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Periodontology 2000, Vol.

16, 1998, 16-33 C o p y r i g h t 0 Muiiksgaard 1998


Priiited in Denniark All rights reserved
PERIODONTOLOGY 2000
ISSN 0906-6713

Epidemiology of periodontal
disease among older adults:
a review
DAVIDLOCKER,GARYD. SLADE& HEATHER
MURRAY

Over the past 30 years, clinical and epidemiological Identifying and selecting
research have transformed our understanding of the the literature
natural history and distribution of periodontal dis-
ease (25, 26). A model widely accepted during the Relevant articles for this review were identified by
1960s suggested that periodontitis was a slowly and a search of computerized databases using the key
continually progressive condition. Beginning as gin- words “periodontal diseases”, “epidemiology” and
givitis, it inevitably developed to affect periodontal “adults”. A manual search was conducted of
ligament, leading to loss of bone and the ultimate journals in which articles on the epidemiology of
loss of teeth. It was also accepted that periodontal periodontal disease appear: Journal of Periodonto-
disease was widespread, affected the majority of the logy; Journal of Periodontal Research; Journal of
adult population and that, ultimately, virtually every- Clinical Periodontology; Periodontology 2000;
one was susceptible to severe disease. These con- Journal of Public Health Dentistry; Community
clusions were based on studies that used invalid Dentistry and Oral Epidemiology; Gerodontics; Ger-
measures of periodontal disease and the erroneous odontology; Journal of Dental Research; Interna-
interpretation of data from cross-sectional epide- tional Dental Journal; Oral Surgery, Oral Medicine,
miological studies (26). In comparison, contempor- Oral Pathology, Oral Radiology & Endodontics;
ary approaches emphasize the episodic nature of the Journal of the American Dental Association; British
disease, in which short periods of tissue destruction Dental Journafi Journal of the Canadian Dental As-
are followed by long periods of remission and heal- sociation; Australian Dental Journal; New Zealand
ing, and that rates of progression of the disease are Dental Journal; and Scandinavian Dental Journal.
low and severe disease is far from universal. The time period for the search was 1980 to 1996.
In spite of these considerable advances, much re- Only studies with the following characteristics were
mains unknown or unclear regarding the nature of included:
periodontal disease and its extent and severity
within contemporary populations (60). Knowledge epidemiological studies of community-dwelling
concerning risk factors for periodontal destruction older adults or studies including older adults.
is also accumulating, but uncertainties remain (20). Here older adults were defined as individuals aged
These stem from the nature of the disease itself, 45 years and over. This definition was used in or-
problems in measuring its presence and severity and der to capture current and future elderly people
the difficulties involved in undertaking studies that and because some studies used the age range 45
conform to strict epidemiological criteria. to 55 years when reporting prevalence and inci-
This chapter critically reviews the current epide- dence data;
miological literature on periodontal disease. It high- studies that were population-based, where appro-
lights the essential requirements of studies designed priate, with subjects selected using random sam-
to estimate prevalence, incidence and risk and some pling methods; and
of the methodological problems involved in con- studies using clinical attachment level, attach-
ducting epidemiological research that have a bearing ment loss or bone loss as indicators of periodontal
on the quality of the evidence available to date. disease and disease progression.

16
Epidemiology of periodontal disease among older adults

Consequently, articles were selected only if they ad- prevalence and incidence and severity or extent by
equately represented the population of interest, met indexes or scales that quantify levels of disease. The
basic epidemiological criteria and measured peri- determinants of disease refer to factors that increase
odontal disease appropriately. the risk of disease onset or that identify population
subgroups most likely to have the disease under
consideration.
Measuring periodontal disease All diseases and disorders, including those affect-
ing the oral cavity and related structures, are amen-
With current technology, the best epidemiological able to study by epidemiological approaches (25).
measures of periodontal disease assess loss of The power of epidemiology as a discipline stems
attachment. Clinical attachment level represents the from the fact that the application of epidemiological
vertical distance in millimeters from the cemento- principles can lead to the control of epidemics or a
enamel junction to the point of clinical periodontal marked reduction in the frequency of a disease in
attachment. In order to fully capture the degree of a population even when the biological mechanisms
destruction of periodontal support, Carlos et al. (27) responsible for the disease are unknown or not well
proposed the Extent and Severity Index. Extent rep- understood (25).
resents the proportion of examined sites per subject
that have clinical attachment level of a given thresh-
old (usually 2 mm or more), and severity represents
the mean clinical attachment level per subject for Characteristics of epidemiological
sites with that threshold. For samples or subgroups, studies
the scores are summarized to yield a mean of the
percentage (extent) and a mean of the mean (se- Epidemiological studies of periodontal disease must
verity). follow the general principles of epidemiology. In this
Attachment loss represents the difference between regard they are distinct from clinical studies. Import-
measures of clinical attachment level at two points ant differences between the two concern the selec-
in time and indicates the degree of additional loss tion of subjects, definitions of periodontal disease
over the time period in question. Bone loss repre- and the units of analysis.
sents the vertical amount of bone lost at the mesial
or distal (or both) surface of the tooth and is ex-
Selection of study subjects
pressed in millimeters or as a percentage of total
root length. As with clinical attachment level, attach- Prevalence refers to the total number of cases of a
ment loss and bone loss can be expressed in terms disease in a population at a given point in time or
of extent and severity (62). over a given period of time. Incidence refers to the
Accordingly, studies using Russell’s Periodontal number of new cases of a disease appearing in a
Index (65), the Community Periodontal Index of population at risk over a defined period of time. In
Treatment Needs (1) or pocket probing depth meas- this context, the population at risk refers to individ-
urement were excluded from this review because of uals with a probability of acquiring the disease of
limitations in their ability to accurately and fully interest. Prevalence can be estimated using a cross-
characterize periodontal disease (8, 10, 16, 27). For sectional survey, whereas incidence requires a longi-
example, measures that rely solely on pocket depths tudinal study in which the same individuals are
substantially underestimate the prevalence of peri- examined at two points in time.
odontal disease and are also insensitive to disease One of the fundamental requirements of epide-
progression (16). miological studies designed to estimate prevalence
and incidence is that they be population-based. That
is, they study random samples drawn from general
Definition of epidemiology populations, population subgroups defined by age,
sex or race or populations at risk. In these studies,
Epidemiology can be defined as “the study of the samples must be random so that results can be gen-
distribution and determinants of disease in human eralized to the population from which the subjects
populations” (36). Distribution refers to the fre- were drawn, and sample sizes must be sufficiently
quency and severity of disease within a population large to give estimates of the required level of pre-
or its subgroups. Frequency is measured in terms of cision.

17
Locker et al.

These requirements mean that epidemiological can easily be followed over time to ensure high fol-
studies are difficult and usually costly to conduct. low-up rates.
This is particularly the case with studies of adults While representativeness is not necessary to
and older adults. The main problem here is that the identify a valid association between exposure to a
selection of a random sample requires a sampling risk factor and a disease, it should be regarded as
frame or list of each individual in the population of desirable for two reasons. First, the association be-
interest. In many jurisdictions, such lists are unavail- tween exposure and disease is more likely to be bi-
able, incomplete or inaccessible. Where population ased if subjects are not representative. Second, they
lists are unavailable, alternative approaches, such as produce “sample-based’’estimates rather than true
a preliminary household enumeration (14) or the use “population-based’’ estimates of risk. Consequently,
of telephone interview surveys based on random di- there is always some uncertainty with regard to gen-
git dialing (54, 29), are effective methods of subject eralizing to the population at large the findings of
recruitment but increase the effort and costs of a analytic studies using unrepresentative samples.
study. If random sampling methods are not used or if
participants are selected from restricted population
Case definition
subgroups, such as dental attenders, study subjects
constitute a convenience sample and inferences The fundamental principle on which epidemiology
about wider populations cannot be drawn. is based is the division of a population into groups;
Accordingly, the conduct and reporting of preva- those with the disease (cases) and those without the
lence studies requires the following: 1) definition of disease (non-cases or controls). A clear and unequi-
the target population; 2) identification of the sam- vocal definition of a case, preferably based on bio-
pling frame or approach and method of ensuring logical considerations, is required (15). However, in
random selection; 3) calculation of the response rate; most studies of periodontal disease, case definitions
4) checking that the subjects from whom data are are arbitrary (30) and inconsistent (63).
collected are representative of the target population; A case may be defined based on three types of
and 5) weighting of data if the sampling design measures of periodontal disease. The first consists of
means that subjects have different probabilities of measures of cumulative disease experience. Clinical
selection or if subjects who participate are not repre- attachment level, attachment loss and bone loss
sentative according to sex, age or any other import- measured in millimeters constitute such measures.
ant characteristic. In the absence of such infor- The second consists of measures of treatment need
mation, it is not possible to determine whether and such as the Community Periodontal Index of Treat-
to whom study results may be generalized. In ad- ment Needs and usually involve the measurement
dition, incidence studies require examination of the of periodontal pockets, which are important in the
rates of loss to follow-up and checking to ensure that clinical management of the disease (16). The third
subjects at follow-up remain representative of the consists of measures of current disease activity.
target population (64). In both types of study, assess- These use biological indicators to identify individ-
ment of the effect of nonresponse bias may be uals experiencing periodontal breakdown at one or
necessary if response rates are low or loss to follow- more sites. Clearly, these types of measures may or
up is high (53). may not coincide; an individual with significant
Identification of risk indicators and risk markers attachment loss at numerous sites may show little in
for oral diseases can be based on information col- the way of pocketing or currently active sites.
lected in cross-sectional surveys. However, the From an epidemiological point of view, one import-
identification of risk factors usually requires analytic ant difference between these types of measures con-
approaches such as case-control (retrospective) or cerns the extent to which missing teeth may influence
cohort (prospective) studies that allow temporal re- case identification. The quite substantial tooth loss
lationships to be established and causal inferences usually observed in older populations, much of which
to be drawn. Both types of study may be, but are not involves periodontally involved teeth, means that dis-
necessarily, population-based (36). Rather, subjects ease experience is based on observation of teeth that
are often selected to maximize internal validity. In a are “healthy survivors”. Consequently, lifetime dis-
case-control study, internal validity is facilitated by ease experience is likely to be underestimated (63)
choosing subjects on whom complete information and subjects misclassified in terms of case status.
on exposure to a risk factor can be obtained; in a However, tooth loss has no effect on measures of
cohort study it is facilitated by using subjects who treatment need or current disease activity.

18
Epidemiology of periodontal disease among older adults

Currently, the case definitions used in epidemio- ence and severity of periodontal disease requires the
logical studies involving clinical attachment level, summary of observations from multiple sites (16).
attachment loss or bone loss appear to be either dis- Examples of summary measures that convert site-
tributional or clinical in origin. A widely used case level observations to individual-level data are to be
definition is the presence of one or more sites with found in the Extent and Severity Index of Carlos et
clinical attachment level of 2 mm or more (59).How- al. (27) described above. Where sites are used as the
ever, in studies of older adults a higher threshold is unit of analysis, statistical methods that take account
used because such a finding is virtually universal of the fact that sites within an individual are not in-
and insensitive to subgroup differences. The ration- dependent are needed (16). Some studies fail to dis-
ale underlying the choice of these thresholds is rarely tinguish between these two levels of analysis. For ex-
described. More clinically oriented case definitions ample, the extent of disease is sometimes reported
usually involve both attachment loss and pocket as the overall proportion of sites examined with loss
depth. For example, Beck at a1 (14) defined a serious exceeding a given threshold (site-level analysis),
case of periodontal disease in older adults as follows: rather than the mean of the proportions observed in
four or more sites with clinical attachment level of 5 each subject (individual-level analysis). In the for-
mm or more with at least one of those sites having mer, failure to correct for the non-independence of
a pocket depth of 4 mm or more. Others have used sites within each subject leads to bias whose magni-
distribution based definitions and consider those in tude and direction is unknown (48).
the upper 20th percentile of the distribution of mean These methodological and analytical consider-
clinical attachment level to be a severe case (55). ations need to be borne in mind when appraising
Case definitions in studies of the incidence of the epidemiological literature on periodontal dis-
periodontal disease are even more problematic, ease.
largely because change is assessed by subtracting
baseline measurements of clinical attachment level Studies of the prevalence of
from follow-up measurements. Here, it becomes cru-
cial to distinguish between genuine clinical change
periodontal disease in older adults
and measurement error arising out of differences in
Clinical attachment level
probe angulation and probing force, inconsistent
probe positioning or reading errors. In order to ac- Thirteen reports were located that described studies
count for such error, some studies have adopted a using randomly selected samples from general popu-
threshold of 3 mm or more (or three times the stan- lations of adults or older adults that measured disease
dard deviation of differences in replicate examin- experience using clinical attachment level. Four (5-7,
ations) of change and report incidence in terms of 72) were excluded since prevalence rates were not
the proportions of subjects with this level of change given or could not be calculated from the data. The
at one or more sites (23). As these investigators rec- design characteristics and results of the remaining
ognize, this excludes individuals with less than 3 mm nine are summarized in Tables 1 and 2 (14,24,29,31,
of ‘real’change so that rates are based on only a sub- 38,40,54,58,68).Seven other articles reported the re-
set of incident cases. As with prevalence studies sults of studies using subjects who were not randomly
based on clinical attachment level, longitudinal selected or were selected from restricted groups such
studies using attachment loss corrected for error as individuals attending senior centers or regular den-
may also misclassify study subjects in terms of case tal attenders so that generalization of the findings to
status. Conversely, some studies make no allowance wider populations was somewhat problematic. These
for measurement error and may misclassify subjects studies are also summarized in Tables 1 and 2 (4, 11,
in the opposite direction. 32,34,41, 56, 59).
In general, the results of these prevalence studies
are difficult to compare due to differences in the age
Units of analysis
of the subjects included and differences in the num-
A consistently reported methodological issue that ber of teeth and sites that were probed. Some studies
arises in periodontal disease epidemiology is the used partial- as opposed to whole-mouth examin-
unit of analysis. While the unit of analysis in epi- ations and the number of sites probed varied from
demiology is the individual, epidemiological studies two to six. Partial-mouth recordings and limiting
of periodontal disease use the site as the unit of ob- probing to buccal and mesial sites can seriously
servation. Consequently, measurement of the pres- underestimate the prevalence of advanced attach-

19
Locker et al.

Table 1. Design characteristics of population-based studies of prevalence of periodontal disease


Location or Number of older Sites or
Authors source of subjects subjects by age teeth probed Definition of prevalent cases
~ ~ . ~ ~ . . _ _ _ _ _ . . --~ .,.

Hoover & Tynan (38) Saskatoon, Canada 79 aged 45 years 4 sites, 6 teeth Subjects with 2 3 mm of clinical
and over attachment
...
level at 21 site
.. ~

Beck et al. (14) Five counties in 690 aged 65 years Zsites, all teeth Subjects with 21 sites with:
North Carolina, and over a) clinical attachment level of 2 4 mm
USA b) clinical attachment level of 2 7 mm
Hunt et al. (40) Two counties, 262 aged 70 years 2 sites, all teeth Subjects with 21 sites with:
Iowa, USA and over a) clinical attachment level of 2 4 mm
b) clinical attachment level of 2 7 mm
.
. ~

Locker & Leake (54) Four communities 378 aged 50-64 2 sites, all teeth Subjects with 2 1 teeth with:
in Ontario, years, 293 aged 65 except third a) clinical attachment level of 2 4 mm
Canada years and over molars b) clinical attachment level of 2 7 mm
~
~- . . .... .-
Fox et al. (31) Six New England 554 aged 70 years 3 sites plus Subjects with 2 1 teeth with
states, USA and over “worst” site, a) clinical attachment level of 2 4 mm
all teeth b) clinical attachment
. .~
level of 2 6 mm
~~~

Slade & Spencer (68) Two cities, South 801 aged 60 years 3 sites, all teeth Subjects with 2 1 sites with:
Australia and over a) clinical attachment level of 4 mm
b) clinical attachment level of 7 mm
~ ~. ... ~ ...
Miyazaki et al. (58) Kitakyushu, Japan 423 aged 65 years 10 index teeth, Subjects with 21 sites with:
and over number of sites per a) clinical attachment level of 2 4 mm
tooth not stated b) clinical attachment level of 2 6 mm
.._ .
.. ..
Dolan et al. (29) Four counties in 761 aged 45 years All teeth; 6 sites Subjects with 2 1 sites with:
northern Florida, and over measured, a) clinical attachment level of 2 4 mm
USA greatest b) clinical attachment level of 2 7 mm
attachment loss
recorded - .... ..... _.
(ZU-....
~~ ~~

Brown et al. United States not stated 2 sites, teeth in Subjects with one site with:
population two randomly a) 2 3 mm of clinical attachment level
selected b) 2 5 mm of clinical attachment level
quadrants, third
-. . -
molars excluded
National Institute Attenders at 5689 aged 265 2 sites in Subjects with:
of Dentaf Research senior citizens’ 2 randomly a) 2 1 sites 24 mm of clinical
(59) centers, USA selected quadrants attachment level
b) 25 mm of clinical attachment level
~. ..
Ismail et al. (41) Residents of two 129 aged 47-74 2 sites, Ramfjord Subjects with:
communities in years teeth a) 21 sites 4-6 mm of clinical
New Mexico, USA attachment level
___- __._-
b) 2 7 mm of loss (check above)
McFall et al. (56) Attenders at 36 538 aged 55 years 2 sites, Ramfjord Subjects with:
dental practices and over teeth a) 21 sites 2 4 mm of clinical
in two North attachment level
Carolina counties, b) 2 6 mm of clinical attachment level
USA
~~ .
. ...___.___
.
Gilbert & Heft (32) 14 senior activity 671 aged 65 years 2 sites, all Subjects with:
centers in 6 and over remaining teeth a) 2 1 sites 2 4 mm of clinical
Florida counties, except third attachment level
____ USA molars b) 2 7 mm of clinical attachment level
Bagramian et al. Amish and non- 68 Amish and 98 6 sites, all teeth 21 sites with clinical attachment
(11, 12) Amish farming non-Amish aged except third level of 2 6 mm
families, 45 years and over molars
~~ ~-
Michigan, USA
Grossi et al. (34) Residents of Erie 538 aged 55-74 All teeth, sites not Overall mean attachment loss of
County, New York, years stated 2 4 mm
USA
~~.~ .
~

Anagnou- Farmworkers and 57 aged 55-64 4 sites, all teeth 2 1 sites with clinical attachment level
Vareltzides (4) hospital years except third of 2 6 mrn
employees, Greece molars
~ ~ ~~~~~~~~~~
__

ment loss (31, 63). Even where whole-mouth record- of periodontal disease experience. In the studies
ing was used, variation in the type and number of using the whole-mouth approach, the number of
teeth remaining can lead to differences in estimates teeth present and examined ranged from a mean of

20
Epidemiology of periodontal disease among older adults

Table 2. Prevalence, extent and severity of periodontal disease in population-based studies


Authors Definition of prevalent case" Prevalence rate Extent" Severity"
~~ ~~~~~

Hoover & TGan Clinical attachment level 2 3 mm 72% - -


(38)
_ _ _ _ _ _ _ ~ -
Beck et al. (14) Clinical attachment level 2 4 mm Blacks: 95% All: 69% All: 3 33 mm
Clinical attachment level 2 7 mm Whites: 85% Blacks: 78% Blacks: 3.98 mm
Blacks: 58% Whites: 65% Whites: 3.06 mm
Whites: 32%
_ _ _ _ _ _ _ _ ~
Hunt et al. (40) Clinical attachment level 2 4 mm Buccal sites: 65% 59% 1.74 mm
Clinical attachment level 2 7 m m Mesial sites: 56%
Buccal sites: 14%
Mesial sites: 11%
Locker & Leake Clinical attachment level 2 4 mm 88% 77% 2.44 mm
(54) Clinical attachment level 2 7 mm 25%
Fox et al. (31) Clinical attachment level 2 4 mm 95% - -
Clinical attachment level 2 6 mm 56%
Slade & Spencer Clinical attachment level 2 4 mm 79% 78% 3.09 mm
(68) Clinical attachment level 2 7 mm 28%
______
Miyazaki et al. Clinical attachment level 2 4 mm 65-74 years: 56% - -
(58) Clinical attachment level 2 6 mm 75-84 years: 69%
2 8 5 years: 50%
65-74 years: 16%
75-84 years: 22%
-
285 years: 14%
Dolan et al. (29) Clinical attachment level 2 4 mm 92% - -
Clinical attachment level 2 7 mm 35%
Brown et al. (24) Clinical attachment level 2 3 mm 55-64 years: 74% 55-64 years: 48% 55-64 years: 2.9 m m
Clinical attachment level 2 5 mm 3 6 5 years: 81% 265 years: 55% 265 years: 3.0 mm
55-64 years: 35%
2 6 5 years: 41%
National Clinical attachment level - Mean clinical
Institute of 2 4 mm 68% attachment level:
Dental Research 2 6 mm 34% Males 3.54 mm
(59) Females 2.99 mm
Ismail et al. (41) Clinical attachment level 4-6 m m 72% 7% of sites had -
Clinical attachment level 2 7 mm 34% 27.0 mm of clinical
attachment level
McFall et al. (56) Clinical attachment level 2 4 mm 60% - Mean clinical
2 6 mm 22% attachment level:
2.10 mm
Gilbert & Heft Clinical attachment level 2 4 mm 86% 88% 3.7 m m
(32) 24%
Bagramian et al. Clinical attachment level 2 4 mm Amish 87% 42% of sites in Mean clinical
(11, 12) Non-Amish 65% Amish had 2 4 mm attachment level:
clinical attachment Amish:
level; 15% 2 6 mm 45-54 1.78 mm
255 2.18 mm
Non-Amish:
45-54 0.89 mm
255 1.69 mm
Grossi et al. (34) Mean clinical attachment level 2 4 mm 25% - -
__ .- ._-
Anagnov- Clinical attachment level 2 6 mm Farmworkers % sites 2 6 mm Mean clinical
Vareltzides 68% clinical attachment attachment level:
et al. (4) Hospital level: Farmworkers 4.8 mm
employees 32% Farmworkers 26% Hospital employees
Hospital employees 4.5 mm
21%
"Subject with 2 1 sites having a clinical attachment level of the stated threshold
"As defined by Carlos et al. (271, unless otherwise stated.

9.5 (40) to a mean of 22.3 (29). The data may then Relatively few reports included an explicit case
not reflect true differences among populations in definition on which prevalence rates were based.
disease experience but differences in methods andl Where a definition was given it was usually couched
or tooth loss. in terms of the percentage of subjects with at least

21
Locker et al.

one site with attachment loss over a certain thresh- of serious periodontal disease as 4 or more sites with
old level. Although attachment loss of 2 mm or more loss of attachment of 5 mm or more with one of
is generally taken to indicate a diseased or previously those sites having a pocket of 4 mm or more, Beck
diseased site, the use of this as a threshold results in et al. (14) reported that 16% of white subjects and
prevalence rates of 95 to 100%. Consequently, 46% of black subjects in their study had this level of
thresholds of 3 mm or more, 4 mm or more or 617 disease.
mm or more of loss have been used. The reporting
of data in graphs showing cumulative frequencies
Bone loss
and/or bar charts meant that prevalence rates often
had to be estimated and in some cases data had to Relatively few studies involving non-patient popula-
be “decoded” (63) in order to obtain rates. In many tions or groups have assessed bone loss and they
studies, the extent and severity of disease as defined varied considerably in terms of measurement.
by Carlos et al. (27) were given, and these have also In a study of unreferred patients to Glasgow Den-
been included in the tables. Where possible, stat- tal Hospital, which included 74 subjects aged 50 to
istics for older adults overall are given unless only 73 years (44), 54% had advanced bone loss (defined
data specific to sites or subgroups were reported. as bone loss exceeding 50% of optimum bone
In six of the population-based studies summar- height) and 5% had generalized advanced bone loss
ized in Tables 1 and 2, prevalence rates based on a (defined as advanced bone loss in 50% or more or
clinical attachment level of 3 mm or 4 mm at one or remaining teeth). Three-quarters of the teeth with
more sites ranged from 72% to 95%. Two studies (40, advanced bone loss were located in 28% of subjects.
58) reported rates of 50% to 65% although both In a study of a random sample of Swedish adults
probed the fewest number of teeth. Using the more that included 258 aged 50 years and over, Salonen et
stringent threshold of 6 or 7 mm of clinical attach- al. (66) found that bone height as a proportion of
ment level, rates were lower and varied from 14% to total root length varied from 76% in those aged 50
58%. The extent (the mean proportion of sites with to 59 years to 65% in those aged 80 years and over.
loss of 2 mm or more) of periodontal disease varied A similar study by Hugoson et al. (39) reported that
from 48% to 78% and the severity (mean loss in sites 12% of 50-year-olds, 38% of 60-year-olds and 60% of
with loss of 2 mm or more) varied from 2.44 to 3.98 70-year-olds had bone loss around the majority of
mm. Hunt et al. (40) calculated severity as mean remaining teeth that exceeded one third of normal
attachment loss beyond 1 mm in sites having more bone height.
than 1 mm of loss. In their population of elderly Diamanti-Kipioti et al. (28) studied farmworkers
Iowans, severity was 1.74 mm. recruited through a local agricultural union and em-
Broadly comparable results were obtained by the ployees of a major hospital in an urban area. A mean
six studies in which selected groups of older adults advanced bone loss of 6 or more mm was observed
were assessed. For example, Gilbert & Heft (32) re- in 40% of the former and 10% of the latter. General-
ported prevalence rates of 86% and 24% when ized advanced bone loss was concentrated in a mi-
thresholds of 4 mm or more and 6 mm or more of nority. In the farmworker sample, 30% of subjects
loss were used and extent and severity scores of 88% accounted for 75% of the sites with advanced bone
and 3.7 mm respectively. Higher rates and a higher loss of 6 mm or more.
mean loss were reported by Anagnou-Vareltzides et
al. (4) among older Greek subjects. However, their
estimates were based on relatively small numbers of Studies of the incidence of
individuals not selected at random.
These data indicate that the majority of subjects
periodontal disease
have some experience of periodontal disease and a
Attachment loss
substantial minority have some advanced loss. How-
ever, where advanced loss occurs, it affected rela- Ten reports were located that addressed periodontal
tively few sites. For example, Ismail et al. (41) report attachment loss over time in non-patient adult
that only 7% of the sites they examined had loss of populations including older adults. The design
7 mm or more. Similarly, in a South Australian study characteristics and results are summarized in Tables
(681, only 5% of subjects aged 60 to 64 years and 10% 3 and 4.
of subjects aged 80 years and over had 20% or more Of the reports identified, four (9, 42, 67, 71) were
of sites with 7 mm or more of loss. Using a definition problematic in terms of interpretation in that it was

22
Epidemiology of periodontal disease among older adults

Table 3. Design characteristics of population-based studies of incidence


Number of
Location or older subjects Sites or Definition of
Authors source of subjects Duration according to age teeth probed incident case
.- ~~ ~

Lindhe et al. (51) City of Ushiku, 12 months Not stated 6 sites per tooth, No definition. Mean
Japan 24 months all teeth attachment level change
used as indicator of
progression
Lindhe et al. (52) City of Ushiku, 12 months Not stated 6 sites per tooth, 2 3 mm of attachment loss at
Japan 24 months all teeth 2 1 sites, that is, > 2 mm in
either examination period
Levy et al. (50) Rural Iowans, USA 2 years 197 aged 270 at Buccal and 2 2 mm of attachment loss at
baseline mesial sites 2 1 or 2 2 sites
Haffajee et al. City of Ushiku, 12 months 40 aged 50-59; 6 sites per tooth, Attachment loss of 2 3 mm at
(35) Japan 51 aged 260 all teeth 21 sites
-~ ~

Brown et al. (23) Five counties in 18 months 492 aged 265 at 2 sites for each 2 3 mm of attachment loss at
North Carolina, base1ine remaining tooth 2 1 , 2 2 or 2 3 sites
USA
Beck & Koch (19) Five counties in 36 months 492 aged 265 at 2 sites for each 2 3 mm of attachment loss at
North Carolina, baseline remaining tooth 2 1 sites
USA
~ _ _ _ _

Ismail et al. (42) City of Tecumseh, 28 years 22 subjects; 35-59 4 sites, Progression measured as
Michigan, USA at baseline Ramfjord teeth difference in mean loss from
1959 to 1987 -~
Baelum et al. (9) Langing County, 6 years 37 subjects aged 4 sites, all teeth a. Attachment loss 2 3 mm
USA 55-69 years; 15 in at one site
“best” and “worst” b. Attachment loss 2 4 mm
periodontal at one site
category at
baseline
Wennstrom et al. Patients attending 12 years 46 subjects aged 3 sites, all teeth -
(71) 12 clinics, 54-65 except third
Varmland, Sweden molars
Regular dental
visitors
Ship & Beck (67) Volunteer 10 years 17 subjects aged 2 sites, 2 2 mm of attachment loss
participants in 50-59, 40 aged Ramfjord teeth
Baltimore 60-79
Longitudinal
Stu& of Aging,
USA

unclear whether or not subjects were randomly time. For example, Levy et al. (50) reported that 35%
sampled at baseline, the study included very few of Iowans aged 70 years and over had at least one
older adults or data were not reported specifically site with 2 mm or more of attachment loss over a 2-
for subjects who were 50 years and over at baseline. year period. Brown et al. (23), using the more strin-
Of the remainder three reported data from a random gent criterion of 3 mm or more of loss at one or more
sample of Japanese adults aged 20 to 79 years at 12- sites, reported 18-month incidence rates of 58% and
and 24-month follow-ups (35, 51, 52) and three were 46% for black and white residents of North Carolina
longitudinal studies of random samples of United aged 65 years and over. Three-year incidence rates
States adults aged 65 years and over at baseline (19, were 74% for blacks and 54% for whites (19). In all
23, 50). studies, incidence rates were substantially lower
Again, problems in data abstraction, different when more demanding case definitions were used.
definitions of an incident case and differences in Broadly comparable rates were reported in the three
time periods meant that the incidence rates reported articles describing the results of the longitudinal
by these studies are not strictly comparable. Never- study conducted in Japan.
theless, they all suggest that substantial proportions Although incidence rates were high, the extent
of older adults experienced additional attachment and severity of attachment loss was low. Brown et
loss over a defined threshold of 2 mm or 3 mm in al. (23) found that only a small percentage of sites
one or more sites over relatively short periods of examined (6%for blacks and 3% for whites) showed

23
Table 4. Incidence, extent and severity in population-based studies
Authors Incidence rate Extent” Severity”
~- _________ ~ ~
~ ~~ ~~~

Lindhe et al. (51) - - a. 0.0 mm per year in subjects


aged 50-59 vears
b. 0115 mm pgr year in
subjects
__
aged 60-79 years”
~-
Lindhe et a1 (52) a 53% of those 50-59 years - -
had 2 1 sites \nth loss
>2 mm; 62% of those
60-79 years
b. 22% of those 50-59 and
40% of those 60-79
>2 mm loss at 2 2 sites _ _ _ _ _ ~
-~~~
Levy et al. (50) a. 35% had 2 1 sites with - a. 20% mean attachment loss
2 2 . 0 m m loss of 0.2 mm
b. 17% had 2 2 sites with b. 7% attachment loss of
__ - - 22.0 mm loss greater than 0.4 mm
~~ ~

Haffajee et al. (35) a. 32% of those 50-59 years


b 43% of those >GO years
.- ~ _ _ _ ~ ~ -~
Brown et a1 (23) a. 58% blacks, 46% whites 21 a. 6% of sites for blacks a. 3.54 mm for blacks
sites with 2 3 mm of loss b. 3% of sites for whites b. 3.37 mm for whites
b. 36% blacks, 27% whites (loss of 2 3 mm at 2 1 sites)
2.2sites
c. 24% blacks, 16% whites
2 3 sites
Beck et al. (19) a. 74% of blacks 21 sites with a. 11% of sites for blacks a. 4.6 mm for blacks
2 3 mm of loss b. 6% of sites for whites b. 4.3 mm for whites
b. 53% of whites . .-
(loss of 2 3 mm at 21 sites) ~~~

Ismail et al. (42) a. Increase of 1.34 mm in


overall mean loss
b. 23% with mean loss of
2 2 mm
__ - - . - .
~ ~~

Baelum et al. (9) a. 100% of “best” and “worst” 15% of sites in “best” and a. Mean attachment loss of
had loss of 2 3 mm at 24% of sites in “worst” 1.21 mm in “best” group,
2 1 sites groups loss 2 3 mm 1.36 mm in “worst” group
h 73% and 86% had loss of b. Range of mean change per
person,
2 4 mm at 2 1 sites
___+0.03 to -3.19 mm
Wennstrom et al. 39% of sites with loss of Increase in mean loss from 2.3
(71) 2 3 mm at baseline, mm to 2.6 mm
49% at follow-up
Ship PC Beck (67) % of sites losing 2 2 mm: Mean attachment loss in sites
50-59 years 28% with 2 2 mm of loss:
60-69 years 17% 50-59 years 2.40 mm
70-79 years 26% 60-69 years 2.70 mm
70-79 years 2.73 mm
--_______. -
’ PerLentdge ot sites examined with stated threshold of lo?$
” Menn loss in sites with loss or overall mean loss

evidence of attachment loss of 3 mm or more, and gival margin, or as more gingival recession with
overall mean loss beyond 3 mm over the 18-month probing depths remaining stable. Overall, 46% of
observation period was approximately 0.5 mm or subjects with loss had more than half their loss
less. At 3 years, the proportion of sites with loss in- manifesting as increased probing depth, and the re-
creased to 11% for blacks and 6% for whites (19). mainder had more than half their loss manifesting
Similarly, Lindhe et al. (51) found little overall as recession.
change in attachment loss in their sample of Ja- In two further articles, data on attachment loss
panese. trends over three years were reported. For both
In a more detailed analysis of the data from the blacks and whites, those who lost attachment during
North Carolina study, Beck & Koch (17) evaluated the first 18-month period of observation were more
subjects with at least one site with 3 mm or more of likely to experience loss during the second 18-month
loss over 18 months to determine whether their dis- period (18). However, sites that lost attachment dur-
ease progression manifested as increased probing ing the first period were no more likely to experience
depth, with no change in the position of the free gin- loss over the second than sites that remained stable
Epidemiology of periodontal disease among older adults

over the first period. These findings were consistent the two groups precludes generalization to a wider
with an episodic model of periodontal disease in population.
which people with loss are at risk of further loss but Similar problems affect the interpretation of the
sites with loss are not. The 3-year data also indicated results of the study by Wennstrom et al. (71).A total
that 41% of subjects had no loss of attachment, 28% of 225 subjects, including 46 aged 54 to 65 years,
had loss only at sites with no loss at baseline (new were randomly selected from a baseline population
lesions), 11%had loss only at sites with loss at base- recruited from among the patients attending 12
line (progressing lesions) and 20% experienced both community dental clinics in one county in Sweden.
kinds of loss (19). More subjects had new lesions In order to be selected at baseline, subjects needed
than had progressing lesions because at baseline to have at least 10 teeth and be a regular dental at-
there were many more sites with no disease than tender. Given these criteria and the fact that the pro-
with disease. Consequently, most disease occurs in cess by which subjects were initially selected is not
previously healthy sites. described, the results cannot be generalized with any
The remaining studies summarized in Tables 3 certainty.
and 4 differed considerably in approach. Ismail et Ship & Beck (67) reported on a 10-year longitudi-
al. (42) examined 165 subjects first assessed 28 years nal study of 95 subjects of whom 17 were aged 50 to
earlier, of whom 22 were aged 35 to 59 years at base- 59 years, 30 were aged 60 to 69 years and 10 were
line. This group showed an overall increase in mean aged 70 to 79 years at baseline. All were volunteer
attachment loss of 1.34 mm over this period and 23% participants in the Baltimore Longitudinal Study of
had a mean loss of 2 mm or more. Data were not Aging and as such were community-dwelling, non-
reported separately for those aged 50 to 59 at base- smoking, ambulatory white people of middle socio-
line, although it is likely that few survived to follow- economic status who visited a dentist at least once
up. This study illustrates the high attrition rates per year. Although based on a limited sample, both
(70%)that characterize studies conducted over long in terms of numbers and selection processes, this
time periods. study confirms that relatively little change in peri-
Baelum et al. (9) selected 30 individuals from a odontal status occurs over even lengthy periods of
random sample of 587 people aged 20 to 80 years time.
old in China who took part in a 1984 epidemiological
survey. They were divided into two groups of 15
Bone loss
(worst and best) according to attachment loss and
probing depths at baseline. Periodontal examin- Four reports were located that presented the results
ations in 1984 and 1990 revealed some of the highest of three studies of bone loss over time. These are
incidence rates reported: 100% of both the worst and summarized in Tables 5 and 6. In all, the nature of
best groups had one or more sites with 3 mm or the sample and its selection are unclear, although
more of attachment loss over 10 years and 73% and Lavstedt et al. (49) suggest that their unselected
86% respectively had loss of 4 mm or more in at least sample of residents of a county in Sweden were rep-
one site. However, small numbers make these esti- resentative of the population from which they were
mates unreliable, and the highly selected nature of drawn. All were studies of adults and included rela-

Table 5. Design characteristics of longitudinal population-based studies of bone loss


Number and age of older
Authors Subjects Duration subjects at baseline Radiographs Measure of bone loss
__ __ ____
__-
Albandar et al. Swedish factory 2 years 29 aged 51-60 years; 6 periapical, a. % of sites with
(2) workers, regular dental 13 aged 61-68 years 3 in each jaw 2 2 mm of bone loss
visitors, volunteers b. mean bone loss
(mm)
Albandar ( 3 ) As above 6 years 52 aged 46-57; As above As above
34 aged 2 5 8
Lavstedt et al. Unselected sample of 10 years 54 aged 51 to 60 years; Intraoral full ABD index: alveolar
(49) residents of Stockholm 17 aged 61-65 years mouth survey bone loss as a % of
County mean root length
Papapanou Not stated 10 years 43 aged 50-55 years; 6 periapical, Mean bone loss (mm)
et al. (61) 42 aged 260 years 4 bitewings
__ -

25
Locker et al.

Table 6. Incidence, extent and severity of bone loss


Authors Incidence rate Extent” Severity
Albandar et al. (2) - % of sites with 2 2 mrn of bone loss: Mean bone loss:
51-55 years 8% 51-55 years 0.32 mm
56-60 years 7% 56-60 years 0.29 mm
61-68 years 8% 61-68 years 0.34 mm
Albandar (3) - % of sites with 2 2 mm of bone loss: Mean annual bone loss:
46-57 years 5% 46-57 years 0.066 mm
258 years 4% 2 5 8 years 0.051 rnm
Lavstedt et al. (49) - Mean ABD index/rnean bone loss:
51-55 years 7%/1.1 mm
56-60 years 10%/1.6 rnrn
61-75 years 7%/1.1 rnm
Papapanou et al. (61) - - Mean bone loss:
50 years 1.5 mm
55 years 1.3 mm
60 years 1.0 mm
65 years 0.9 mm
70 years 2.8 mm
‘I Percentage of sites with stated threshold of loss.

tively few subjects aged 50 years and over at baseline show loss, the majority of sites do not; 2) advanced
and even fewer aged 60 years and over. loss was concentrated in a few individuals; 3) where
Across the four reports, age-specific estimates of loss occurred, intra- and inter-individual differences
mean annual bone loss range from 0.051 mm to 0.28 were observed; 4) where two observational periods
mm with the majority around 0.15 mm. The percen- were used a very small proportion of sites (1.2%)
tage of sites that had lost 2 mm or more of bone was showed loss in each period; 5) findings on the as-
generally low. In a study of Swedish factory workers sociation between baseline loss and further loss were
(2) it ranged from 7% to 8% according to age over inconsistent; and 6) the data tend to support a ran-
2 years. Because of the small numbers of subjects dom, episodic model of disease. However, since the
involved, all these estimates should be treated with analyses on which these conclusions were based
caution. were conducted using all subjects, it is not known
Other findings from these studies confirm those whether they apply specifically to the older adults
obtained from studies of attachment loss. They indi- included in the studies.
cate that: 1) although the majority of individuals

Table 7.Terms used in analytic epidemiological


Analytic epidemiology:
studies identification of risk factors for
Risk factor
periodontal disease
Causal correlate of disease frequency, as evidenced by:
1) exposure precedes disease (longitudinal study Analytic epidemiology is concerned with identifymg
design required); correlates of disease in human populations. Three
2) strength of association (statistically significant and
clinically important elevated risk ratio observed distinct types of correlates have been described
after controlling for other potential confounding (Table 7): risk factors, which are causal (that is, bio-
risk factors); and
3) consonance with existing biological knowledge logical or psychosocial causes of disease); risk indi-
(in vitro experimental studies) and population cators, which are thought to be causal but have not
epidemioIogy
been demonstrated to be so in studies using appro-
Risk indicator priate methods; and risk markers, which are not in-
Suspected causal correlate of disease frequency
Satisfies criterion 1 for risk factor, but insufficient for volved in causation but identify individuals or
criteria 2 and 3 groups who experience relatively high rates of dis-
Risk marker ease (13). Risk factors are often regarded as the most
Non-causal correlate of disease frequency useful types of disease correlates because of the po-
No known biological causal mechanism accounts for
disease correlation tential to reduce the incidence of disease by reduc-
ing exposure to those factors.
Epidemiology of periodontal disease among older adults

No single study can definitively identify a risk fac- A final use for all categories of disease correlates
tor. Instead it is necessary to compile evidence from (risk factors, risk indicators and risk markers) is their
several sources that collectively meet criteria for cau- combination in risk prediction models. These aim to
sation, such as those proposed by Hill (37). For epi- identify individuals most likely to experience peri-
demiological studies, three of the most important odontal disease so that they can be targeted for more
criteria are: time sequence (exposure precedes dis- intensive clinical care. Although risk prediction is an
ease); strength of association (magnitude of elevated appealing clinical concept, it is only one step in a
risk and dose-response gradient) and consonance process of improving efficiency in delivering oral
with existing knowledge (57). The latter rests on a health care (69). If an effective intervention is not
combination of biological experimental evidence available or cannot be delivered to high-risk individ-
(demonstrating cellular or subcellular mechanisms uals, risk prediction has little value other than pro-
that relate exposure to a pathological process in- viding practitioners with an improved ability to ad-
volved in the disease) and population epidemiology vise patients about prognosis. In addition, the set of
(demonstrating that the distribution of disease explanatory variables that are identified in risk pre-
within populations is found to follow the distri- diction studies usually cannot be used to make inter-
bution of the proposed causal factors) (47). pretations about causal variables (13). This is be-
For many correlates that are statistically associ- cause some of the best risk predictors are strongly
ated with disease occurrence, there have been insuf- linked to past disease activity (for example, prior
ficient studies to meet all of the criteria above and attachment loss or tooth mobility) and, in multivari-
their status as risk factors remains uncertain. For ex- ate models, their strong correlation with future dis-
ample, based on data from cross-sectional studies, ease activity tends to displace other causal variables
systemic osteoporosis is thought to be a potential from the model.
risk factor for periodontal disease (43). Where there This section considers two main questions that
are reasonable theoretical grounds and cross-sec- have been addressed in analytic epidemiological
tional epidemiological data to believe that such fac- studies of periodontal disease among current and
tors may be involved in causing disease, they should future elderly people. The studies reviewed in this
be referred to as risk indicators. Further studies are section are limited to longitudinal studies, because
then justified in order to establish their status as they provide the best evidence about risk factors.
causes of disease. However, numerous cross-sectional and case-con-
The third type of correlate is a risk marker, which trol studies have identified risk indicators and risk
is associated with disease occurrence but is not in- markers, and these have been reviewed elsewhere
volved in causing disease. For example, low socio- (15, 21, 63). These include sociodemographic and
economic status can be confirmed as a risk marker socioeconomic factors, behavioral factors, psy-
for periodontal disease based on numerous cross- chosocial factors, dental visiting patterns, general
sectional and longitudinal epidemiological studies. health status and medical conditions, prior peri-
However, there is no specific biological mechanism odontal disease experience and other oral diseases.
by which, for example, low educational attainment Factors associated with periodontal disease experi-
causes periodontal attachment loss. In part, the re- ence in cross-sectional studies do not always sur-
lationship may exist because people with low educa- vive multivariate analysis (151, nor do they necess-
tional attainment may have increases in other risk arily enter models predicting the incidence of dis-
factors (for example, periodontal pathogens, smok- ease.
ing or less use of dental services). Even though
educational attainment cannot be regarded as a risk
factor, there clearly is value in identifying it as a risk
marker, because it provides a rationale for public Aging as a risk factor for
health interventions and for pursuing other research periodontal disease
that identifies the behavior or exposures that ac-
count for this correlation. Since some studies have There is debate about the extent to which physio-
found a significant correlation between socioecon- logical and pathological changes that accompany
omic status and periodontal destruction, even after aging are due to the aging process itself or caused
controlling for these other factors (34), it may be that by concomitant pathoses, medication usage or social
these variables are documenting a general suscepti- and environmental change (46). Nevertheless, since
bility to disease. numerous age-associated changes can be observed

27
Locker et al.

in the biochemical, immunological and physiologi- of disease experience in older adults is a function of
cal processes of periodontal tissues, there are time or aging. Hence, longitudinal studies are
reasonable grounds to suspect that increasing age needed to address whether aging is a risk factor for
could potentially be a risk factor for periodontal dis- periodontal disease.
ease. A recent review of the epidemiological litera- Table 8 summarizes information from eight longi-
ture (26) concluded that age is associated with some tudinal studies reported during the last decade that
moderate loss of periodontal attachment and al- have examined potential relationships between age
veolar bone loss, but that the amount is rarely of and attachment loss or bone loss. Four studies found
therapeutic significance. The review noted that significant bivariate relationships, although for one
cross-sectional studies measuring disease experi- of them ( 3 ) ,the relationship was not linear with in-
ence necessarily show more attachment loss and creasing age. The age effect persisted in multivariate
bone loss among older age groups, since clinical analysis for two of those studies. No age associations
attachment level and bone loss are (effectively) irre- were observed in three studies in Table 8, although
versible measures of prior disease experience. the studies of Brown et al. (23) and Beck et al. (19)
Consequently, it is unclear whether the higher level were confined to people aged 265 years, whereas the

Table 8. Relationship between age and periodontal disease incidence


Authors Location Population Methods Findings
Papapanou Sweden 25-70 years; 201 people; Bivariate analysis: mean annual bone
et al. (61) source of subjects bone loss all teeth; loss=0.28 mm aged 270, 0.14 mm aged
not stated 10 years of follow-up 40-55, 0.07 mm aged 25-39 ( R 0 . 0 5 ) .
Multivariate analysis: age was implicated
(P=0.08) as risk factor after controlling for
baseline bone loss, tooth type and site
USA Random sample 165 people; Bivariate analysis: mean clinical
of community- clinical attachment level attachment level increase= 1.34 aged
dwelling people; all teeth/4 sites; 36-50, 1.23 mm aged 26-35, 1.21 mm aged
5-60 years over 28 years of follow-up 16-25, 0.8 mm aged 5-15. Multivariate
analysis: age was significant (P<0.05) risk
factor after controlling for smoking, tooth
mobility and plaque
Haffajee et al. Japan Random sample 271 people; Bivariate analysis: % of people with 2 2
(35) of community- clinical attachment level m m increase in clinical attachment level=
dwelling people; all teeth/6 sites; 43% aged r 6 0 years, 32% aged 50-59 years,
20-79 years 1 year of follow-up 31% aged 40-49 years; <20% for younger
ages (RO.01).
Multivariate analysis: age was significant
risk factor after controlling for baseline
tooth loss, pocket depth and recession
Albandar (3) Norway Employed people at 142 people; bone loss Bivariate analysis: % of people with >O
industrial plant; from 6 periapical mm increase in bone loss=4.3 aged 18-33
18-67 years radiographs / person; years, 7% aged 34-45 years, 13% aged
6 years of follow-up 46-57 years; 10% aged 57-67 years
(R0.05)
Grbic et al. USA Periodontal 75 people with =) 18 teeth Multivariate analysis: age associated with
(33) patients; '30 years and periodontal disease; 2 1 sites having 22.5 mm clinical
clinical attachment level attachment level increase, after controlling
excluding third molars; for number of teeth and baseline clinical
6 months of follow-up attachment level
Brown et al. USA Random sample 492 people; Bivariate analysis: no differences among
(23) of community- clinical attachment level 4 age groups in extent and severity of
dwelling people: all teeth/2 sites; clinical attachment level increase.
'65 years 18 months of follow-uD Multivariate analysis: no effect of age
-.
Beck & Koch USA As above 338 people Multivariate analysis: no effects of age
(19) clinical attachment level
all teeth/2 sites
3 years of follow-ur,
Ship & Beck USA Healthy men, 95 men Bivariate analysis: no differences among
(67) volunteers in aging clinical attachment level 5 age groups in % of sites losing 2 2 mm of
study; 29-76 years 6 index teeth/2 sites; clinical attachment level
8-12 vears of follow-ur,

28
Epidemiology of periodontal disease among older adults

study of Ship & Beck (67) relied on partial-mouth ated increase in risk may not be linear, since some
recordings and was confined to a selected sample of studies show no significant differences within age
healthy men. groups above the age of 65 years. A more import-
The studies in Table 8 should be considered in ant issue is the magnitude of any increase in risk:
light of other earlier studies that have shown equivo- the studies that demonstrate statistically significant
cal relationships between age and the risk of inci- associations do not necessarily indicate that this
dent periodontal disease. For example, in an earlier will lead to a serious clinical outcome for older
study of the cohort described in Table 8, Albandar et adults. For example, the 28 year follow-up study of
al. (2) found a curvilinear relationship between 2- Ismail et al. (42) reported an odds ratio of 10.4 for
year incidence of attachment loss and age, such that people aged 36-50 compared with people aged 5-
the incidence rate peaked in the age range 33-56 15 years. While this is comparable in magnitude
years. This finding is noteworthy in light of other with other clinically important risk factors (for ex-
epidemiological studies that suggest that the inci- ample, the smoking odds ratio in the same study
dence of tooth loss is highest during middle dge (61, was 14), it corresponds to a mean increase in clin-
71). Although periodontal disease is not thought to ical attachment level of only 1.34 mm over 28
be the major cause of tooth loss among adults, the years. As Burt (26) concluded, this level of in-
loss of teeth in epidemiological studies usually pro- creased risk probably is not sufficient, alone, to
duces an underestimate of periodontal disease inci- cause tooth loss, which he cites as the most clin-
dence, since attachment loss tends to be greater in ically iinportant endpoint of periodontal disease.
teeth that are extracted (whether or not the extrac- The most important clinical conclusion to draw
tion is due to periodontal disease), and such teeth from these studies concerning the effects of aging
cannot be measured in follow-up studies. is that increased age poses some increased risk for
In summary, the consistent findings from the periodontal destruction, but the amount of destruc-
studies reviewed above indicate statistically sig- tion due to age alone is probably consistent with
nificant relationships between age and incidence “successful aging” rather than accelerated patholog-
of periodontal disease. However, this age-associ- ical processes. Indeed, it is probably appropriate to

Table 9. Risk factors, risk indicators and risk markers for periodontal disease among older adults“
Authors Location Risk factors Risk indicators and markers ..
-..
Papapanou et al. Sweden Mean bone level change over 10 years Greater baseline bone loss: distal sites;
(61) maxillary sites; molars and incisors
Ismail et al. (42) USA Mean clinical attachment level Current smoker; tooth mobility
increase of 2 2 mm over 28 years
. . ~~

Haffajee et al. (35) Japan 2 1 sites with 2 3 mm clinical Greater % of s i t e F k h pocket probing depth-
attachment level increase over 1 year >3 mm; greater number of missing teeth;
greater % of sites with recession > l mm
Bolin et al. (22) Sweden Mean bone level change over 10 years Smokers >quit smokers >never smokers;
plaqueh
___.. .- __-. ~.~
Brown et al. (23) USA 2 2 sites with 2 3 mm clinical Blacks: Preuotellu intermediu >2%;
attachment level increase over 18 Porphyromonas gingivulis >2%; not flossing
months regularly; memory getting worse; dental
visit 2 3 years ago
Whites: J? gingivulis >2%: medical care in
last 6 months; felt depressed;
smoke cigarettes regularly
Beck & Koch (19) USA People with clinical attachment level No history of calcium useb; no history of
increase, mainly due to greater cervical abrasion; greater salivary flow;
pocket probing depth reported bleeding p m s : use of tobacco?
use of mouthwash
Beck et al. (18) USA 1) New clinical attachment level 1) Low income; medication use; smokeless
( 2 3 m m increase at sites with tobacco use: history of oral pain
<3 mm at baseline); 2) Low income; medication use; cigarette
2) Progressing clinical attachment level smoking: BANA positive; E! gingivalis
( 2 3 m m increase at sites positive; reported financial problems
with 2 3 mm at baseline)
a This table is confined to risk factors and risk indicators and markers, other than age, as identified in multivariate models from longitudinal studies that
included older adults (age 250 years).
Involved in interactions with other variables in the model

29
view the aging-periodontitis association as a ration- either of which would be involved in causing peri-
ale for redefining appropriate endpoints of peri- odontal disease. On the other hand, these may serve
odontal therapy, such that the objective of treatment as markers of other causal mechanisms, such as re-
is to maintain a functioning dentition rather than a ceipt of preventive dental care or reference other, as
perfect level of periodontal attachment. For ex- yet unknown, risk factors. ClearIy, additional studies
ample, Wennstrom et al. (70) have proposed age-re- are warranted to confirm the risk factor status of
lated thresholds that could be used to decide on ap- these variables and to identify others not yet in-
propriate levels of therapy. cluded in the research conducted to date.

Summary
Other risk factors, indicators and
markers for periodontal disease Although many epidemiological studies have been
conducted concerning periodontal disease, the ma-
Five of the longitudinal studies in Table 8 together jority were not included in this review because of
with two other longitudinal studies provide ad- deficiencies in the measures used. Although it is in-
ditional information about risk factors for peri- creasingly common for studies in this field to
odontal disease among older adults, and the results measure periodontal disease using clinical attach-
are summarized in Table 9. ment level, attachment loss or bone loss, the evi-
Several of the studies found that baseline indi- dence pertaining to prevalence, incidence and risk
cators of disease (greater probing pocket depth, re- in older adult populations is limited. Although it is
cession or clinical attachment level, mobility or the best indicator to date, characterizing periodontal
missing teeth) were significant predictors. As noted disease by means of attachment loss has some limi-
already, these variables can best be regarded as risk tations. Prevalence and incidence rates may vary ac-
markers, since they capture prior disease experience, cording to the number of teeth and sites probed and
rather than causal risk factors. They may be regarded bias and case misclassification may occur because
as proxies for combinations of risk factors. Moreover, of the healthy survivor effect. Moreover, prevalence
the analyses that use such variables in multivariate data that document lifetime disease experience are
models may overlook specific microbiological or be- of little use in planning for periodontal treatment
havioral risk factors. needs. Problems with sampling or subject selection
The risk factors identified in Table 9 include ciga- and idiosyncratic ways of reporting data also limit
rette smoking and periodontal pathogens, which the quality of the evidence currently available. In or-
have also been identified as risk indicators in nu- der to standardize the collection of data on loss of
merous cross-sectional studies, both among older attachment and to measure it as accurately as poss-
adults (45, 55) and other age groups (21). For ex- ible, Papapanou (63) recommends that studies use
ample, a recent meta-analysis of cross-sectional and full-mouth periodontal examinations and the assess-
case-control studies found an overall odds ratio of ment of clinical attachment level at four sites on
2.8 for periodontal disease (using various case defi- each remaining tooth.
nitions) comparing smokers with nonsmokers (63). Given the inconsistencies in and problems with
The fact that smoking has emerged as a factor in the methods used in the studies reviewed above,
many studies with different designs and approaches only broad conclusions can be drawn concerning
adds weight to the conclusion that it plays an im- periodontal disease in older adults. These confirm
portant causal role. Other behavioral factors in- the conclusions reached in other reviews of the
cluded in Table 9 relate to plaque accumulation and literature.
receipt of dental care although the totality of the evi-
dence with respect to these variables means that
their role remains uncertain.
. While moderate levels of attachment loss are to
be found in a high percentage of middle-aged and
For other predictors in Table 9, the biological elderly subjects, severe loss is confined to a mi-
pathway to link exposure with periodontal destruc- nority, albeit a substantial one. Severe loss is evi-
tion is less clear, and hence their status as risk fac- dent in only a few sites and, in general, affects
tors is uncertain. For example, worsening memory, only a small proportion of sites examined. Never-
feelings of depression and low income could influ- theless, approximately one-fifth of older individ-
ence oral hygiene behavior or may increase stress, uals have experienced more generalized severe

30
Epidemiology of periodontal disease among older adults

loss; the rate is much higher in the oldest subjects to the disease experience of current and future
and subjects from minority groups. Although not elderly people. Further, more methodologically
universal, severe disease is common in some older oriented research is required to assess the effects of
populations and some population subgroups. tooth loss and measurement protocols on estimates
Studies using common approaches are needed to of prevalence, incidence and risk.
fully elucidate the extent to which disease experi-
ence varies across different populations.
Similar conclusions can be drawn from preva-
lence studies measuring bone loss. These show
References
that a minority of subjects accounted for most
1. Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-
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