Periodontology 2000, Vol. 58, 2012, 1025 Printed in Singapore.

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2012 John Wiley & Sons A/S

PERIODONTOLOGY 2000

Global periodontal disease epidemiology

B R U C E A. D Y E

Our understanding of the global epidemiology of periodontal disease has changed considerably over the past 50 years, inuenced not only by our evolving knowledge of the natural history and distribution of the disease but by changing measurement methodologies. Although great strides have been made in describing the underlying contributions of microorganisms and plaque ecology, as well as the inammatory and host responses, there is still much that is not known regarding risk susceptibility and prevention effectiveness. The focus of global periodontal epidemiology during the last half century has been on identifying populations who have periodontal disease and on disparities in disease prevalence between groups. Unlike dental public health activities directed toward dental caries, less effort has been made in periodontal epidemiology with regard to surveying or monitoring groups who may be more at risk for moderate or severe disease and in evaluating public health initiatives aimed at mitigating risk or reducing disease prevalence. Additionally, there is limited information regarding current national estimates of periodontal disease. Although numerous periodontal studies have been performed globally, most comprise clinical research and very few are epidemiological studies using nationally representative samples. The aim of this review is to briey discuss the historical context of global periodontal disease epidemiology, highlight key activities and ndings since the last review of global periodontal epidemiology in Periodontology 2000, and comment on how changes in the practice of epidemiology may affect global periodontology.

Historical context
To adequately describe our current position with regard to understanding of global periodontal disease epidemiology and what the near future may hold, it is

useful to review some key milestones from the past. Five decades ago, the prevailing assumption was that periodontal disease was a gradually progressive disease, starting as gingivitis and ending with signicant bone loss (17). This perspective was best exemplied by the use of Russells (50) periodontal index, in which the numerical score increases as the condition worsens from gingival inammation to signicant bone loss with tooth mobility. Indeed, in one of the earliest reviews of global periodontal disease epidemiology, Russell (51) reported that one of the most universal ndings is the observation that virtually all disease seen in the eld is periodontitis that is, disease characterized by inammation in the presence of local irritating agents, with pocket formation and eventual loss of alveolar bone. Reporting on e ndings from a longitudinal study a decade later, Lo et al. (38) concluded that the periodontal lesion progresses at a relatively even pace and that the progress is continuous. Contrastingly, contemporary disease models now de-emphasize the linear progression theory of untreated gingivitis leading to periodontitis, and emphasize progression by intermittent short bursts of destructive activity followed by longer periods of inactivity. Recently, it has been suggested that the non-intermittent and burst models for disease progression may actually be more reective of the inuence of inadvertent measurement and analytical artifacts rather than the natural history of the disease (13, 30). Consequently, the continuous and intermittent models of disease progression could be less than ideal descriptions of the same disease event. When summarizing the literature for his paper on the global impact of periodontal disease (51), Russell concluded that periodontitis was widespread, and that, because many adults had gingival inammation, the risk of acquiring destructive disease was high. When Kelly and Van Kirk described the rst repre-

10

Global periodontal disease epidemiology

sentative assessments of periodontal disease in the USA from 1960 to 1962, they reported that 74% of all adults had some form of periodontal disease, with almost 49% experiencing disease without pockets and 25% having disease with pocketing. They concluded that periodontal disease was an ailment of major proportions in the USA (34). Russell (51) concluded that these ndings were invaluable as a bench mark for comparison with data from other populations and other places because the report included nationally represented data from a well-conducted study. Independent of Russells assessment of the global extent of periodontal disease, Ramfjord (49) also indicated that periodontitis was widespread when he concluded that the results from World Health Organization surveys conducted in ve Asian and African countries between 1957 and 1963 had recorded an extremely high prevalence of periodontal disease. It became widely accepted that the prevalence and severity of periodontal disease was greater in the developing world compared to higherincome areas. However, as our understanding of the relationship between plaque, gingivitis and periodontitis has changed, so has our understanding of the global extent of periodontal disease. This change was a direct result of changes in measurement methodologies. The rst major methodological change in the measurement of periodontal disease was introduction of the Community Periodontal Index of Treatment Needs (CPITN). The CPITN was developed in the late 1970s to overcome many of the recognized limitations of Russells periodontal index and Ramfjords periodontal disease index, and to facilitate performance of population-based surveys under a variety of conditions (1). The CPITN was endorsed by the World Health Organization (61), who later renamed it the Community Periodontal Index (CPI). The CPITN methodology was quickly adopted, and soon many epidemiological studies were reporting CPITN results across a number of countries. Principal ndings from these studies have been collected by the World Health Organization Oral Health Program since the 1980s, and are available online (62). The results of these CPITN studies, as well as other key studies (5, 47), showed that global differences in the prevalence and severity of periodontal disease were not as evident as previously believed. When the last global periodontal disease epidemiology review for Periodontology 2000 was performed, a number of the reviews reported on the global distribution of periodontal disease, mostly using the CPI scoring system and covering a period from the 1980s

to the early 1990s. Among European adults aged 35 44 years, the estimated proportion of people with a CPI score of 3 ranged from 13% (Ireland) to 57% (Norway) (53). Overall, the estimated mean percentage for Europe was 37% (45% for Eastern Europe and 36% for Western Europe). The estimated proportion of 3544 year old with a CPI score of 4 ranged from 3% (Malta) to 40% (Turkmenistan). It was estimated that 23% of East Europeans had a CPI score of 4, whereas the prevalence was only 9% in Western Europe. Overall, 14% of Europeans aged 3544 years had a CPI score of 4. In another review focusing on Asia and Oceania, it was reported that the number of adults aged 35 44 years with a CPI score of 3 ranged from 57% (Hong Kong) to 8% (Saudi Arabia) (19). For a CPI score of 4, the percentages ranged from 28% (Nepal) to 5% (Sri Lanka, Syria and New Zealand). Similar results were obtained in Africa: a CPI score of 3 was fairly frequent and a CPI score of 4 was more infrequent (8). The prevalence of a CPI score of 3 was reported to be >50% in studies originating from Kenya, Morocco, South Africa and Tanzania, and <5% in studies from Zimbabwe and Zaire. The prevalence of a CPI score of 4 was reported to be >30% in studies from Libya, Mauritius, Nigeria, Sierra Leone and South Africa. Reporting on the prevalence of periodontal disease in North America for comparison purposes is more challenging. First, as reported in a previous review, the number of Canadian epidemiological studies is limited (2). One study from Quebec reported that almost 21% of adults aged 3544 years had a CPI score of 4 if full-mouth probing was performed (11). However, the prevalence decreased to 19% if probing was performed around ten index teeth, as proposed by World Health Organization, and to approximately 9% if probing was restricted to two sites around each tooth. When the rst Canadian Health Measures Survey was implemented in 20062009 by Statistics Canada, periodontal assessments were performed around six index teeth (upper right rst or second molar; upper right central incisor; upper left rst or second molar; lower left rst or second molar; lower left central incisor; the lower right rst or second molar) using a standard Williams periodontal probe. Use of the CPITN CPI scoring system has never really been embraced in the USA. National surveys in the USA used Russells periodontal index from the 1960s to 1970s, and then switched to a partial-mouth periodontal assessment in which two measurements were made around each tooth in an upper and lower randomly selected quadrant (23). Consequently,

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international comparisons with US periodontal estimates are problematic. Findings from a study that used the 19881994 national survey data to estimate CPITN scores found that, among persons aged 20 59 years, almost 3% experienced a CPI score of 4, and 19% had a CPI score of 3 (24). The most recent compilation of CPITN CPI scores published by the World Health Organization shows that the mean prevalence of CPI scores of 4 in North and South America combined is 20% among adults aged 35 44 years (Fig. 1), which is the highest score across the six World Health Organization regional areas (46). Moreover, the World Health Organization estimates that 40% of similarly aged adults have a CPI score of 3 in North and South America combined. Given the comparably low prevalence of CPI scores of 3 and 4 in North America, it appears that periodontitis may affect those living in Latin and South America to a greater level compared to the rest of the world. Overall, the global prevalence of generalized, severe periodontal disease among adults during the 1980s and 1990s appeared to be low, ranging from 515% globally regardless of geographical and economical considerations (18, 40, 45). However, between the 1950s and 1970s, data from many areas of the world suggested that severe periodontal disease was more extensively distributed. The difference between these periods can be explained at least partially by the transition from collecting epidemiological data using Russells periodontal index assessment protocols to using CPITN CPI and World Health Organization methodology. However, similar to the concern that arose regarding the shortcomings of Russells periodontal index to accurately assess periodontal disease in populations,

leading to the introduction of the CPITN, concern has also arisen regarding the limitations of the CPITN for use in periodontal epidemiology (6). Subsequently, there has been a reduction in the use of CPITN CPI in epidemiological studies and a gradual increase in use of standard measurements of pocket depth and attachment loss. This has required changes in instrumentation, i.e. the type of probe used and accompanying measurement procedures. These modications have also promoted changes in the denition of periodontitis for population-based studies.

Current activities and ndings

The recent transition in global periodontal epidemiological methodology is exemplied by the design characteristics of selected international periodontal epidemiology studies detailed in Table 1. Since the mid-1990s, of the 14 population-based periodontal studies selected for this review, less than half used the CPI probe. Two studies used the UNC 15 and three used probes with 2 mm graduated markings such as the Hu-Friedy PCP-12 probe or the old NIDR probe. Not only have the probes selected changed, so have the protocols for making measurements. Two of the national studies (Australia and Vietnam) used the same protocols used in the USA for the National Health and Nutrition Examination Survey (NHANES). Finally, a number of studies have used various probing locations for measuring pocket depth and calculating attachment loss. About half of the studies used a full-mouth assessment and ve studies used a partial-mouth assessment based on six pre-specied index teeth. Probing locations varied across studies from two sites per tooth to six sites per tooth. Summary results for pocket depth and attachment loss are presented in Table 2. Among the six studies that used World Health Organization methodology for data collection, the prevalence of pocket depths >6 mm (CPI score 4) among adults aged 3544 years ranged from 21% (Germany and Quebec, Canada) to 5% or less (Hungary, China, UK and Zimbabwe). The prevalence of pocket depths between 4 and 6 mm (CPI score 3) ranged between 12% (China) to approximately 55% (Germany, the UK and Quebec, Canada). The reporting of pocket depth and attachment loss prevalence, including those studies utilizing World Health Organization methodology, provide improved opportunities for population comparisons. Among 3544 year olds, the prevalence of at least one pocket 4 mm deep ranged between 14% (China), 2324% (Zimbabwe and Australia), 27% (Hungary),

Fig. 1. Mean percentages of highest Community Periodontal Index (CPI) scores in 3544 year olds based on WHO Regional Ofces (RO). AFRO, Africa RO; AMRO, Americas RO; EMRO, Eastern Mediterranean RO; EURO, Europe RO; SEARO, Southeast Asia RO; WPRO, Western Pacic RO. Reprinted from Ref. (46) (Reprinted with permission).

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Global periodontal disease epidemiology

Table 1. Study design characteristics of selected international periodontal epidemiology studies

Country Australia Canada Reference 54 16 Year 20042006 19941995 Sample frame* National Quebec Probe NIDR CPI Examination site FM-3 FM-6 Probe location MSB, MIB, DSB MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MIL MSB, MIB, DSB, MIL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB, MSL, MIL, DSL MSB, MIB, DSB MSB, MIB MSB, MIB, DSB, MSL, MIL, DSL Protocol NHANES WHO

China

59

19951996

National

CPI

PM-6

WHO

China

60

2005

National

Hu-Friedy UNC 15 CPI

PM-6

Other

Denmark

37

20002001

National

FM-6

WHO

France Germany Germany

14 32 39

20022003 19972001 2005

National Pomerania National

Williams sensor Hu-Friedy PCP-11 CPI

FM-4 PM-4 PM-6

Other Other WHO

Hungary

31

20032004

National

CPI

PM-6

WHO

Thailand

1999

Kaun-Niang

Hu-Friedy UNC 15 CPI

FM-6

Other

UK

42

1998

National

FM-6

WHO

US Vietnam Zimbabwe

22 20 28

19992004 1999 1995

National National National

NIDR Hu-Friedy PCP-12 NIDR CPI

PM-2 FM-2 PM-6

NHANES NHANES WHO

WHO, World Health Organization; NHANES, National Health and Nutrition Examination Survey; FM, full-mouth; PM, partial-mouth; MSB, mesio-buccal; MIB, midbuccal; DSB, disto-buccal; MSL, mesio-lingual; MIL, mid-lingual; DSL, disto-lingual; CPI, Community Periodontal Index; NIDR, National Institute of Dental Research. *Cross-sectional and random representative national or regional sample. Six index teeth.

42% (Denmark), 57% (Vietnam), 59% (UK) and 7374% (Germany and Quebec, Canada). In studies reporting prevalence for similar age groups, the prevalence of pocket depths 4 mm ranged between 12% (USA), 44% (France) and 63% (Pomerania, Germany). Among younger adults, the prevalence of attachment loss 4 mm ranged from 1820% (Denmark,

China and the USA) to more than 60% (Vietnam, France and Pomerania, Germany). As expected, attachment loss prevalence universally increased with age. Among older adults, 96% of individuals living in Pomerania, Germany (ages 6081), 84% of French adults (ages 6064), 85% of adults in the UK (ages 65 and older), 81% of Australian adults (age 75 and

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14
Sample size CPI 3 CPI 4 4 mm pocket depth 23.9 23.7 26.0 52.2 12.1 18.4 3.8 22.2 19-Urban 30-Rural 39-Urban 54-Rural 81.2 35.7 62.1 20.0 6.2 41.9 82.1 44.0 51.0 56.1 56.4 62.7 82.2 81.6 78.7 7081 68.9 77.1 20.0 64.8 62.5 73.6 82.1 83.8 61.5 83.9 90.7 96.1 95.8 33.8 63.1 74.0 79.6 73.6 2.0 14.1 21.4 73.6 80.5 73.0 48.8 4 mm clinical attachment loss Age (years) Percentage distribution Periodontitis 2040 1631 224 2110 2132 2132 491 499 50 762 290 241 231 195 195 753 733 737 601 323 5059 6069 4049 3039 6064 5059 4049 3539 6574 3544 4049 4559 3544 6574 3544 3544 75+ 5574 3554 24.5 43.6 60.8

Table 2. Sample size and percentage distribution of key periodontal indicators by reported age groups for selected international periodontal epidemiology studies

Country

Reference

Australia

54

Canada (Quebec)

16

China

59

China

60

Denmark

37

France

14

Germany (Pomerania)

32

Table 2. (Continued)
Sample size CPI 3 CPI 4 4 mm pocket depth 73.0 88.0 27.4 39.0 37.0 42.3 11.6 23.5 45.0 54.0 55.0 53.0 52.0 15.0 9.0 6.0 5.0 2.0 47.0 59.0 61.0 62.0 67.0 11.9 13.2 11.4 12.1 56.5 19.0 4.0 23.0 23.9 63.9 26.0 42.0 52.0 70.0 85.0 17.8 17.8 46.6 53.8 73.6 5.0 10.7 14.3 20.1 4 mm clinical attachment loss Age (years) Percentage distribution Periodontitis

Country

Reference

Germany 904 786 743 1753 408 116 209 154 2534 3544 4554 5564 65+ 3536 2966 1942 1868 575 1195 3544 3544 75+ 6574 5064 3549 5059 3039 75+ 32.8 9.5 6574 26.2 11.0 4564 27.7 11.3 3544 21.9 5.5 6574 48.0 40.0 3544 52.0 21.0

39

Hungary

31

Thailand (Kaun-Niang)

UK

42

USA

22

Vietnam

20

Zimbabwe

28

Global periodontal disease epidemiology

CPI, Community Periodontal Index score. *Total periodontitis using the CDC AAP denition (see Table 3).

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older), 65% of Danish adults (ages 6574) and 47% of Americans (ages 6574) experienced attachment loss 4 mm. Interestingly, the relationship between attachment loss and pocket depth 4 mm deep was not consistent among younger adults across nations. For example, among Danish 3544 year olds, the prevalence of pocket depth was high compared to attachment loss (42 vs. 20%), but the inverse existed among Australians aged 3554 years with attachment loss prevalence being twice as high compared to pocket depth (49 vs. 24%). However, among 40 49 year olds in Germany, the difference in prevalence between attachment loss and pocket depth was negligible (8284%). Since the 1950s, epidemiological studies have used a variety of methods to assess inammation, oral hygiene and periodontal disease status. The key outcome for assessing periodontal disease in both Russells Periodontal Index and the CPITN was the presence or absence of periodontal pocketing. However, there has been growing concern that periodontal disease denitions should not be limited by pocket depth alone. Consequently, studies began to report periodontal disease in terms of a combination of attachment loss and pocket depth. In one report describing the prevalence of periodontal disease in the USA from 1988 to 1994, the authors dened advanced periodontitis as occurring when 30% or more teeth had a probing depth 5 mm, or 60% or more teeth had attachment loss and probing depth 4 mm, or at least one tooth had a furcation grade 2 (4). Another study used a less complex approach and dened periodontitis as the presence of one or more probing sites with both attachment loss 4 mm and probing depth 4 mm (55). Although these approaches are laudable attempts to use a more valid denition of periodontitis for dental and public health research, they also contribute to greater diversity in the disease denitions being used. This lack of uniformity in application of case denitions for periodontal disease reduces opportunities for comparisons across population-based studies and impedes epidemiological and clinical research (18, 45). Recently, efforts have been made to address these issues. A consensus report from the 5th European Workshop on Periodontology in 2005 recommended that attachment loss should be the key outcome measure when describing risk factors for periodontitis, and that attachment loss in combination with probing depths and or bleeding from probing sites should characterize periodontal disease denitions (56). The report also proposed a two-tier case denition for

disease based on the severity and extent of attachment loss. Two years later, recommendations from a work group jointly sponsored by the Centers for Disease Control and Prevention and the American Academy of Periodontology (CDC AAP) were published, emphasizing use of a combination of attachment loss and pocket depth measurements for periodontal disease denitions (44). These recommendations included standard case denitions for severe and moderate periodontitis, as well as no or mild periodontitis (Table 3). The impact of this effort on periodontal epidemiology can be seen in Table 2, which gives details for three large studies from Australia, Germany and the USA that used the CDC AAP denitions to obtain national or regional estimates of periodontitis. The estimates from Australia indicate that almost 25% adults aged 3554 years have moderate or severe periodontitis. Among 3549-year-old US adults, 5% have either moderate or severe periodontitis, whereas 34% of 3039-year-old adults living in Pomerania, Germany, have periodontitis. Although utilization of the same case denitions facilitates comparisons across periodontal epidemiology studies, differences in probing methodology present difculties in interpretation of that data. The Australian study used a full-mouth six-site examination, whereas the German and American studies used a random half-mouth four-site or two-site examination. Partial-mouth probing examinations under-estimate disease prevalence (27, 35, 36). The magnitude of under-estimation

Table 3. Centers for Disease Control and Prevention and the American Academy of Periodontology (CDC AAP) case denitions for moderate and severe periodontitis for use in population-based surveillance (44)
Severe periodontitis Two or more teeth with clinical attachment loss 6 mm at interproximal sites AND one or more teeth with pocket depth 5 mm at interproximal sites (pocket depth measurement can be on one of the teeth that meets the clinical attachment loss criteria) Two or more teeth with clinical attachment loss 4 mm at interproximal sites OR two or more teeth with pocket depth 5 mm at interproximal sites (pocket depth measurement can be on one of the teeth that meets the clinical attachment loss criteria) Neither moderate nor severe periodontitis as described above

Moderate periodontitis

No or mild periodontitis

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Global periodontal disease epidemiology

of prevalence is dependent upon the partial-mouth design used and the type of measure being assessed, which is affected by the true population prevalence. For example, sensitivity, i.e. the ability to correctly identify true prevalence, is lower when the probability of an event is rarer. Sensitivity estimates for partial-mouth examinations range between 0.41 and 0.97 for attachment loss and 0.61 and 1.00 for pocket depth (35). In contrast, the measurement error associated with estimating disease severity (either mean pocket depth or attachment loss) when using partial-mouth examinations is typically within 10% of the true population mean (36). When making direct comparisons is problematic, there is the possibility of using statistical approaches to promote indirect comparison of prevalence estimates derived from a partial-mouth examination with those obtained from a full-mouth examination. Because both the Australian and US studies used the same probing protocols (only the number of probed sites differed) and used the same CDC AAP case denition for total (moderate or severe) periodontitis (Table 3), we can enhance our comparison by use of a correction factor to adjust the US estimates. The percentage relative bias (%RB) inuencing the true prevalence (TP) estimation of total periodontitis has been calculated to be 59.81 if the number and location of probing sites used is equivalent to the NHANES two-site protocol rather than use of all six probing sites to assess prevalence (27). Using the formula: TP = CP (1)%RB), where the calculated prevalence (CP) is the estimation derived from partial-mouth assessments, we can predict what the TP

estimation would be if a full-mouth periodontal examination had been performed. As an example, Table 4 give the results for a select group of periodontal disease indicators for persons aged 3554 and 5574 years living in the USA or Australia. As the calculated prevalence for adults aged 3554 years is 5%, the estimated true prevalence is 5 (1)0.5981), i.e. 12.4%. This suggests that the prevalence of periodontitis is only twice as high in Australian adults compared to similarly aged Americans (24.5 vs. 12.4%), rather than four times as high (24.5 vs. 5%) as suggested by comparison using the unadjusted US estimates. For adults aged 5574 years, the adjusted US prevalence of periodontitis is 27.4%, compared with an unadjusted value of 1.0%. It appears that older Australian adults are also twice as likely to experience periodontitis as similarly aged Americans (43.6 vs. 27.4%). An important caveat regarding this particular comparison exercise is that the adjusted US estimates are reective of a full-mouth examination in which six sites per tooth are probed, whereas the Australian estimates were obtained from a fullmouth examination in which three sites per tooth were probed. We can also compare attachment loss prevalence between Australia and the USA by using an ination factor designed to account for under-estimation of prevalence when partial-mouth examination methodologies are used (35). For example, Kingman & Albandar calculated that the sensitivity of a NHANES two-site random mouth protocol for attachment loss 4 mm was 0.57, corresponding to an ination factor of 1 0.57, i.e. 1.75. Thus, as the prevalence of

Table 4. Percentage distribution of key periodontal indicators by reported age groups for national studies performed in Australia and the USA
Country Year Age (years) Percentage distribution 4 mm pocket depth Australia 20042006 3544 5574 USA 19992004 3554 3554 5574 5574 23.9 23.7 12.4 17.0 13.8 18.9 4 mm clinical attachment loss 48.8 73.0 16.1 28.2 33.5 58.6 Periodontitis*

24.5 43.6 5.0 12.4 11.0 27.4

*Total periodontitis using the Centers for Disease Control and Prevention and the American Academy of Periodontology (CDC AAP) denition (see Table 3). Data from the National Health and Nutrition Examination Survey (NHANES). Adjusted prevalence estimates.

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attachment loss 4 mm in the USA was 16.1% for adults aged 3554 years, the estimated true prevalence is 16.1% 1.75, i.e. 28.2%. As previously reported, the prevalence of attachment loss 4 mm among 3554 year olds in Australia is 48.8%, which is considerably higher than the adjusted estimated prevalence of 28.2% in the USA. A similar approach can be used to calculate an adjusted prevalence estimate for pocket depths 4 mm using a sensitivity of 0.73 (35).

Global trends
Using standardized assessment protocols and case denitions will facilitate cross-national comparisons, but a greater benet will be realized when international trend-analyses can be performed. A current benet of the existing CPI repository is the ability to consider changes in periodontal status. Table 5

shows information abstracted from the World Health Organization periodontal database and other sources to illustrate recent periodontal disease trends. Three of the ve countries for which data are presented in Table 5 used World Health Organization methodology. In Germany, the prevalence of periodontal pockets 4 mm deep among adults aged 3544 years increased from 46 to 73% between 1997 and 2005. An increase was also observed for older adults aged 6574 years (64 vs. 88%) during the same period. Increases occurred for CPI scores of 3 and 4 for both age groups. In Hungary, there also appears to be a trend for increasing prevalence of periodontal pockets 4 mm deep among adults aged 3544 years (18 vs. 27%). However, the trend appears to be moving in the opposite direction in the UK. Between 1988 and 1998, the prevalence of periodontal pockets 4 mm deep among adults aged 3544 years decreased from 75 to 59%. This decrease was observed for CPI scores of 3 and 4.

Table 5. Trends in key periodontal indicators (percentage) by reported age groups for selected international periodontal epidemiology studies
Country Reference Year Age (years) Percentage distribution CPI 3 CPI 4 4 mm pocket depth 36.8 23.9 32.0 40.0 52.0 48.0 16.0 21.9 62.0 60.0 54.0 52.0 14.0 24.0 21.0 40.0 2.0 5.5 13.0 17.0 5.0 15.0 46.0 64.0 73.0 88.0 18.0 27.4 75.0 77.0 59.0 67.0 22.2 22.1 11.9 11.4 25.4 54.9 17.8 46.6 9.0 24.2 5.0 14.3 4 mm clinical attachment loss Periodontitis*

Australia

15 54

19951996 20042006 1997

3544 3554 3544 6574

23.7

12.9

Germany

62

39

2005

3544 6574

Hungary

62 31

1991 20032004 1988

3544 3544 3544 6574

UK

62

42

1998

3544 65+

USA

22

19881994

3549 6574

22

19992004

3549 6574

CPI, Community Periodontal Index score. *Total periodontitis using the Centers for Disease Control and Prevention and the American Academy of Periodontology (CDC AAP) denition (see Table 3).

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Global periodontal disease epidemiology

As in the UK, the USA is showing improvements in periodontal health. Among adults aged 3549 years, the prevalence of periodontal pockets 4 mm deep decreased from 22.2 to 11.9%, and the prevalence of attachment loss 4 mm decreased from 25.4 to 17.8% between 19881994 and 19992004. The prevalence of periodontal pockets 4 mm deep and the prevalence of attachment loss 4 mm also decreased for older adults aged 6574 years during the same period. Overall, the prevalence of periodontitis decreased for older adults between 19881994 and 19992004 (24.2 vs. 14.3%). Evaluating periodontal trends for Australia is a little more challenging. Recent changes in measurement methodology limit what periodontal outcomes can be compared, but it does appear that the proportion of adults aged 3544 years with periodontal pockets 4 mm deep has decreased between 19951996 and 20042006. In a recent review of global trends in periodontitis, Hugoson & Norderyd (33) suggested that a downward trend has been emerging over the past three decades. In a previous review on global periodontal disease epidemiology for Periodontology 2000, Sheiham & Netuveli (53) suggested that periodontal health was improving in Europe. However, more recent ndings indicate a mixed picture, with periodontal health improving in the UK but possibly worsening in Germany and Hungary. In the review by Hugoson & Norderyd (33), the authors reported that the number of epidemiological studies focusing on periodontal trends in Europe was limited. Consequently, they concentrated their European review on two studies from Norway and Sweden, and reported that periodontal disease does appear to be declining, at least in the Scandinavian parts of Europe. As a result of ndings extrapolated from the World Health Organization periodontal disease database, the authors also concluded that the prevalence of periodontitis, when measured as a CPI score of 4, decreased in China, France, Hungary and Japan, remained unchanged in Germany, and increased in Syria and Zimbabwe between the 1980s and 1990s.

Risk factors
Epidemiology is the study of the distribution and determinants of diseases and health-related events in populations. Evaluating and understanding determinants of disease is central to recognizing the impact of risk factors on disease. Discussion of risk factors in the context of periodontal disease epidemiology typically focuses on two key elements identifying

groups at risk and describing the magnitude of the increased risk. In large cross-sectional studies, such as the representative surveys described in this review, the increased risk or a determinants effect on disease outcome are assessed by evaluating the magnitude of the association between those members of a subgroup with the presence of the risk factor compared to those without the factor under study and the occurrence of the event. In this context, a risk factor is more like a periodontal risk group, in that we are interested in identifying which subgroup(s) of a larger population is are more likely to experience an adverse periodontal event compared to other members of the group (3). Although there appears to be a global downward trend toward lower prevalence of periodontitis, we do not know what is inuencing this decrease. In the USA, the trend toward a lower prevalence of periodontitis is seen across all major risk group categories (22). The trend is for lower prevalence regardless of age, gender, race ethnicity, income and education status, and smoking history, with some of the largest decreases being seen in non-Hispanic blacks, lowincome adults and current smokers. Risk factors can be categorized into two broad groups: those that are modiable and those that are not. A non-modiable risk factor is a determinant of disease that cannot be inuenced or modied by intervention activities that could reduce the risk of acquiring disease. Important non-modiable risk factors for periodontal disease include age, gender, race ethnicity and other hereditary factors (29). What is particularly interesting with regard to the downward trend in periodontal disease prevalence in the USA is that the risk for periodontitis has decreased signicantly even among groups with age and race ethnicity risk indicators (12). The decreasing inuence of age in risk prediction could be related to cohort (generational) effects, and a subsequent reduction in the cumulative effects of weakening of periodontal tissues over time, and the observed changes in disease risk based on race ethnic characteristics could be partially affected by confounding as a result of changes in socio-economic status (43). As people live healthier lives and become more vigilant about oral hygiene, our understanding of the role of age, race ethnicity and other genetic risk factors will continue to evolve. Smoking is a signicant modiable risk factor for periodontal disease. It was estimated that almost 50% of all periodontal disease cases in the USA during 19881994 could be attributed to current or former cigarette use, and 75% of the cases of periodontal disease among current smokers were attrib-

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uted to smoking (55). Between 19881994 and 1999 2004, the prevalence of periodontitis decreased by more than 5% among American adults (22), but the overall smoking prevalence declined by <4% between 1995 and 2004 (58). Among adults currently smoking cigarettes, the prevalence of periodontitis decreased by more than 8% (22). Table 6 presents key risk factors for periodontal disease as reported across a number of recent epidemiological studies. Tobacco use was reported to be associated with periodontitis in China, Germany, Hungary and the USA. Of other potentially modiable social and behavioral risk factors at the population level, more studies used educational attainment rather than income or poverty status to describe the impact of socio-economic pressures on periodontal disease prevalence. Studies from Australia, China, Denmark, Germany, Hungary, the USA and Zimbabwe reported associations between education status and periodontal disease. Indeed, education may be a more important universal risk factor for periodontitis than income, given the recent ndings from China and Denmark indicating that income was not associated with periodontal disease. Utilization of dental services (specically annual dental visits) was associated with periodontitis in Australia, Canada, Denmark, Hungary and the USA. Although dental insurance coverage was associated with periodontitis in Australia, it was found not to be associated with disease prevalence in the USA. Age is often considered to be associated with periodontal disease, and is the one risk factor for periodontal disease that is generally reported by all epidemiological studies. All of the international studies in Table 6, for example, identied a signicant relationship between age and periodontal disease, regardless of the case denition used. However, the role of age as a risk indicator for periodontitis is complicated. Epidemiological studies have shown that periodontal disease, specically loss of attachment, is not a consequence of increased susceptibility or the aging process but rather a cumulative measure of previous disease activity. Increased age as a risk factor for periodontitis could also be viewed as an increased opportunity for exposure to disease. In a susceptible person, a longer duration of exposure could provide more opportunities for a genetic, microbial or environmental trigger to initiate the periodontal disease process. From a global perspective, the impact of aging on attachment loss varies. For instance, in the UK, the prevalence of attachment loss 4 mm doubles for persons age 65+ years

compared to those age 3544 years, whereas in Denmark the prevalence increases more than threefold between the two similar age groups (Table 2). However, in Germany, where the prevalence of attachment loss 4 mm is already quite high in the younger age group, the change over three decades is relatively unremarkable. Systemic risk factors for periodontitis are probably the area that has seen the greatest expansion of knowledge with regard to periodontal disease epidemiology. The earliest identied and probably most well-known systemic risk factor is diabetes mellitus. In his landmark report on Oral Health in America (57), the US Surgeon General concluded that persons with diabetes were at greater risk for periodontal disease, although the impact of periodontal therapy on glycemic control remained unclear. However, only two cross-sectional studies from Table 6 reported either an observed or a suggested association between diabetes and periodontal disease (USA and Denmark). Other potential systemic factors associated with periodontitis that have recently received much attention include adverse birth outcomes, cardiovascular diseases, hypertension, and a number of other chronic diseases characterized by underlying systemic inammation. Interestingly, the authors of the 2005 German National Oral Health Survey reported a correlation between high body mass index (overweight status) and periodontal disease. Abdominal obesity (high body mass index) is one of a number of risk indicators that characterize metabolic syndrome, which can increase a persons risk for heart disease, stroke and diabetes. As our understanding of the systemic inammatory response and genetic pathways improves, it may be that the relationship between periodontitis and many of these systemic factors will ultimately be characterized only as a sharing of common risk factors with other chronic diseases (43). Although a wealth of information has been contributed by clinical studies, global periodontal disease epidemiology could markedly benet from improved reporting by national and regional epidemiological studies with regard to the relationship between systemic risk factors and periodontitis.

Future activities
The status of global periodontitis will change as new prevalence information and surveillance tools emerge in the short-term. Estimates of periodontitis from the 2009 National Dental Health Surveys from

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Table 6. Summary of periodontal disease risk factors included in international studies

Social and behavioral factors Income
Y Y N N Y N Y Y Y N Suggested diabetes, alcohol, and smoking Y Y Y Y Y

Country Age
Y Y Y Y N N Y Y Y Y*

Reference Subject determinants Gender Race ethnicity Education Metro Smoking Oral hygiene Dental visits Dental insurance

Systemic factors

Outcome measure

Australia

54

Periodontitis CPI = 4 AL 3 mm CPI = 3 or 4

Canada (Quebec)

16

China

60

Denmark

37

France Y Y Y Y

14

Y Correlation with high body mass index (overweight status)

Mean AL CPI = 4

Germany

39

Germany (Pomerania) Y Y Y Y Y Y** Y** Y

32

Y Y**

Periodontitis CPI 3 AL 4 mm Suggested smoking, and dental visits Y Y Y Y Y Y Y Y Y Y N Diabetes, marital status CPI 3

Hungary

31

Thailand (Kaun-Niang)

UK

42

US Y Y Y N

22

Periodontitis Periodontitis CPI = 3 or 4

US

12

Zimbabwe

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Global periodontal disease epidemiology

Y indicates that the risk factor was included; N indicates that the risk factor was included but was not associated with the periodontal outcome measure. Where a cell is left blank, the risk factor was not included in the analyses. AL, adjustment loss; CPI, Community Periodontal Index score. *Race based on indigenous identity. Income assessed based on eligibility for subsidized dental care. Only unadjusted results were signicant. Race based on language spoken. Any tobacco use. **A signicant interaction between gender and dental visits or education. Ethnicity based on religious faith. Any three sites with clinical attachment loss 4 mm and any two sites with pocket depth 3 mm.

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the UK (England, Wales and Northern Ireland) and New Zealand are due to be published soon. Additionally, the rst national estimates of periodontal disease from Canada will soon be available. Canadas rst comprehensive national oral health survey was integrated into a national health study modeled on the NHANES, which will enhance opportunities for studying the impact of a plethora of risk factors on periodontitis in Canada. Likewise, South Korea has included an oral health examination in a national health study that is now known as the Korean Health and Nutrition Examination Survey (KHANES), and data are currently being collected. In the USA, the NHANES included a comprehensive periodontal assessment in adults starting in 2009, which included obtaining six probing measures for every tooth. Fullmouth information on recession, pocket depth and attachment loss from the current NHANES data collection cycle will permit calculation of appropriate ination factors to adjust for under-estimation of disease in previous years, and will permit calculation of appropriate ination factors to adjust for underestimation of disease to permit the calculation of estimates based on partial- or half-month examination designs, which will facilitate international comparisons. Comparisons of various international prevalence estimates will also improve over the next decade as more epidemiological studies report estimates using standardized case denitions and examination methods. A recent review of case denitions and methods used in periodontal epidemiology concluded that signicant diversity exists across studies of periodontal diseases, including the variety of case denitions used and the lack of consensus with regard to a classication system for disease, and a lack of uniformity with regard to which teeth are selected for examination and which instruments are used (52). Efforts toward creating and using standard denitions for moderate and severe periodontitis, such as those promoted by the CDC AAP or the European Workshop on Periodontology, are an important rst step in addressing the denition and classication problems. Preliminary work that has illustrated some benet in this area, for example using the CDC AAP denitions, has already been demonstrated in epidemiological studies from Australia, Germany (Pomerania), and the USA. One key advantage of World Health Organizations Community Periodontal Index (CPI) is standardization of the examination method. If periodontal epidemiology is to realize the full potential of using standardized case denitions, the examination

methodology should also be harmonized. Of the 14 studies identied in Table 1, seven reported using World Health Organization examination methodology and three reported using NHANES methodology, while the rest used non-dened procedures or protocols that were unique to the study. The World Health Organization method was designed for the purpose of use in surveys, focusing on six index teeth to reduce examination time and recording pocket depth to emphasize treatment needs. On the other hand, the NHANES methodology was designed for a greater range of epidemiological research. The NHANES periodontal assessment protocols have been used in an esophageal cancer study in China and an elderly health study in Puerto Rico (25, 41). Periodontal epidemiology could benet from consolidation of examination protocols for use across a broad spectrum of epidemiological studies. This would facilitate efforts to assess not only prevalence but also to evaluate risk factor relationships and to explore systemic hypotheses more comprehensively. Global periodontal disease epidemiology is at an important crossroads. Not only do our basic methods for assessing disease need to be updated to reect our current understanding of the clinical presentation and life cycle of periodontitis, but the methods need to be integrated into a translational process that can lead to improved periodontal health. Similar to the waxing and waning of active periodontitis over an individuals life, methods utilized to ascertain the distribution and patterns of periodontitis in populations have also gone through a number of evolutions. Over the past ve decades, we have seen Russells periodontal index, which was used in a number of early international nutritional and periodontal epidemiology studies, supplanted by the CPITN CPI score. Now use of the CPI score is beginning to fade as more epidemiological studies focus on measuring attachment loss. Indeed, Bourgeois et al. (14) have suggested that the golden age of the CPI score may now be over, as the quantity and quality of studies utilizing the CPI continues to diminish. However, the transition from use of the CPI score to attachment loss assessments is not without concern. Sheiham & Netuveli (53) have stated that periodontal epidemiologys emphasis on methods rather than on health is problematic because it reduces the focus of epidemiological practice on understanding determinants of disease and initiating measures that improve health. An important concept that underlies this transition is the relationship between accuracy and precision. There are many examples of concerns being raised

22

Global periodontal disease epidemiology

regarding the ability of epidemiological methods to accurately ascertain disease status, i.e. measure the true prevalence of periodontitis in study populations. On the other hand, precision is more reective to how well dened an item may be, for example, describing in detail what periodontitis is. Precision does not signify accuracy. Ramfjords introduction of the indirect measurement technique for attachment loss by use of a periodontal probe was an early attempt to address the issue of accuracy, whereas development of the CDC AAP case denitions for periodontitis was an attempt to address precision. Improving accuracy and precision in periodontal epidemiology also improves opportunities for evaluating determinants of disease, facilitates international periodontal health research activities, and enhances surveillance activities. In the USA, most health promotion and disease prevention activities are implemented at the state and local level. However, oral health surveillance activities are limited, and often under-resourced at state and local levels. The Centers for Disease Control and Prevention therefore organized a work group in collaboration with the American Academy of Periodontology in 2003 to identify population-based periodontal surveillance methods that were not exclusively dependent on resource-intense examinations and could be included in a variety of existing surveillance systems (26). The efforts of this work group have lead to development of a questionnaire to ascertain periodontal status in populations (26). These questions are included in the 20092010 NHANES, as is a full-mouth periodontal examination. If the English and Spanish language versions of the questionnaire are successfully validated on a national basis, state and local programs will be able to incorporate the periodontal questionnaire into a variety of interview formats to improve surveillance efforts and monitor the effectiveness of prevention activities. At the national level, it is envisaged that that the fullmouth periodontal examination would be performed infrequently, maybe once in a generation, to permit detailed, long-term trend analyses, and the self-reported questions would be administered much more frequently to generate national benchmark estimates. A possible adjunct to using self-reported questionnaires for future population-based surveillance activities is the use of serological markers. It has been suggested that periodontal serology could be useful for assessing periodontal status in epidemiological studies, and that serology may also be useful in investigating associations between periodontal infection and systemic health (48). It has also been

shown that differing levels of periodontal bacteria and associated antibody responses are related to periodontal and cardiovascular disease status (10), and that the antibody response to oral bacteria is more likely to be associated with coronary heart disease instead of smoking or periodontal clinical status (9). Initial work has begun to investigate the potential of combining assessments of serum IgG titers to selected periodontal bacteria with demographic and behavioral information to improve the estimation of periodontitis in epidemiological studies (21). A questionnaire and blood sampling could be easier to administer compared to a physical exam, particularly in more remote survey locations, and could be included in pre-existing surveillance systems. Nevertheless, the use of biomarkers in periodontal surveys remains a theoretical concept, and much more work is required to validate their use as surrogates for more direct measures of periodontal disease.

Summary
The periodontal status of populations globally in the rst decade of the 21st century is not known. Fewer than 10 national or regional oral health surveys have included periodontal assessments, with the majority being performed in the developed world. Among these, only ve countries reported ndings using comparable methodologies that permit assessments of general trends. Among adults under 55 years of age, pocket depth 4 mm has decreased in Australia, the UK and the USA, but has increased in Germany and Hungary. Overall, it appears that there is not enough current information to refute or support earlier estimates of severe periodontitis, which ranged from 515% of the adult global population. Methodologies for practicing periodontal epidemiology are in ux again. Large epidemiological studies are shifting away from focusing on pocket formation (CPI methodology) to assessing loss of attachment. Both smaller epidemiological studies and large national surveys are now more likely to include a combination of pocket depth and attachment loss to describe periodontitis, and these efforts are now promoting the creation and use of standardized case denitions for population-based studies. These activities and others may portend a future periodontal survey instrument that includes self-reported questions and blood sampling, and this may have important international potential for monitoring periodontal disease status in populations.

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10. Beck JD, Offenbacher S. Systemic effects of periodontitis: epidemiology of periodontal disease and cardiovascular disease. J Periodontol 2005: 76: 20892100. 11. Benigeri M, Brodeur J-M, Payette M, Charbonneau A, Ismail AI. Community periodontal index of treatment needs and prevalence of periodontal conditions. J Clin Periodontol 2000: 27: 308312. 12. Borrell LN, Burt BA, Taylor GW. Prevalence and trends in periodontitis in the USA: from NHANES III to the NHANES, 19882000. J Dent Res 2005: 84: 924930. 13. Borrell LN, Papapanou PN. Analytical epidemiology of periodontitis. J Clin Periodontol 2005: 6: 132158. 14. Bourgeois D, Bouchard P, Mattout C. Epidemiology of periodontal status in dentate adults in France, 20022003. J Periodontol Res 2007: 42: 219227. 15. Brennan DS, Spencer AJ, Slade GD. Prevalence of periodontal conditions among public-funded dental patients in Australia. Aust Dent J 2001: 46: 114121. 16. Brodeur J-M, Payette M, Benigeri M, Charbonneau A, Olivier M, Chabot D. Periodontal diseases among Quebec adults aged 3544 years. J Can Dent Assoc 2001: 67: 3438. 17. Burt BA. The role of epidemiology in the study of periodontal diseases. Periodontol 2000 1993: 2: 2633. 18. Burt BA, Eklund SA. Dentistry dental practice and the community, 6th edn. St Louis, MO: Elsevier Saunders, 2005. 19. Corbet EF, Zee K-Y, Lo ECM. Periodontal diseases in Asia and Oceania. Periodontol 2000 2002: 29: 122152. 20. Do LG, Spencer AJ, Roberts-Thomson K, Ha DH, Tran TV, Trinh HD. Periodontal disease among the middle-aged Vietnamese population. J Int Acad Periodontol 2003: 5: 77 84. 21. Dye BA, Herrera-Abreu M, Lerche-Sehm J, Vlachojannis C, Pikdoken L, Pretzl B, Schwartz A, Papapanou PN. Serum antibodies to periodontal bacteria as diagnostic markers of periodontitis. J Periodontol 2009: 80: 634647. 22. Dye BA, Tan S, Smith V, Lewis BG, Barker LK, ThorntonEvans G, Eke P, Beltran-Aguilar ED, Horowitz AM, Li CH. Trends in oral health status United States, 19881994 and 19992004. National Center for Health Statistics. Vital Health Stat 2007: 11: 248. 23. Dye BA, Thornton-Evans G. A brief history of national surveillance efforts for periodontal disease in the US. J Periodontol 2007: 78: 13731379. 24. Dye BA, Vargas CM. The use of a modied CPITN method to estimate periodontal treatment needs among adults aged 2079 years by socio-demographic characteristics in the United States, 19881994. Community Dent Health 2002: 19: 215223. 25. Dye BA, Wang R, Lashley R, Wei W, Abnet CC, Wang G, Dawsey SM, Cong W, Roth MJ, Li X, Qiao Y. Using NHANES oral health examination protocols as part of an esophageal cancer screening study conducted in a high-risk region of China. BMC Oral Health 2007: 7: 10. 26. Eke PI, Genco RJ. CDC periodontal disease surveillance project: background, objectives, and progress report. J Periodontol 2007: 78: 13661371. 27. Eke PI, Thornton-Evans GO, Wei L, Dye BA. Accuracy of NHANES partial mouth periodontal examination protocols. J Dent Res 2010: 89: 12081213. 28. Frencken JE, Sithole WD, Mwaenga R, Htoon HM, Simon E. National oral health survey Zimbabwe 1995: periodontal conditions. Int Dent J 1999: 49: 1014.

Review methodology
For this review, the types of studies eligible for inclusion had a cross-sectional study design with random selection of adult study participants who were either nationally or regionally representative of the population. The examinations had to have been performed in 1995 or thereafter, and the studies also had to include: A description of periodontal examination procedures that was sufcient to determine probe selection and use, and examination protocols utilized, and Measures of periodontal status using either CPITN CPI scores or prevalence of pocket depth and attachment loss. An electronic search using MEDLINE was performed using the following keywords in a variety of combinations: epidemiologic studies, periodontal epidemiology, epidemiology, epidemiologic surveys, periodontal diseases, periodontitis, periodontal pocket depth and attachment loss. Additional electronic sources were searched to identify government publications that were potentially relevant to this review.

References
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