NR NR

41 55–64 29% 34% 37% NR NR NR NR NR NR NR NR NR


52 65+ 23% 46% 31% NR NR NR NR NR NR NR NR NR
Phipps 1210 65–95 FM, 6 sites NR NR 26% 10% NR NR 26% 10% NR NR NR NR
et al.
634 65–74 NR NR 23.3% NR NR NR 23.3% NR NR NR NR NR
2009;
USA; 576 75+ NR NR 28% NR NR NR 28% NR NR NR NR NR
(MrOS)
(42)
Do 3161 15+ FM, 3 sites 77% 23%2 NR 72% 28%2 NR 82% 18%2 NR
et al. 2
598 15–34 92% 8% NR NR NR NR NR NR NR
2008;
Australia3; 1331 35–54 78% 22%2 NR NR NR NR NR NR NR
(NSAO-
2
H)(19) 692 55–64 60% 40% NR NR NR NR NR NR NR
2
540 65+ 48% 52% NR NR NR NR NR NR NR
Table 1. Continued

All Male participants Female participants

Examina-
Authors ⁄ Age (in tion None ⁄ Edentu- None ⁄ Edentu- None ⁄ Edentu-
Country n1 years) method Mild Moderate Severe lism Mild Moderate Severe lism Mild Moderate Severe lism
Dye 16128 20+ HM, 2 86% 14%2 NR 82% 18%2 NR 89% 7%2 NR
et al. sites
5126 20–34 97% 3%2 0.5% NR NR NR NR NR NR
2007;
USA3; 4065 35–49 91% 9%2 4% NR NR NR NR NR NR
(NHANES
2
III 2982 50–64 80% 20% 17% NR NR NR NR NR NR
1988– 2
2084 65–74 76% 24% 29% NR NR NR NR NR NR
1994) (21)
2
1871 75+ 71% 29% 43% NR NR NR NR NR NR

Dye 13159 20+ HM, 2 92% 8%2 NR 90% 10%2 NR 95% 5%2 NR
et al. sites
3593 20–34 NR NR NR NR NR NR NR NR NR
2007;
USA3; 2
3250 35–49 95% 5% 3% NR NR NR NR NR NR
(NHANES
2
1999– 2777 50–64 89% 11% 10% NR NR NR NR NR NR
2004) (21) 1816 65–74 86% 14%2 24% NR NR NR NR NR NR
1723 75+ 80% 20%2 32% NR NR NR NR NR NR
1
Sample size reported for dentate participants.
2
Periodontitis definition was not separated according to moderate or severe but rather as a combination of moderate and severe.
3
Indicates nationally representative samples.
FM, full mouth; HM, half mouth; MrOS, Osteoporotic Fractures in Men Study; NHANES, National Health and Nutrition Examination Survey; NR, not reported; NSAOH, Australian National Survey of Adult Oral; Health; SHIP, Study
of Health in Pomerania.
Epidemiologic patterns of chronic and aggressive periodontitis

35
36
Table 2. Prevalence estimates based on qualifying studies using the 1999 International Classification Workshop severity criteria (2)

Age (in Mild Moderate Severe


Authors ⁄ years) ⁄ Examination
Country n Gender method Localized Generalized Localized Generalized Localized Generalized
Brothwell & 94 18+, M ⁄ F PM, 6 sites 1% 34% 27% 16% 16% 6%
Demmer & Papapanou

Ghiabi 2009;
Canada (Sandy
Bay First
Nation in
Manitoba) (12)
Bourgeois 2144 35–64, M ⁄ F FM, 22% 27% 2% 25% 1% 19%
et al. 4 sites
35–39, M 26% 31% 3% 22% 0.4% 10%
2007; France;
(NPSES) (11) 35–39, F 31% 31% 4% 19% 1% 6%
40–49, M 19% 28% 1% 31% 1% 16%
40–49, F 30% 29% 2% 19% 1% 13%

50–59, M 17% 23% 1% 26% 1% 31%


50–59, F 22% 23% 2% 28% 2% 21%
60–64, M 12% 19% 3% 26% 1% 38%
60–64, F 17% 30% 1% 30% 1% 21%
Dalla Vecchia 706 30–65, M ⁄ F FM, NR NR NR NR NR 43%
et al. 2005; 6 sites
329 30–65, M NR NR NR NR NR 51%
Brazil (16)
377 30–65, F NR NR NR NR NR 35%
Susin 848 30–103, M ⁄ F FM, NR NR NR NR NR 50%
et al. 6 sites
249 30–39, M ⁄ F NR NR NR NR NR 22%
2004; Brazil
(46) 253 40–49, M ⁄ F NR NR NR NR NR 58%
175 50–59, M ⁄ F NR NR NR NR NR 65%
84 60–69, M ⁄ F NR NR NR NR NR 73%
42 70+, M ⁄ F NR NR NR NR NR 92%

F, female; FM, full-mouth; M, male; NR, not reported; NPSES, National Periodontal Systemic Examination Survey project; PM, partial-mouth examination of pre-specified index teeth.
Table 3. Estimates of clinical attachment loss severity and extent based on qualifying studies

Examina- All Male participants Female participants


Authors ⁄ Age (in tion
Country n1 years) method %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6
Holtfreter 3557 20–81 HM, 4 63% 41% 27% 18% 97% 43% 29% 20% 60% 38% 24% 15%
et al. 2009; sites
587 20–29 22% 5% 2% 1% 24% 6% 2% 1% 20% 5% 1% 0.4%
Germany;
(SHIP) 745 30–39 50% 22% 10% 5% 53% 24% 11% 6% 46% 19% 8% 4%
(27)
714 40–49 72% 47% 30% 19% 76% 52% 34% 23% 68% 41% 26% 15%
695 50–59 82% 59% 42% 28% 86% 66% 48% 35% 79% 53% 36% 22%
544 60–69 91% 75% 56% 40% 95% 80% 64% 48% 88% 69% 49% 33%
267 70–81 95% 83% 68% 50% 97% 85% 71% 55% 95% 83% 64% 48%
Phipps 1210 65–95 FM, 6 sites NR NR 13% NR NR NR 13% NR NR NR NR NR
et al. 2009;
634 65–74 NR NR 12% NR NR NR 12% NR NR NR NR NR
USA;
(MrOS) 576 75+ NR NR 15% NR NR NR 15% NR NR NR NR NR
(42)

Costa 340 30–45 FM, 4 sites NR NR NR 8% NR NR NR NR NR NR NR NR


et al. 2009;
Brazil (14)
Do et al. 3161 15+ FM, 3 sites NR 3.5% NR NR NR NR NR NR NR NR NR NR
2008;
Australia;
(NSAOH)
(19)
Lee et al. 1234 20+ HM, 1 site NR 7% NR NR NR NR NR NR NR NR NR NR
2008; USA;
(NHANES
1999–
2002) (34)
Epidemiologic patterns of chronic and aggressive periodontitis

37
38
Table 3. Continued

All Male participants Female participants


Examina-
Demmer & Papapanou

Authors ⁄ Age (in tion


Country n1 years) method %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6
Corraini 39 12–19 FM, 6 sites 20% NR 0.1% NR NR NR NR NR NR NR NR NR
et al. 2008;
62 20–29 26% NR 2% NR NR NR NR NR NR NR NR NR
Brazil
(13) 40 30–39 41% NR 9% NR NR NR NR NR NR NR NR NR
27 40–49 57% NR 21% NR NR NR NR NR NR NR NR NR
46 50+ 79% NR 44% NR NR NR NR NR NR NR NR NR
Bourgeois 2144 35–64 FM, 4 sites 29% 9% 3% 0.9% 32% 10% 4% 1.0% 27% 8% 2% 0.5%
et al. 2007;
35–39 22% 5% 1% 0.3% 24% 5% 1% 0.3% 20% 4% 1% 0.2%
France;
(NPSES) 40–49 28% 8% 3% 0.8% 32% 10% 3% 1.0% 24% 7% 2% 0.5%
(11)
50–59 32% 12% 5% 1.2% 35% 40% 42% 31% 30% 10% 3% 0.7%
60–64 37% 14% 6% 1.5% 41% 18% 8% 2% 35% 11% 4% 0.9%
Elter et al. 6744 45–64 FM, 6 sites 13% NR NR NR NR NR NR NR NR NR NR NR
2004;
USA(22)
Des- 55+ FM, 6 sites NR 41% NR NR NR NR NR NR NR NR NR NR
varieux
et al. 2003;
USA;
(INVEST)
(17)
Baelum 209 30–39 FM, 6 sites NR 24% NR NR NR 25% NR NR NR 23% NR NR
et al. 2003;
Thailand
(7)
Table 3. Continued

All Male participants Female participants


Examina-
Authors ⁄ Age (in tion
Country n1 years) method %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6 %AL‡3 %AL‡4 %AL‡5 %AL‡6
Do et al. 575 35–44 FM, 2 sites 22%** 12% 5% 3% NR NR NR NR NR NR NR NR
2003;
Vietnam
(20)
Papapa- 103 30–34 FM, 6 sites NR NR 5% NR NR NR NR NR NR NR NR NR
nou et al.
104 35–39 NR NR 11% NR NR NR NR NR NR NR NR NR
2002;
Thailand 71 50–54 NR NR 27% NR NR NR NR NR NR NR NR NR
(41)
78 55–59 NR NR 32% NR NR NR NR NR NR NR NR NR
Griffiths 100 16–20 FM, 4 sites 1% NR NR NR NR NR NR NR NR NR NR NR
et al.
2001;
Britain
(25)
Albandar 9689 30–90 HM, 2 20% NR NR NR 23% NR NR NR 17% NR NR NR
et al. sites
30–39 8% NR NR NR 10% NR NR NR 6% NR NR NR
1999;
USA1; 40–49 16% NR NR NR 21% NR NR NR 11% NR NR NR
(NHAN-
ES III) 50–59 28% NR NR NR 33% NR NR NR 23% NR NR NR
(1) 60–69 35% NR NR NR 40% NR NR NR 29% NR NR NR
70–79 39% NR NR NR 42% NR NR NR 36% NR NR NR
80–90 50% NR NR NR 54% NR NR NR 47% NR NR NR

Note that data in this table represent the mean percentage of sites per mouth beyond specified severity thresholds (3–6 mm). These data do not represent the prevalence of any disease at the given severity thresholds.
1
The NHANES III data presented by Albandar et al. (1) was published before the 1999 International Classification Workshop (40). We identified this publication via bibliography reviews and include it because it presents
comparable, nationally representative data that we were unable to locate elsewhere.
AL, attachment loss; FM, full mouth; HM, half mouth; INVEST, Oral Infections and Vascular Disease Epidemiology Study; MrOS, Osteoporotic Fractures in Men Study; NSAOH, Australian National Survey of Adult Oral Health;
NHANES, National Health and Nutrition Examination Survey; NPSES, National Periodontal Systemic Examination Survey project; NR, not reported; SHIP, Study of Health in Pomerania.
Epidemiologic patterns of chronic and aggressive periodontitis

39
Demmer & Papapanou

it appears that the prevalence of aggressive perio- mation of the disease. The degree of overestimation
dontitis among individuals younger than 35 years of vs. underestimation is currently impossible to deter-
age ranges from approximately 1% to a maximum mine. Similarly, the Australian national data (19) also
of 15%, depending on the age of participants and merged the Centers for Disease Control ⁄ American
the study. For example, data from the Study of Health Academy of Periodontology definitions of moderate
in Pomerania (27) show the prevalence of moderate ⁄ and severe periodontitis and grouped participants
severe periodontitis among participants £29 years of who were 15–35 years of age, making the results
age to be 13% and the prevalence of severe perio- difficult to reconcile with our proposed definition.
dontitis among participants 30–39 years of age to be Thus, the ÔceilingÕ estimate for the prevalence of
7%. As the Centers for Disease Control ⁄ American aggressive periodontitis in the Australian population
Academy of Periodontology definitions are likely to is 8%. It should be noted that, overall, these estimates
be overestimates of what our proposed definition of aggressive periodontitis mostly ignore disease
would yield, in addition to the fact that the reported among adolescents, as only three studies included
age ranges in Table 1 include participants over the participants under 20 years of age (15, 19, 47). Con-
ages of 25 and 35 years, respectively, further overes- sequently, the ÔceilingÕ estimates are almost certainly
timation is probable. However, in the Study of Health overestimates of aggressive periodontitis in any
in Pomerania, these overestimates were probably source population, including the full age range of
offset to some degree by the use of half-mouth adolescents.
examinations (which generally underestimate disease Table 3 provides estimates of the extent of clini-
prevalence). Consequently, these estimates of 13% cal attachment loss across various severity thresh-
and 7% are almost certainly biased towards overes- olds and demonstrates that the prevalence of
timation. Although the degree of overestimation attachment loss extent varies substantially across
cannot be precisely established from these data, it age, gender and region. Similarly to the trends seen
appears useful to define an approximate ÔceilingÕ in Tables 1 and 2, the estimates of extent of
characterizing the highest likely estimate of aggres- attachment loss in Table 3 were consistently higher
sive periodontitis in a given population. In compari- in men vs. women and among older participants vs.
son, applying this approach to the prevalence data younger participants. Of the 14 studies presented in
reported by Genco and colleagues (23) in the Erie Table 3, seven provided estimates for extent of
County Study, suggests a prevalence ÔceilingÕ of attachment loss for either the 3- or 4-mm severity
approximately 15% for aggressive periodontitis thresholds, six provided estimates for the 5-mm
(averaging severe periodontitis estimates for the age threshold and four provided estimates for attach-
ranges 25–29 and 30–39 years and considering that ment loss beyond the 6-mm threshold. Although
approximately one-third of participants were over extent and severity definitions are not specific
35 years of age and should not contribute to the enough for clinical definitions of periodontitis, their
estimate), while data from the Osteoporotic Fractures ease of use and general resistance to underestima-
in Men study suggest a prevalence ÔceilingÕ of 11% for tion in protocols using anything less than a
aggressive periodontitis among participants under full-mouth examination makes them an attractive
26 years of age (42). In contrast, the National Health option for reporting in epidemiologic studies.
and Nutrition Examination Survey III (21) data sug- However, continuous extent and severity definitions
gest an aggressive periodontitis ÔceilingÕ prevalence of (i.e. the mean percentage of sites per mouth that
around 3% but these estimates are difficult to rec- exhibits attachment loss at or above specific
oncile with our proposed definition of aggressive severity thresholds) are not dichotomous and
periodontitis because they (i) combine moderate and thereby fail to identify what proportion of a popu-
severe periodontitis categories (according to the lation exhibits disease at a given threshold.
Centers for Disease Control ⁄ American Academy of Despite the substantial interstudy variation in the
Periodontology definition); and (ii) combine the data reported periodontitis prevalence estimates, the data
from participants 20–35 years of age, which com- corroborate the well-established notion in the
pletely merges the two age ranges we have suggested periodontal literature that (i) men experience more
(£25 years and 26–35 years). Taken together, these periodontitis than women, although the disparity
two facts are likely to overestimate the prevalence of varied considerably across studies; and (ii) the prev-
aggressive periodontitis, while the half-mouth alence of periodontitis increases with age. In regard
examinations in the National Health and Nutrition to the consistently observed age gradient, the data
Examination Survey certainly result in an underesti- indicate that the prevalence of periodontitis, based on

40
Epidemiologic patterns of chronic and aggressive periodontitis

the Centers for Disease Control ⁄ American Academy under consideration, the within-study consistency of
of Periodontology definition, tends to peak around their case definition over time still provides a
the 5th or 6th decade of life, at which point the trend meaningful estimate of variation in prevalence
stabilizes or at least attenuates. For example, data patterns. Moreover, National Health and Nutrition
from the Study of Health in Pomerania (27) demon- Examination Survey data published by Dye et al. (21),
strate that severe periodontitis (Centers for Disease and presented in Table 1, show similar patterns of
Control ⁄ American Academy of Periodontology defi- decline in periodontitis.
nition) increases by 30 fold between the 3rd and 6th Likewise, a number of studies from Scandinavia
decade of life, from 1% to 31%, and then remains have demonstrated consistent improvements in
stable in individuals into their 80s (Table 1). Results periodontal health, although as noted earlier (24, 40),
from other populations were similar, although the these improvements tend to be restricted to gingivitis
gradient was not as extreme. In contrast to the results and mild ⁄ moderate forms of periodontitis, while the
in Table 1, a plateau of prevalence estimate trends in prevalence of more severe forms of periodontitis
the oldest age groups was not evident when using appears to remain relatively stable. Recently pub-
extent and severity definitions. Instead, the pre- lished data from four serial cross-sections over
valence of periodontitis in Table 3 generally increased 30 years demonstrate this point (28). These investi-
with older age and did not show signs of levelling off gators reported general improvement in oral health
in the oldest age groups. This is probably influenced and that Ôthe proportion of periodontally healthy
by the reduced specificity of extent and severity individuals increased from 8% in 1973 to 44% in 2003
definitions, the prevalence of which increases for and the proportion of individuals with gingivitis and
reasons other than true periodontitis. moderate periodontitis decreased.Õ Interestingly,
despite decreases in moderate periodontitis, the
proportion of individuals with advanced forms of
Periodontitis prevalence time trends
periodontitis remained unchanged. These observa-
Few studies have been performed that allow a valid tions are unique and particularly valuable because of
estimation to be made of secular trends in perio- the high degree of periodontal examination stan-
dontitis prevalence. Again, one important reason for dardization over an extended time span. Similar
a lack of time trend data is the fact that periodontal trends, although based in less-precise methodologies,
examination protocols often vary over time. The have been published from Norway (44), Finland (3)
historical experience in the USA related to the and the Netherlands (29). Nevertheless, one should
National Health and Nutrition Examination Surveys be cautious to extrapolate from the above data and
is emblematic of this difficulty. Page & Eke (38) have conclude that the global prevalence of periodontitis is
recently summarized the complicated history of the declining, as the data reviewed above originate
National Health and Nutrition Examination Survey in exclusively from Europe and North America. It
relation to dental examination protocols and the should also be realized that tooth retention in older
subsequent difficulty in producing valid secular trend age cohorts may translate into the presence of teeth
data. Nevertheless, these authors concluded that Ôit is with some degree of attachment loss. In other words,
clear that the prevalence and severity of periodontitis a decline in edentulism must be expected to con-
have decreased significantly over the last 50–60 tribute to an increased prevalence of periodontitis
yearsÕ, although the precise magnitude of this in the elderly.
decrease is difficult to ascertain because of the con-
stant evolution of periodontal examination protocols
Limitations
and case definitions. Accordingly, focused analyses
restricted to recent National Health and Nutrition Some important limitations of, and caveats about,
Examination Survey cross-sections, using more this review should be noted. First, although we at-
comparable periodontal examination protocols, tempted to include only studies that provided rea-
support the concept of decreasing prevalence of sonable estimates of disease prevalence from the
periodontitis over time. Borrell et al. (9) reported that source population studied, most studies do not
periodontitis prevalence decreased by about 3% in comprise nationally representative population sam-
absolute terms from 7.3 to 4.2% and that these trends ples, which precludes true international compari-
were consistent across race ⁄ ethnic groups. Note that sons. In general, prevalence estimates arising from
although the definition of periodontitis in their national samples tended to be lower than estimates
analysis was different from the definitions presently arising from nonnational samples.

41
Demmer & Papapanou

Second, despite the fact that the inclusion criteria standardization is needed before comprehensive
applied in this review vs. older reviews resulted in global comparisons can be made. A decade after the
relatively homogeneous examination methodologies, introduction of the current system of Classification
the residual variation in the periodontal examination of Periodontal Diseases and Conditions, it is apparent
methods used among the reviewed studies must be that it is not possible to obtain an accurate estimate of
recognized. Important differences relate to full- the prevalence of the currently recognized major
mouth vs. half-mouth examination protocols, the diagnostic forms of periodontitis. As discussed earlier,
varying number of periodontal sites assessed per the defined primary features of the two diseases do
tooth and ⁄ or per mouth, and the types of perio- not facilitate a distinction between them in epidemi-
dontal probing devices used. These differences ologic studies. Thus, while more research is clearly
should be considered before making definitive needed before an evidence ⁄ biology based conver-
inferences based on any specific between-population gence on periodontitis definitions can emerge,
comparisons that may be of interest to the reader. adoption of additional criteria is essential to facilitate
Third, this review does not address periodontitis differential diagnosis in epidemiologic studies and
incidence. It is often tempting to speculate about to permit the accurate assessment of secular trends.
population incidence (number of new cases per time Over the past few years, a number of definitions for
period) patterns based on the observed prevalence descriptive epidemiologic studies of ÔperiodontitisÕ
patterns. However, because prevalence is a function as a single disease entity have emerged, such as the
of both incidence and disease duration (26), preva- joint Centers for Disease Control ⁄ American Academy
lence does not directly reflect incidence patterns and of Periodontology definition, as well as clinical
can be misleading in some situations. For example, attachment loss extent measures at specific severity
assume the age-standardized prevalence of peri- thresholds (incipient, moderate, advanced). It is
odontitis to be equal in populations A and B, but with essential for future epidemiologic studies of perio-
the treatment standards in population A favoring dontitis to provide data on attachment loss and
more aggressive tooth-extraction practices among inflammatory status with sufficient detail and in a
patients with periodontitis. In this case, the observed standardized manner so that more complex ÔcaseÕ
prevalence in population A is lower than what would definitions can be easily constructed and applied to
have been observed if tooth extractions were equally nationally representative data sets.
likely in population A vs. population B (i.e. more
teeth with periodontitis in population A were ex-
tracted and therefore are unavailable for recording in Acknowledgments
epidemiological studies). Therefore, as pointed out
by Hennekens & Buring (26), Ôa change in prevalence This work was supported by grants K99 DE-018739
from one time period to another may be the result of (R.T.D.) and DE015649 (P.N.P.) and a CTSA Award
changes in incidence rates, changes in the duration of RR025158.
disease, or bothÕ. Importantly, the same is true for
between-study variations in disease prevalence.
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