Abstract
Background: The Arab World consists of 22 countries from North and North-east Africa and the Middle East. Periodontal disease is an important global oral health burden, and is highly prevalent in developing countries. Objectives: The objective of this narrative review is to report on the recorded prevalence of periodontitis in the Arab World, and to examine the methods used in collecting the data. Data and sources: A search of the literature was performed using the PubMed database up to September 2011 to identify articles that reported on the prevalence of periodontal disease in the 22 Arab countries. Reports kept in the World Health Organization (WHO) Global Health Data bank were also used in this review. Conclusion: There is a paucity of up-to-date data regarding the prevalence of periodontitis in the Arab adult population. Most relevant data are at least 10 years old. From the literature available, it is clear that there is a need for epidemiological data that are representative of the adult population from this region. Such data will enable proper development of guidelines, allocation of resources and the development of appropriate public health programmes.
Key words: Periodontal diseases, periodontitis, oral health, Arab countries, Middle East
INTRODUCTION
The Arab World comprises 22 countries from North and North-east Africa, and the Middle East. These countries are Algeria, Bahrain, Comoros, Djibouti, Egypt, Iraq, Jordan, Kuwait, Lebanon, Libya, Mauritania, Morocco, Oman, the Palestinian territories, Qatar, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, the United Arab Emirates and Yemen. The provision of dental care in most of these countries is through a combination of public and private services.
Periodontal diseases are inflammatory conditions affecting the tooth-supporting tissues. Gingivitis and periodontitis are the two most common manifestations. Periodontitis contributes extensively to the global burden of oral diseases1. It is also associated with systemic conditions such as cardiovascular diseases2 and diabetes mellitus3. The mild-to-moderate form of periodontitis is the most common, with prevalence estimates ranging from 13% to 57%, depending on the sample characteristics and the case definition used4., 5., 6.. The extent and severity of periodontitis increases with age7. The first published report on the prevalence of periodontitis from an Arab country was an Egyptian study conducted in 19478; it reported the prevalence of what was classified as ‘light’, ‘medium’ and ‘severe’ periodontitis to be 27.6%, 25.2% and 45%, respectively.
In 1981, the Fédération Dentaire Internationale (FDI) and the World Health Organization (WHO) established the first global oral health goals9. More recently, goals for the year 2020 have been established jointly by the FDI, WHO and the International Association of Dental Research (IADR)10. These goals involve reducing the impact of oral diseases on health and psychosocial development, and minimising the impact of oral manifestations of systemic diseases10. However, knowledge and understanding of the occurrence of oral diseases is a prerequisite for adequate monitoring of progress towards oral health goals, and for the proper allocation of resources.
A recent review of the burden of oral diseases in the Middle East found that little attention has been given to periodontitis in those countries11. It is therefore appropriate to examine the published data on periodontitis available from the Arab countries in order to inform the development of oral care and disease prevention strategies that are suitable for the needs of the Arab population. This narrative literature review reports on the prevalence of periodontitis in the Arab World and examines the methodological implications of the findings.
DATA SOURCES
A search of the literature was performed using the PubMed database up to September 2011 in order to identify articles that reported on the prevalence of periodontal diseases in the Arab countries. Keywords used in keyword/title/abstract searches included ‘periodontal disease’, ‘periodontitis’, ‘pocket depth’, ‘clinical attachment loss’, ‘CPITN’, ‘Arab’ and ‘Middle East’, together with the name of each of the Arab countries. Data from the WHO Global Oral Health periodontal profile Data Bank (http://www.dent.niigata-u.ac.jp/prevent/perio/contents.html) were also used in this review.
FINDINGS
The literature search for articles on the prevalence of periodontitis in adults in the Arab world revealed few studies; these were either analytical studies on the association of periodontitis with different risk factors12., 13., 14., 15., 16., 17., 18., 19., 20., 21. or assessments of the effect of the use of the miswak22., 23., or fluoride24. These (and a number of other published studies from Kuwait, Saudi Arabia, Iraq, Jordan and Yemen) included reports on the periodontal status of adult samples25., 26., 27., 28., 29., 30., 31., 32., 33., 34.. Three of the studies used pocket depth (PD) and/or clinical attachment loss (CAL) to determine periodontal status16., 23., 33.. The remainder used the Community Periodontal Index of Treatment Needs (CPITN)35 to report on periodontal status.
In 1992, periodontitis was reported as the percentage of people with one or more sextants with shallow or deep pockets [Community Periodontal Index (CPI) scores 3 and 4, respectively] in a Saudi Arabian study of the adult population from the central province of Saudi Arabia26. Just over one-quarter of those aged 19 years and over had shallow pockets, and 9.0% had deep pockets26. A 2008 report from a study of a non-representative Saudi Arabian sample reported the prevalence of shallow pockets to be 37.4%, and none had deep pockets33. The latter finding was also reported in another Saudi Arabian study of a representative sample of young adults aged 20–24 years (in Jeddah city), where none had deep pockets, while shallow pockets were observed in 7.2%25. A Kuwaiti study reported the periodontal status as the mean number of sextants with PD greater than 3 mm; this was reported to be 1.5 for those aged 20 years and over30. An Iraqi study of a representative sample of 1,418 individuals (aged 7–70 years) from three randomly selected rural villages in the province of Ninevah Governorate was conducted in 199928. In this study, shallow pockets were observed in 41.2% of those aged 25 years and over and 22.6% of the same age group had deep pockets. In the Yemeni study, deep pockets were observed in 12.5% of the 35- to 44-year age-group27. This was lower than estimates from Iraq and higher than those from Saudi Arabia. The Moroccan study used a convenience sample of two areas with differing fluoride levels24. The prevalence of shallow pockets was 32.4% and 54.6% in those aged 21–30 years and 41–60 years, respectively, and the prevalence of deep pocketing was 8.5% and 28.6%, respectively. The lowest reported occurrence of periodontitis was in Jordan31, where the prevalence of shallow pocketing was 4.7% and 18.6% in the 20–39 year age-group and 50–60 year age-group respectively; 4.1% and 11.1% of those age groups, respectively, had deep pockets. However, these comparisons should be treated with caution because, although all of the previous studies used the CPITN, the samples comprised different age groups and some studies examined all teeth while others examined index teeth only.
Few of the studies used PD and/or CAL to determine periodontal status12., 14., 16., 21., 23.. The studies are difficult to compare because they reported their data using different case definitions and thresholds. Moreover, some examined all teeth using six sites per tooth16., 21. and others conducted partial examinations14., 23.. For example, a Sudanese study examined index teeth and defined periodontitis using different thresholds of PD or CAL. They reported that approximately one in 10 participants had at least one site with 4+ mm PD, 2% had at least one site with 6+ mm PD, approximately half had at least one site with 4+ mm CAL and one in 12 had at least one site with 6+ mm CAL23. The Saudi Arabian study examined all teeth using four sites per tooth, and they reported the periodontal status as the mean probing depth per person; this was reported to be 2.8 mm for those aged 17 years and over14. The two Jordanian studies examined all teeth (except third molars), using six sites per tooth, and defined periodontitis as the presence of four or more teeth with one or more sites with PD of 4+ mm and CAL of 3+ mm12., 16.. The reported prevalence of periodontitis was 26.8% in one study16 and 30.9% in the other12.
WHO Global Oral Health periodontal profile data
Table 1 summarises the WHO data for CPI scores 3 and 4 from reports on periodontal status in the Arab countries. The reported prevalence of shallow pockets ranged from 0% to 53%, and deep pockets ranged from 0% to 34%36. Despite being collected using the CPITN, epidemiological data in the Global Oral Health Data Bank are at least comparable because they use the same method of data collection and case definitions36. The contemporary relevance of the data is questionable because most estimates are at least two decades old, and the most recent is 10 years old. Moreover, the most striking feature of this table is what is missing; that is, it does not have representative data on periodontal diseases among the adult population reported from more than half of the Arab countries.
Table 1.
Summary of the epidemiological data on the prevalence of periodontitis in adults from the Global Oral Health Data Bank representing the Arab countries*
| Percentage of people with highest score of: | Age range | Year | Country | |
|---|---|---|---|---|
| CPI 4 (PD 6+ mm) |
CPI 3 (PD 4–5 mm) |
|||
| 13 | 45 | 35–44 | 1987 | Algeria |
| 0 | 0 | 33–49 | 2000/2001 | Comoros |
| 16 | 40 | 35–44 | 1990 | Egypt |
| 11 | 37 | 35–44 | 199? | Iraq |
| 8 | 14 | 35–44 | 1994 | Lebanon |
| 34 | 53 | 35–44 | 1982/1983 | Libya |
| 16 | 49 | 31–40 | 1987 | Morocco |
| 0 | 8 | 35–44 | 1988 | Saudi Arabia |
| 12 | 9 | 35–44 | 1998 | Syria |
CPI, Community Periodontal Index: PD, pocket depth. Data accessed from the electronic site of WHO Global Oral Health periodontal profile Data Bank (http://www.dent.niigata-u.ac.jp/prevent/perio/contents.html) on 09/09/2011.
DISCUSSION
Most published surveys describing oral health status (including periodontal diseases) in the Arab world have been carried out in schoolchildren and adolescents37., 38., 39., 40., 41., 42., 43.. The present review clearly demonstrates the lack of data on periodontitis among the adult Arab population. These are important data for oral health planning, as has been suggested by the WHO report on oral health for the 21st century44. Another general finding from the studies reviewed is that periodontitis is more prevalent among older age groups. Furthermore, studies on the reasons for tooth extractions in the Arab countries show that more than one-third of missing permanent teeth have been extracted because of periodontitis; in those older than 40 years, more teeth have been lost to periodontitis than for any other reason45., 46., 47.. These facts emphasise the need for new epidemiological studies of the periodontal health of the adult Arab population.
The prevalence of periodontitis in the reported studies ranged from 0.0% to 54.6%. Data from the Global Oral Health Data Bank reported prevalence of what they defined as ‘shallow pockets’ (CPI 3) ranged from 0% to 53%, and ‘deep pockets’ (CPI 4) ranged from 0% to 34%.These wide ranges may result from a lack of standardisation of data collection and reporting. It is important that a standard and well-accepted approach is used in conducting epidemiological research on periodontal diseases. Studies should include the measurement of clinical characteristics such as periodontal destruction (including PD, CAL and radiographically determined bone loss, where possible), and the measurement of inflammation (such as bleeding on probing). While some of these factors (such as CAL and bone loss) reflect past disease, measures of PD and such as bleeding on probing are needed (and used together) to assess the presence or absence of current disease48. Some epidemiological studies have reported the prevalence of periodontitis based on measuring no more than PD, but a limitation of this is that a greater PD may result from ‘pseudo-pockets’, and not necessarily be associated with attachment loss. Thus, measurement of probing pocket depth does not provide an accurate measure of accumulated periodontal tissue destruction, and it is of limited value for the assessment of the extent and severity of periodontitis49. It is important, therefore, to combine reports of CAL, PD and bleeding on probing in epidemiological studies. Full-mouth clinical assessment of periodontitis is considered to be the gold standard in epidemiological studies50 of the condition. Susin et al.51 studied the effect of underestimation of specific partial recording protocols and found that partial recordings that use full-mouth measurements produce less bias. They concluded that the bias in the assessment of CAL is influenced by the partial recording design and the type and number of sites assessed, and by the severity of disease in the population under investigation. The effect of using different combinations on estimates of the prevalence of periodontitis is presented in Table 2, which shows that, in comparison with the gold standard, the approach leading to the greatest bias is the use of only some of the teeth and some of the sites. Furthermore, the reporting of data should be standardised, both within and among countries, in order to develop packages of oral care suitable for the needs of the Arab population. However, periodontal research does not yet have uniformly established epidemiological criteria for defining a case, with the result that different case definitions have been used in different studies52, limiting the comparability of the disease estimates. It is also important that the surveys be conducted on representative samples rather than convenience samples. Detailed descriptions of sampling procedures, the derivation and use of any sampling weights, and calibration of examiners are important in allowing an informed analysis and critique of the survey findings53.
Table 2.
Effect of different combinations of teeth and sites on prevalence estimates of periodontal disease
| Some sites | All sites | Teeth |
|---|---|---|
| Least underestimation* Most underestimation |
Gold standard Moderate underestimation |
All (except third molars) Some |
Depends on sites used (the best partial site combination is mesio-buccal, buccal and disto-lingual).
Moreover, according to current understanding of the pathogenesis of periodontitis, other factors that may play a role in the progression of periodontitis should be reported because they may be important in the occurrence of the condition. Some of these factors include tobacco use54., 55., 56. and diabetes57., 58..
RECOMMENDATIONS FOR FUTURE WORK
-
•
There is an urgent need for surveys on the prevalence, extent and severity of periodontal diseases (gingivitis and periodontitis) in the adult populations of the Arab countries. This is an important prerequisite to aid practitioners and policy makers to develop clear dental care strategies specific for this group
-
•
Standardisation of data collection and reporting will allow comparability of data from the different countries
-
•
The combined use of CAL, PD and bleeding on probing is critical in order to accurately report on periodontal status.
References
- 1.Petersen PE, Bourgeois D, Ogawa H, et al. The global burden of oral diseases and risks to oral health. Bull World Health Organ. 2005;83:661–669. [PMC free article] [PubMed] [Google Scholar]
- 2.Beck J, Garcia R, Heiss G, et al. Periodontal disease and cardiovascular disease. J Periodontol. 1996;67:1123–1137. doi: 10.1902/jop.1996.67.10s.1123. [DOI] [PubMed] [Google Scholar]
- 3.Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care. 1993;16:329–334. [PubMed] [Google Scholar]
- 4.Albandar JM, Brunelle JA, Kingman A. Destructive periodontal disease in adults 30 years of age and older in the United States, 1988–1994. J Periodontol. 1999;70:13–29. doi: 10.1902/jop.1999.70.1.13. [DOI] [PubMed] [Google Scholar]
- 5.Sheiham A, Netuveli GS. Periodontal diseases in Europe. Periodontol 2000. 2002;29:104–121. doi: 10.1034/j.1600-0757.2002.290106.x. [DOI] [PubMed] [Google Scholar]
- 6.Corbet EF, Zee KY, Lo EC. Periodontal diseases in Asia and Oceania. Periodontol 2000. 2002;29:122–152. doi: 10.1034/j.1600-0757.2002.290107.x. [DOI] [PubMed] [Google Scholar]
- 7.Beck JD, Koch GG, Rozier RG, et al. Prevalence and risk indicators for periodontal attachment loss in a population of older community-dwelling blacks and whites. J Periodontol. 1990;61:521–528. doi: 10.1902/jop.1990.61.8.521. [DOI] [PubMed] [Google Scholar]
- 8.Dawson CE. Dental defects and periodontal disease in Egypt, 1946–1947. J Dent Res. 1948;27:512–523. doi: 10.1177/00220345480270041201. [DOI] [PubMed] [Google Scholar]
- 9.Global goals for oral health in the year 2000 Federation Dentaire Internationale. Int Dent J. 1982;32:74–77. [PubMed] [Google Scholar]
- 10.Hobdell M, Petersen PE, Clarkson J, et al. Global goals for oral health 2020. Int Dent J. 2003;53:285–288. doi: 10.1111/j.1875-595x.2003.tb00761.x. [DOI] [PubMed] [Google Scholar]
- 11.Morgano SM, Doumit M, Al-Shammari KF, et al. Burden of oral disease in the Middle East: opportunities for dental public health. Int Dent J. 2010;60:197–199. doi: 10.1922/IDJ_2556Morgano03. [DOI] [PubMed] [Google Scholar]
- 12.Khader YS, Bawadi HA, Haroun TF, et al. The association between periodontal disease and obesity among adults in Jordan. J Clin Periodontol. 2009;36:18–24. doi: 10.1111/j.1600-051X.2008.01345.x. [DOI] [PubMed] [Google Scholar]
- 13.Ashril NY, Al-Sulamani A. The effect of different types of smoking habits on periodontal attachment. J Int Acad Periodontol. 2003;5:41–46. [PubMed] [Google Scholar]
- 14.Natto S, Baljoon M, Bergstrom J. Tobacco smoking and periodontal health in a Saudi Arabian population. J Periodontol. 2005;76:1919–1926. doi: 10.1902/jop.2005.76.11.1919. [DOI] [PubMed] [Google Scholar]
- 15.Al-Zahrani MS, Kayal RA. Alveolar bone loss and reported medical status among a sample of patients at a Saudi dental school. Oral Health Prev Dent. 2006;4:113–118. [PubMed] [Google Scholar]
- 16.Bawadi HA, Khader YS, Haroun TF, et al. The association between periodontal disease, physical activity and healthy diet among adults in Jordan. J Periodontal Res. 2010;46:74–81. doi: 10.1111/j.1600-0765.2010.01314.x. [DOI] [PubMed] [Google Scholar]
- 17.Ababneh KT, Al Shaar MB, Taani DQ. Depressive symptoms in relation to periodontal health in a Jordanian sample. Int J Dent Hyg. 2010;8:16–21. doi: 10.1111/j.1601-5037.2009.00373.x. [DOI] [PubMed] [Google Scholar]
- 18.El-Sayed A. Relationship between overall and abdominal obesity and periodontal disease among young adults. East Mediterr Health J. 2010;16:429–433. [PubMed] [Google Scholar]
- 19.Al-Shammari KF, Al-Ansari JM, Moussa NM, et al. Association of periodontal disease severity with diabetes duration and diabetic complications in patients with type 1 diabetes mellitus. J Int Acad Periodontol. 2006;8:109–114. [PubMed] [Google Scholar]
- 20.Mokeem SA, Molla GN, Al-Jewair TS. The prevalence and relationship between periodontal disease and pre-term low birth weight infants at King Khalid University Hospital in Riyadh, Saudi Arabia. J Contemp Dent Pract. 2004;5:40–56. [PubMed] [Google Scholar]
- 21.Khader YS, Rice JC, Lefante JJ. Factors associated with periodontal diseases in a dental teaching clinic population in northern Jordan. J Periodontol. 2003;74:1610–1617. doi: 10.1902/jop.2003.74.11.1610. [DOI] [PubMed] [Google Scholar]
- 22.Al-Khateeb TL, O’Mullane DM, Whelton H, et al. Periodontal treatment needs among Saudi Arabian adults and their relationship to the use of the Miswak. Community Dent Health. 1991;8:323–328. [PubMed] [Google Scholar]
- 23.Darout IA, Albandar JM, Skaug N. Periodontal status of adult Sudanese habitual users of miswak chewing sticks or toothbrushes. Acta Odontol Scand. 2000;58:25–30. doi: 10.1080/000163500429398. [DOI] [PubMed] [Google Scholar]
- 24.Haikel Y, Turlot JC, Cahen PM, et al. Periodontal treatment needs in populations of high- and low-fluoride areas of Morocco. J Clin Periodontol. 1989;16:596–600. doi: 10.1111/j.1600-051x.1989.tb02144.x. [DOI] [PubMed] [Google Scholar]
- 25.Farsi JM. Dental visit patterns and periodontal treatment needs among Saudi students. East Mediterr Health J. 2010;16:801–806. [PubMed] [Google Scholar]
- 26.Guile EE. Periodontal status of adults in central Saudi Arabia. Community Dent Oral Epidemiol. 1992;20:159–160. doi: 10.1111/j.1600-0528.1992.tb01554.x. [DOI] [PubMed] [Google Scholar]
- 27.Mengel R, Eigenbrodt M, Schunemann T, et al. Periodontal status of a subject sample of Yemen. J Clin Periodontol. 1996;23:437–443. doi: 10.1111/j.1600-051x.1996.tb00571.x. [DOI] [PubMed] [Google Scholar]
- 28.Khamrco TY. Assessment of periodontal disease using the CPITN index in a rural population in Ninevah, Iraq. East Mediterr Health J. 1999;5:549–555. [PubMed] [Google Scholar]
- 29.Behbehani JM, Shah NM. Oral health in Kuwait before the Gulf War. Med Princ Pract. 2002;11(Suppl 1):36–43. doi: 10.1159/000057777. [DOI] [PubMed] [Google Scholar]
- 30.Behbehani JM, Scheutz F. Oral health in Kuwait. Int Dent J. 2004;54:401–408. doi: 10.1111/j.1875-595x.2004.tb00018.x. [DOI] [PubMed] [Google Scholar]
- 31.El-Qaderi SS, Quteish Ta’ani D. Assessment of periodontal knowledge and periodontal status of an adult population in Jordan. Int J Dent Hyg. 2004;2:132–136. doi: 10.1111/j.1601-5037.2004.00080.x. [DOI] [PubMed] [Google Scholar]
- 32.Taani DS. Oral health in Jordan. Int Dent J. 2004;54:395–400. doi: 10.1111/j.1875-595x.2004.tb00017.x. [DOI] [PubMed] [Google Scholar]
- 33.Farsi N, Al Amoudi N, Farsi J, et al. Periodontal health and its relationship with salivary factors among different age groups in a Saudi population. Oral Health Prev Dent. 2008;6:147–154. [PubMed] [Google Scholar]
- 34.Beiruti N, Van Palenstein Helderman WH. Oral health in Syria. Int Dent J. 2004;54:383–388. [PubMed] [Google Scholar]
- 35.Ainamo J, Barmes D, Beagrie G, et al. Development of the World Health Organization (WHO) community periodontal index of treatment needs (CPITN) Int Dent J. 1982;32:281–291. [PubMed] [Google Scholar]
- 36.Periodontal country profile [database on the Internet]2010. Available from: http://www.who.int/oral_health/databases/niigata/en/index.html. Accessed 09 September 2011
- 37.El-Angbawi MF, Younes SA. Periodontal disease prevalence and dental needs among school children in Saudi Arabia. Community Dent Oral Epidemiol. 1982;10:98–99. doi: 10.1111/j.1600-0528.1982.tb00371.x. [DOI] [PubMed] [Google Scholar]
- 38.Hussein S, doumit M, Doughan B, et al. Oral health in Lebanon: a pilot pathfinder survey. East Mediterr Health J. 1996;2:299–303. [PubMed] [Google Scholar]
- 39.Al-Ismaily M, Al-Khussaiby A, Chestnutt IG, et al. The oral health status of Omani 12-year-olds – a national survey. Community Dent Oral Epidemiol. 1996;24:362–363. doi: 10.1111/j.1600-0528.1996.tb00877.x. [DOI] [PubMed] [Google Scholar]
- 40.Abid A. Oral health in Tunisia. Int Dent J. 2004;54:389–394. doi: 10.1111/j.1875-595x.2004.tb00016.x. [DOI] [PubMed] [Google Scholar]
- 41.El-Nadeef MA, Al Hussani E, Hassab H, et al. National survey of the oral health of 12- and 15-year-old school children in the United Arab Emirates. East Mediterr Health J. 2009;15:993–1004. [PubMed] [Google Scholar]
- 42.Elamin AM, Skaug N, Ali RW, et al. Ethnic disparities in the prevalence of periodontitis among high school students in Sudan. J Periodontol. 2010;81:891–896. doi: 10.1902/jop.2010.090709. [DOI] [PubMed] [Google Scholar]
- 43.Fanas SH, Omer SM, Jaber M, et al. The periodontal treatment needs of Libyan school children in Kufra and Tobruk. J Int Acad Periodontol. 2008;10:45–49. [PubMed] [Google Scholar]
- 44.Organization WH . WHO/ORH/Oral C21.94; Geneva: 1994. Oral health for the 21st century. [Google Scholar]
- 45.Haddad I, Haddadin K, Jebrin S, et al. Reasons for extraction of permanent teeth in Jordan. Int Dent J. 1999;49:343–346. doi: 10.1111/j.1875-595x.1999.tb00535.x. [DOI] [PubMed] [Google Scholar]
- 46.Hassan AK. Reasons for tooth extraction among patients in Sebha, Libyan Arab Jamahiriya: a pilot study. East Mediterr Health J. 2000;6:176–178. [PubMed] [Google Scholar]
- 47.Al-Shammari KF, Al-Ansari JM, Al-Melh MA, et al. Reasons for tooth extraction in Kuwait. Med Princ Pract. 2006;15:417–422. doi: 10.1159/000095486. [DOI] [PubMed] [Google Scholar]
- 48.Tonetti MS, Claffey N. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research Group C consensus report of the 5th European Workshop in Periodontology. J Clin Periodontol. 2005;32(Suppl 6):210–213. doi: 10.1111/j.1600-051X.2005.00822.x. [DOI] [PubMed] [Google Scholar]
- 49.Albandar JM, Rams TE. Global epidemiology of periodontal diseases: an overview. Periodontol 2000. 2002;29:7–10. doi: 10.1034/j.1600-0757.2002.290101.x. [DOI] [PubMed] [Google Scholar]
- 50.Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol. 1996;1:1–36. doi: 10.1902/annals.1996.1.1.1. [DOI] [PubMed] [Google Scholar]
- 51.Susin C, Kingman A, Albandar JM. Effect of partial recording protocols on estimates of prevalence of periodontal disease. J Periodontol. 2005;76:262–267. doi: 10.1902/jop.2005.76.2.262. [DOI] [PubMed] [Google Scholar]
- 52.Preshaw PM. Definitions of periodontal disease in research. J Clin Periodontol. 2009;36:1–2. doi: 10.1111/j.1600-051X.2008.01320.x. [DOI] [PubMed] [Google Scholar]
- 53.Kingman A, Albandar JM. Methodological aspects of epidemiological studies of periodontal diseases. Periodontol 2000. 2002;29:11–30. doi: 10.1034/j.1600-0757.2002.290102.x. [DOI] [PubMed] [Google Scholar]
- 54.Haber J. Smoking is a major risk factor for periodontitis. Curr Opin Periodontol 1994: 12–18. [PubMed]
- 55.Grossi SG, Zambon JJ, Ho AW, et al. Assessment of risk for periodontal disease I. Risk indicators for attachment loss. J Periodontol. 1994;65:260–267. doi: 10.1902/jop.1994.65.3.260. [DOI] [PubMed] [Google Scholar]
- 56.Schatzle M, Faddy MJ, Cullinan MP, et al. The clinical course of chronic periodontitis: V Predictive factors in periodontal disease. J Clin Periodontol. 2009;36:365–371. doi: 10.1111/j.1600-051X.2009.01391.x. [DOI] [PubMed] [Google Scholar]
- 57.Cianciola LJ, Park BH, Bruck E, et al. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes) J Am Dent Assoc. 1982;104:653–660. doi: 10.14219/jada.archive.1982.0240. [DOI] [PubMed] [Google Scholar]
- 58.Grossi SG, Skrepcinski FB, DeCaro T, et al. Response to periodontal therapy in diabetics and smokers. J Periodontol. 1996;67:1094–1102. doi: 10.1902/jop.1996.67.10s.1094. [DOI] [PubMed] [Google Scholar]
