_

Validity of self-reported periodontal disease: a systematic review and meta-analysis

Hadeel M. Abbood [footnoteRef:2] [2: PhD student, MSc Periodontics ]

Juliane Hinz[footnoteRef:3] [3: Undergraduate student in Public Health and Intern student in Epidemiology Group]

George Cherukara[footnoteRef:4] [4: Senior Lecturer and Honorary Consultant in Restorative Dentistry, PhD (Dentistry) ]

Tatiana V. Macfarlane[footnoteRef:5] [5: Honorary Reader in Epidemiology, PhD (Epidemiology)]

For correspondence please contact

Hadeel M. Abbood

E-mail: hadeel.abbood@abdn.ac.uk (can be published)

University of Aberdeen,

Dental School and Hospital

Cornhill Road, Foresterhill,

Aberdeen, UK

AB25 2ZR

The validity of self-reported periodontal disease.

We have found that self-reported periodontal disease has acceptable validity, and can be used in epidemiological studies.

Abstract

Periodontal disease is shown to be related to other systemic diseases. However in order to assess this relationship, large epidemiological studies are required. Such studies need validated self-report measures.

The aim of this systematic review was to assess the validity of self-reported measures in the diagnosis of periodontal disease.

The review followed PRISMA guidelines. Medline, Embase and Google Scholar were searched up to January 2016. Two periodontal journals were searched manually. Two reviewers independently made study selection and data extraction. All disagreements were resolved after discussion with a third reviewer. Risk of bias was evaluated using The Quality Assessment tool for Diagnostic Accuracy Studies tool. Sensitivity, specificity, diagnostic odds ratio and 95% confidence interval were calculated.

Out of 933 papers found, 11 were selected for the review. All the studies, except two, had acceptable quality. Study size ranged from 114 to 1426 participants. Four comparable studies were selected for meta-analysis. Sensitivity and specificity ranged from 4% to 93% and 58% to 94%, respectively. Diagnostic odds ratio was 1.4 (95% confidence interval 0.9 - 2.2) for question on bleeding gums and 11.7 (95% confidence interval 4.1 - 33.4) for question on tooth mobility. Heterogeneity was low for most of the questions except questions on painful gums and tooth mobility.

Self-reported periodontal disease has acceptable validity and can be used for surveillance of periodontal disease in large epidemiological studies. However, there is a need for large well-designed diagnostic studies.

Keywords: Self Report; Self-Assessment; Periodontitis; Gingival Disease; Epidemiology; Diagnosis.

1

Introduction

There is a growing evidence that periodontal disease (PdD) is associated with several systemic diseases.1 It has been shown that there is a bidirectional association between PdD and diabetes mellitus.2 Other studies suggested that there is an association between PdD and cardiovascular disease, rheumatic disease, adverse events during pregnancy, respiratory diseases in elderly people and Alzheimer.3-8

Epidemiological studies are important for estimating prevalence of disease, studying the aetiology and association between different conditions and diseases. They are important for developing prevention and control strategies.9 PdD surveillance in epidemiological studies requires large-scale samples with full-mouth examination, Which is costly and time-consuming.10,11 This raised the importance of using self-reported questions in surveillance of PdD.

Self-reported questions are less demanding on cost and time.12,13 Additionally, they can be added to ongoing studies, in order to evaluate association between PdD and other diseases and conditions.

Studies showed that self-reported questions had good validity when compared to medical records for diabetes mellitus, hypertension and myocardial infarction.14,15 But low validity for other conditions, such as cerebral ischemia and skin diseases.16

The validity of self-reported questions regarding oral health is high for tooth count and presence of removable dentures.17,18 Studies that investigated the validity of self-reported PdD have variable results.19,20

The aim of this systematic review is to assess the validity of self-reported PdD.

Method

Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines were followed to design this systematic review.21 This systematic review has been registered in PROSPERO[footnoteRef:6]22 and SRDR[footnoteRef:7].23 [6: The International Prospective Register of Systematic Reviews (Registration number: CRD42015025139).] [7: Systematic Review Data Repository.]

The following criteria were used in selecting studies:

Types of studies: Observational studies of all design-types were included in this review. There was evidence that case-control design exaggerated diagnostic accuracy. In case-control study, the selection of cases with advanced disease is likely to lead to overestimation of sensitivity. On the other hand, selection of healthy controls is likely to lead to overestimation of specificity.24-26 This effect can be assessed by using appropriate quality assessment tool. Therefore, no exclusion has been made according to study design.

Types of participants: Participants had to be randomly selected. They should be blinded to the results of the clinical examination.

Inclusion and exclusion criteria: There were no restriction on publication types. Only studies in English language were included. Included studies were required to evaluate questionnaire by comparing responses to a clinical gold standard. The clinical gold standard can be defined as the best acceptable test for diagnosis.27 The clinical gold standard for PdD diagnosis is periodontal examination. Studies that did not validate self-report questionnaire or validate them overall were excluded.

Periodontal disease definition: The Centres for Disease Control and Prevention and the American Academy of Periodontology (CDC-AAP) classified the severity of periodontitis into mild, moderate and severe.28 Moderate disease is defined as 2 interproximal sites (not on same tooth) with clinical attachment loss (AL) 4 mm or 2 interproximal sites (not on same tooth) with probing depth (PD) 5 mm. Severe periodontitis is defined as 2 interproximal sites (not on same tooth) with AL 6 mm and 1 interproximal sites with PD 5 mm.28 The definition of mild periodontitis was updated in 2012 to be defined as 2 interproximal sites with AL 3 mm and 2 interproximal sites with PD 4 mm (not on the same tooth) or one site with PD 5 mm.29

Other studies used Community Periodontal Index (CPI).30 The extent of loss of attachment is recorded using CPI probe and measured in millimetres. Additionally, bleeding on probing and presence or absence of calculus should be recorded. The following codes are applied: 0 = healthy gingiva with normal PD; 1 = mild gingival inflammation with bleeding on probing, but normal PD; 2 = moderate inflammation of the gingiva, bleeding on probing and calculus present, with normal PD; 3 = 4-5mm PD and 4 = 6mm or more PD.30

Search strategy:

MEDLINE search strategy was adapted from the review by Blicher et al.31 The search was updated to include studies from 2005 to January 2016. Embase and Google Scholar databases were added to the electronic search.

The search strategy terms were grouped into three categories. Group 1 terms were related to PdD (gingivitis, gingival, gingival disease, periodontal, periodontal disease, periodontitis, tooth mobility, loss of attachment, bleeding gums); group 2 included terms associated with self-reporting (questionnaire, self-assessment, self-report, self-reported), and group 3 consisted of terms concerning validation (comparison, compared, validity, validation). Intra-group terms were combined with the Boolean commands OR, and inter-group terms were combined with AND. Additionally, two journals (Journal of Clinical Periodontology and Periodontology 2000) were searched manually from 2005 to January 2016. The titles of the contents were screened on the web-archive of each journal. Additionally, the reference list of the selected studies were screened for any new title.

Data extraction:

After completing the database search and manual search, two independent reviewers (HA and JH) screened the title and the abstract of each study following the inclusion criteria. When disagreements occurred between them, a third reviewer (TM) was consulted. Data extraction was done by two independent reviewers (HA and JH). Extracted information included: study type, population description (sample size, mean age, gender, method of recruitment), questions used for self-report, clinical gold standard, and time of data collection. A special data extraction form was designed in SRDR website.23 The data extracted were used to construct 2 by 2 tables to calculate sensitivity and specificity. If the necessary information was missing, the authors were contacted.

Good validity level was defined according to the validity classification introduced by Nelson et al.15 based on sensitivity and specificity values. They classified validity into three levels, low, moderate and high when sensitivity and specificity were < 60%, 60-79% and 80%, respectively. Nelson et al. used a qualitative process to produce this validity classification, taking into consideration number of studies in their review, consistency of findings, sample selection and strength of the statistical measures.15

Quality assessment:

QUADAS-2[footnoteRef:8],32 was used to evaluate the risk of bias and applicability of primary diagnostic accuracy for each study. The tool consists of four key domains regarding patient selection, index test, reference standard and flow and timing. Critical appraisal of the previous systematic review31 was conducted using AMSTAR[footnoteRef:9].33 [8: The QUality Assessment tool for Diagnostic Accuracy Studies.] [9: Quality assessment tool for assessing the methodological quality of systematic review.]

Statistical analysis:

Sensitivity, specificity and Diagnostic Odds Ratio (DOR) were calculated. DOR of a test is the ratio of the odds of positivity in patients with disease relative to the odds of positivity in the healthy.34,35 When the value is equal to one, this means that a test is not able to distinguish between patients with disease and healthy people. Values >1 indicate that a test has acceptable performance and can distinguish patients with a disease from healthy people. Values 0.5).

The question regarding painful gums Have you ever had painful gums?42,43 has a PDOR of 2.07 (95% CI 0.72 - 5.96) when using moderate periodontitis as a gold standard. I2 value was 70.9% (p = 0.064). Nearly the same results were obtained when using severe periodontitis as a gold standard (PDOR 1.71 (95% CI 0.22 - 13.57), I2 = 82.8%, p = 0.016).

Two studies43,45 used a question about tooth migration Have you ever noticed that your front teeth have moved forward (towards the lip) or that gaps have developed between your front teeth? and used severe periodontitis as gold standard. PDOR was 2.14 (95% CI 1.17- 3.91), I2 was 0.0% (p = 0.348).

The results of the quality assessment of the included studies are presented in Table 3. Four studies did not mention whether the participants were blinded to their clinical diagnosis when they filled the questionnaires.45,47-49 In contrast, six studies did not mention if the clinical examiners were blinded to the participants answers during periodontal examination.40-42,45,48,49 Moreover, five studies did not mention the length of the interval between filling the questionnaires and periodontal examination.40,42,45,47,49 The period between answering the questionnaire and the clinical examination should be as short as possible, as gingival bleeding can develop in 14 days and could be resolved within a week.50

On the other hand, all the selected studies had good quality in selection of the population and providing a pre-specified threshold depending on CDC-AAP or CPI.

Quality assessment of the systematic review by Blicher et al.31 (Table 4) showed that, the review was appropriately designed; the review aim was clear, had appropriate selection criteria, inclusion and exclusion criteria and comprehensive literature search were done. It was not clear whether literature was searched regardless of publication type (i.e. in-press literature, conference abstracts or other types of grey literature which is any publication that is not controlled by commercial publishers51).

However, there was no quality assessment of the listed studies included in the review. The review included 16 studies with sample size ranging from 63 to 1333 participants. The validity of the selected studies was considered good when the summation of the sensitivity and specificity 120%. This value was arbitrary chosen by the authors31.

Discussion

Whilst a valid self-reported instrument is a useful alternative to clinical examination. There are several challenges, such as patients awareness of their oral health, access to dental care, age, prevalence and severity of PdD.1,52

Generally, self-reported PdD has acceptable validity when compared to clinical gold standards. Self-reported PdD concerning painful gums, tooth mobility and peoples opinions whether they have gums disease, can be classified as having moderate to high validity based on Nelsons validity classification.15

The question regarding patients awareness of gums disease had a moderate validity in two studies,43,45 when using severe and moderate periodontitis as a gold standard. Another study used the same question,41 but the sensitivity was low with high specificity. This study had mentioned some limitations, one of them is the use of four sites instead of six sites per tooth to determine the clinical periodontal status and subsequent use of three of these sites for the final report. This may have underestimated the periodontal status of the participants. Blicher et al.31 stated that this question had a good validity, which is similar to our results. The question regarding patients awareness of gums disease had a good validity and can be representative of the patients periodontal status.

Questions regarding tooth mobility and tooth migration had high specificity with high PDOR,42,43,45 but with different values of sensitivity. Similar findings were reported by Blicher et al.31 with high sensitivity. These questions seems to have greater validity in predicting severe periodontitis, because they represent clinical symptoms that can be easily identified by individual.45

Question on bleeding gums had low sensitivity with high specificity in both studies that used this question.41,42 These findings were similar to the findings in the previous review31, which stated that self-reported gingivitis had a poor validity. There are several explanations for such low validity. First, self-reported bleeding gums used CDC-AAP classification of PdD as a gold standard, and periodontitis is not usually associated with bleeding gums, especially if the periodontitis is chronic, or if the patient is undergoing treatment for it. Bleeding on brushing is usually related to marginal gingivitis.53 Secondly, bleeding is masked in smokers regardless of the severity of periodontitis. Therefore, smoking should be taken into consideration when using this question.54-56 There may be sites that exhibit bleeding on probing but without attachment loss, that will increase the value of false positive and thereby decrease the sensitivity value. Conversely, bleeding on probing is usually associated with a high degree of specificity, in that its absence is a good predictor of periodontal health. In other words, sites that consistently do not bleed are not likely to exhibit loss of attachment and have a significantly low risk for periodontitis.57-63 Epidemiological studies need a test with high sensitivity as well as specificity. However, there are some tests that can be used in epidemiological studies even with low sensitivity but high specificity, like in question on bleeding gums. This test will identify correctly the healthy subjects.

Two studies used a question about bone loss.43,45 This type of question had a high specificity with low sensitivity. It conflicted with the previous findings by Blicher et al.,31 who stated that it was the best measure found. It could be possible that patients may not have been told about bone loss that may affect their answer to the question.

Generally, the validity of self-reported PdD is acceptable to identify the presence of periodontitis. The sensitivity values of most of the questions were lower than the specificity values. This would suggest that a proportion of patients with PdD may not be recognised by these questions. It could be due to the fact that patients have either not been advised of their disease by their dentist, or do not recall well having been advised. The high specificity suggested that these questions can identify those who do not have PdD correctly.40 There was no significant statistical difference between studies for all the questions except for questions on painful gums and tooth mobility. However, as the number of studies is small. The detection of heterogeneity maybe inaccurate due to low power.

There were no sufficient information in the selected studies to investigate the effect of age on the validity of self-reported PdD. Cyrino et al.45 mentioned that the sensitivity and specificity of self-reported PdD was higher in old age group than younger age. That could be due to the increased severity of PdD which may make the signs and symptoms easily observed by participants.45 Additionally, access to dental care could be a factor that may affect the validity of self-reported PdD. As that may affect the individuals awareness of PdD.

Using several self-reported measures in combination may prove to be a good alternative, as using one measure has not consistently proved to be valid for use in general population.31 Therefore, a need for large well-designed diagnostic study evaluating validity of self-reported PdD.

Conclusion

From the results above, self-reported PdD is efficient tool for surveillance of PdD in large epidemiological studies. Self-evaluating painful gums; tooth mobility and peoples awareness of PdD are the most efficient type of questions that can be used to identify PdD. Question on bleeding gums still needs more detailed and large study to identify its validity, taking into account sociodemographic factors including access to dental care.

Acknowledgments

H.A. received funding from the Higher Committee for Education Development in Iraq (HCED-Iraq) (Baghdad, Iraq) to undertake her PhD. J.H. worked on the project while taking part in an Erasmus student placement under the European Lifelong Learning Programme. Authors declare no conflict of interest.

References:

1. Eke PI. Public health implications of periodontal infections in adults: Conference proceedings. J Public Health Dent 2005;65:56-65.

2. Casanova L, Hughes FJ, Preshaw PM. Diabetes and periodontal disease: a two-way relationship. Br Dent J 2014;217:433-437.

3. Khader YS, Albashaireh ZS,. Alomari MA. Periodontal diseases and the risk of coronary heart and cerebrovascular disease: A meta-analysis. J Periodontol 2004;75:1046-1053.

4. Mustapha IZ, Debrey S, Oladubu M, Ugarte R. Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: A systematic review and meta-analysis. J Periodontol 2007;78:2289-2302.

5. Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. Ann Periodontol 2003;8:54-69.

6. Scannapieco FA, Bush RB, Paju S. Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Ann Periodontol 2003;8:70-78.

7. Xiong X, Buekens P, Fraser WD, Beck J, Offenbacher S. Periodontal disease and adverse pregnancy outcomes: A systematic review. BJOG 2006;113(2):135-143.

8. Kaur S, White S, Bartold PM. Periodontal disease and rheumatoid arthritis: a systematic review. J Dent Res. 2013;92(5):399-408.

9. Centers for Disease Control and Prevention (CDCP). Behavioral Risk Factor Surveillance System. Available at: http://www.cdc.gov/brfss/. Accessed March 17, 2010.

10. Slade GD. Interim analysis of validity of periodontitis screening questions in the Australian population. J Periodontol 2007;78(Suppl. 7):1463-1470.

11. Eke PI, Dye B. Assessment of self-report measures for predicting population prevalence of periodontitis. J Periodontol 2009;80:1371-1379.

12. Siegal MD, Martin B, Kuthy RA. Usefulness of a local oral health survey in program development. J Public Health Dent 1988;48:121-124.

13. Kallio P.Self-assessed bleeding in monitoring gingival health among adolescents. Community Dent Oral Epidemiol 1996;24:128-132.

14. Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ, Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol 2004;57:1096-1103.

15. Nelson DE, Holtzman D, Bolen J, Stanwyck CA, Mack KA. Reliability and validity of measures from the behavioral risk factor surveillance system (BRFSS). Soz Praventivmed 2001;46(Suppl.1):S3-S42.

16. Bergmann MM, Jacobs EJ, Hoffmann K, Boeing H. Agreement of self-reported medical history: Comparison of an in-person interview with a self-administered questionnaire. Eur J Epidemiol 2004;19:411-416.

17. Gilbert GH, Duncan RP, Kulley AM. Validity of selfreported tooth counts during a telephone interview. J Public Health Dent 1997;57:176-180.

18. Palmqvist S, Soderfeldt B, Arnbjerg D. Self-assessment of dental conditions: Validity of a questionnaire. Community Dent Oral Epidemiol 1991;19:249-251.

19. Heloe LA. Comparison of dental health data obtained from questionnaires, interviews, and clinical examination. Scand J Dent Res1972;80:495-499.

20. Pitiphat W, Garcia RI, Douglass CW, Joshipura KJ. Validation of self-reported oral health measures. J Public Health Dent 2002;62:122-128.

21. Moher D, Liberati A, Tetzlaff J, Altman DG, the PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009 6(7): e1000097. doi:10.1371.

22. International prospective registers of systematic reviews, University of York, National Institute for Health Research, Available at: http://www.crd.york.ac.uk/PROSPERO/. Accessed 25 May 2016.

23. Systematic review data repository, AHRQ. Agency for Healthcare Research and Quality, Rockville, MD. , March 2016. Available at: http://srdr.ahrq.gov/home/index. Accessed 25 May 2016.

24. Whiting P, Rutjes AW, Reitsma JB, Glas AS, Bossuyt PM, Kleijnen J. Sources of variation and bias in studies of diagnostic accuracy: a systematic review. Ann Intern Med 2004;140:189-202.

25. Pai M, Flores LL, Pai N, Hubbard A, Riley LW, Colford JM. Diagnostic accuracy of nucleic acid amplification tests for tuberculous meningitis: a systematic review and meta-analysis. Lancet Infect Dis 2003;3:633-643.

26. Lijmer JG, Mol BW, Heisterkamp S et al.Empirical evidence of design-related bias in studies of diagnostic tests. JAMA 1999;282:1061-1066.

27. Walter SD, Irwig L, Glasziou PP. Meta-analysis of diagnostic test with imperfect reference standards. J Clin Epidemiol 1999;52:943-951.

28. Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007;78:1387-1399.

29. Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ. Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 2012;83(12):1449-1454.

30. WHO, Oral Health Surveys: Basic methods, 5th ed., Geneva: World Health Organization, 2013.

31. Blicher B, Joshipura K, Eke PI. Validation of self-reported periodontal disease: a systematic review. J Dent Res 2005;84(10):881-890.

32. QUADAS, University of Bristol. Available at: http://www.bristol.ac.uk/social-community-medicine/projects/quadas/. Accessed 25 May 2016.

33. Shea BJ, Grimshaw JM, Wells GA, et al. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Methodol 2007;7(10). doi:10.1186/1471-2288-7-10.

34. Korte de PJ. Probability analysis in diagnosing coronary artery disease. [Thesis]. Netherlands, Maastricht: Universitaire Pers Maastricht; 1993 38-39.

35. Kraemer HC. Predictive values: The Bayesian approach, risk ratios and odds ratios. In: Kraemer HC eds. Evaluating medical tests, Newbury Park, CA: AGE Publications; 1992:103-113.

36. Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol. 2003 Nov;56(11):1129-1135.

37. Zamora J, Abraira V, Muriel A, Khan K, Coomarasamy A. Meta-DiSc: a software for meta-analysis of test accuracy data. BMC Med Res Methodol 2006; doi:10.1186/1471-2288-6-31

38. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta analysis. Stat Med 2002;21:1539-1558.

39. Coburn BW, Sayles HR, Payne JB, Redman RS, Markt JC, Beatty MW, Griffiths GR, McGowan DJ. Performance of Self-Reported Measures for Periodontitis in Rheumatoid Arthritis and Osteoarthritis. J Periodontol 2015;8(1):16-26.

40. LaMonte MJ, Hovey KM, Millen AE, Genco RJ,. Wactawski-Wende J. Accuracy of self-reported periodontal disease in the Women's Health Initiative Observational Study. J Periodontol 2014;85(8):1006-1018.

41. Genco RJ, Falkner KL, Grossi S, Dunford R, Trevisan M. Validity of self-reported measures for surveillance of periodontal disease in two western New York population-based studies. J Periodontol 2007;78(suppl: 7):1439-1454.

42. Taylor GW, Borgnakke WS. Self-reported periodontal disease: validation in an epidemiological survey. J Periodontol 2007;78(Suppl 7): 1407-1420.

43. Wu X, Weng H, Lin X. Self-reported questionnaire for surveillance of periodontitis in Chinese patients from a prosthodontic clinic: a validation study. J Clin Periodontol 2013;40(6): 616-623.

44. Dietrich T, Stosch U, Dietrich D, Schamberger D, Bernimoulin JP, Joshipura K. The accuracy of individual self-reported items to determine periodontal disease history. Eur J Oral Sci 2005;113(2):135-140.

45. Cyrino RM, Miranda Cota LO, Pereira Lages EJ, Bastos Lages EM, Costa FO. Evaluation of self-reported measures for prediction of periodontitis in a sample of Brazilians. J Periodontol 2011;82(12):1693-1704.

46. Balappanavar AY, Sardana V, Nagesh L, Ankola AV, Kakodkar P, Hebbal M. Questionnaire vs clinical surveys: the right choice? A cross-sectional comparative study. Indian J Dent Res 2011; 22(3): 494.

47. Akaji EA, Jeboda SO, Oredugba FA. Comparison of Normative and Self-perceived Dental needs among Adolescents in Lagos, Nigeria. Niger Postgrad Med J. 2010;17(4):283-286.

48. Vered Y, Zini A, Sgan-Cohen HD. Psychological distress and self-perception of oral health status among an immigrant population from Ethiopia. Ethn Health 2009;14(6):643-652.

49. Yazdani R, Vehkalahti MM, Nouri M, Murtomaa H. Validity of self-assessment of oral health among 15-year-olds in Tehran, Iran. Oral Health Prev Dent 2008; 6(4): 263-269.

50. Le H, Theilade E, Brglum JS. Experimental Gingivitis in Man. J Periodontol 1965; 36(3):177-187.

51. Website. What is Grey Literature?. Available at: http://www.greylit.org/about. Accessed June 13,2016.

52. Chattopadhyay A. Periodontal disease.In: Chattopadhyay A. ed. Oral Health Epidemiology. Principles and Practice, Massachusetts: Jones and Bartlett Publishers; 2011: 257-271.

53. Pihlstrom BL. Periodontal risk assessment, diagnosis and treatment planning. Periodontol 2000 2001;25:37-58.

54. Danielsen B, Manji F, Nagelkerke N, Fejerskov O, Baelum V. Effect of cigarette smoking on the transitional dynamics in experimental gingivitis. J Clin Periodontol 1990;17:164-159.

55. Lie MA, Loos B, Henskens YMC, Timmerman MF, Veerman ECI, van der Velden U, van der Weijden G. A. Salivary cystatin activity and cystatin C in natural and experimental gingivitis in smokers and non-smokers. J Clin Periodontol 2001;28:979-984.

56. Nair P, Sutherland G, Palmer RM, Wilson RF, Scott DA. Gingival bleeding on probing increases after quitting smoking. J Clin Periodontol 2003;30:435-437.

57. Haffajee A, Socransky S, Goodson J. Clinical parameters as predictors of destructive periodontal disease activity. J Clin Periodontol 1983;10(3):257-265.

58. Badersten A, Nilvus R, Egelberg J. Effect of nonsurgical periodontal therapy. VII. Bleeding, suppuration and probing depth in sites with probing attachment loss. J Clin Periodontol 1985;12:432-440.

59. Lang N, Joss A, Orsanic T, Gusberti F, Siegrist B. Bleeding on probing. A predictor for the progression of periodontal disease?. J Clin Periodontol 1986;13:590-596.

60. Claffey N, Nylund K, Kiger R, Garrett S, Egelberg J. Diagnostic predictability of scores of plaque, bleeding, suppuration and probing depth for attachment loss. J Clin Periodontol 1990;17:108-114.

61. Kaidahl W, Kalkwarf K, Patii K, Molvar M. Relationship of gingival bleeding, gingival suppuration, and supragingival plaque to attachment loss. J Periodontol 1990;61:347-351.

62. Lang N, Nyman S, Senn C, Joss A. Bleeding on probing as it relates to probing pressure and gingival health. J Clin Periodontol 1991;18: 257-261.

63. Clerehugh V, Worthington HV, Lennon MA, Chandler R. Site progression of loss of attachment over 5 years in 14- to 19-year-old adolescents. J Clin Periodontol 1995; 22: 15-21.

Table 1 General description of the included studies.

First author (Year of Publication)

Country of study

Type of the study

Participant recruitment

No. of participants

Males/Females ratio

Age of participants (years)

Coburn (2015)39

USA

cross sectional

Rheumatology clinic

617

380/237

59.2 mean age

LaMonte (2014)40

USA

cohort

Female recruited for parent study called WHI-OS

972

only females

53 82 range

Wu (2013)43

China

cross-sectional

Prosthodontic clinic

114

46/68

18-77 range

Cyrino (2011)45

Brazil

cross-sectional

Employees of a large corporation in Brazil

284

208/76

No information

Balappanavar (2011)46

India

cross-sectional

Bank employees

860

507/353

18-60 range

Akaji (2010)47

Nigeria

cross-sectional

Stratified random from 4 secondary schools

504

No information

10-19 range

Vered (2009)48

Israel

Cross-sectional

Immigrated Ethiopian

340

145/195

+18

Yazdani (2008)49

Iran

cross-sectional

No information

509

No information

15 years old

Genco 2007)41

USA

cross-sectional sub-study from case-control

No information

1426

685/741

25-74 range

Taylor (2007)42

USA

cross-sectional

Telephone interview based on census tracts

455

194/261

18-81 range

Dietrich (2005)44

China

cross-sectional

Endodontic surgery clinic

246

No information

20-80 range

Table 2 Diagnostic odds ratio and 95% confidence interval of highly frequent questions in the selected studies.

Question (Key word)

Clinical gold standard

Sensitivity %, Specificity %

Pooled sensitivity (95% CI)

Pooled Specificity (95% CI)

DOR (95% CI)[footnoteRef:10] [10: Diagnostic Odds Ratio (95% Confidence Interval)]

PDOR[footnoteRef:11] [11: Pooled Diagnostic Odds Ratio]

I2 % [footnoteRef:12](p for heterogeneity chi-squared) [12: Inconsistency]

Studies used

Do you think you have gum disease? (Gums disease)

Moderate CDC-AAP[footnoteRef:13]28 [13: The Centres for Disease Control and Prevention and the American Academy of Periodontology]

64.3, 69.0

45.1, 75.7

20.9, 93.3

35.8% (30.3- 41.6)

84.2% (80.8- 87.1)

4.00 (1.83- 8.72)

2.57 (1.49- 4.41)

3.67 (2.01- 6.70)

3.20 (2.23-4.57)

0.0 (0.563)

Wu (2014)43

Cyrino (2011)45

Taylor (2007)42

Severe CDC-AAP28

64.3, 58.1

54.5, 72.9

29.6, 90.7

45.2% (35.9- 54.8)

80.7% (77.6- 83.5)

2.50 (1.03- 6.05)

3.23 (1.54- 6.77)

4.10 (2.08- 8.08)

3.35 (2.17- 5.18)

0.0 (0.674)

Wu (2014)43

Cyrino (2011)45

Taylor (2007)42

Have you ever had any teeth become loose on their own, without an injury? (Tooth mobility)

Moderate CDC-AAP28

67.9, 89.7

17.1, 95.5

20.5, 95.2

28.3% (23.3- 33.7)

94.7% (92.5- 96.4)

18.30 (6.64- 50.45)

4.41 (1.83- 10.66)

5.06 (2.62- 9.75)

6.99 (3.17- 15.43)

62.4 (0.070)

Wu (2014)43

Cyrino (2011)45

Taylor (2007)42

Severe CDC-AAP28

92.9, 79.1

24.2, 94.0

41.1, 93.7

54.9% (47.2- 62.5)

91.9% (89.8- 93.7)

49.11 (10.64- 226.62)

5.03 (1.94- 13.04)

10.43 (5.34- 20.35)

11.72 (4.12- 33.36)

69.6 (0.037)

Wu (2014)43

Cyrino (2011)45

Taylor (2007)42

Have you ever had painful gums? (Painful gums)

Moderate CDC-AAP28

48.2, 79.3

6.6, 94.5

17.1% (12.4- 22.7)

91.9% (88.5- 94.6)

3.57 (1.57- 8.13)

1.21 (0.55- 2.67)

2.07 (0.72- 5.96)

70.9 (0.064)

Wu (2014)43

Taylor (2007)42

Severe CDC-AAP28

60.7, 74.4

3.6, 93.7

22.6% (14.2- 33.0)

90.3% (87.3- 92.8)

4.50 (1.83- 11.06)

0.55 (0.13- 2.41)

1.71 (0.22- 13.57)

82.8 (0.016)

Wu (2014)43

Taylor (2007)42

Have you ever noticed that your front teeth have moved forward (towards the lip) or that gaps have developed between your front teeth? (Tooth migration)

Moderate CDC-AAP28

42.9, 79.3

25.6, 82.7

32.6% (24.9- 41.1)

81.9% (76.7- 86.4)

2.87 (1.26 - 6.57)

1.64 (0.89- 3.04)

2.02 (1.19- 3.44)

11.8 (0.287)

Wu (2014)43

Cyrino (2011)45

Severe CDC-AAP28

50.0, 74.4

27.3, 81.3

37.7% (25.6- 51.0)

79.5% (74.8- 83.7)

2.91 (1.20- 7.05)

1.63 (0.71- 3.73)

2.14 (1.17- 3.91)

0.0 (0.348)

Wu (2014)43

Cyrino (2011)45

Have you been told that you have bone lost around your tooth? (Bone loss)

Moderate CDC-AAP28

14.3, 89.7

22.0, 87.1

18.8% (12.7- 26.4)

87.7% (83.1-91.4)

1.44 (0.47- 4.47)

1.90 (0.98- 3.70)

1.77 (1.00 -3.15)

0.0 (0.679)

Wu (2014)43

Cyrino (2011)45

Severe CDC-AAP28

21.4, 90.7

33.3, 86.9

21.6% (16.1- 28.0)

87.8% (84.9- 90.3)

2.66 (0.83- 8.48)

3.30 (1.47- 7.43)

3.08 (1.58- 5.98)

0.0 (0.764)

Wu (2014)43

Cyrino (2011)45

Have you received the following treatment: scaling and root planing? (deep cleaning)

Moderate CDC-AAP28

25.0, 89.7

22.0, 88.6

22.9% (18.8- 27.3)

87.7% (85.7- 89.5)

2.89 (1.02- 8.18)

2.19 (1.11- 4.32)

2.38 (1.35 -4.20)

0.0 (0.661)

Wu (2014)43

Cyrino (2011)45

Severe CDC-AAP28

21.4, 83.7

30.3, 87.6

22.9% (18.8- 27.3)

87.7% (85.7-89.5)

1.40 (0.48- 4.08)

3.09 (1.34- 7.09)

2.24 (1.05 -4.80)

23.8 (0.252)

Wu (2014)43

Cyrino (2011)45

Have you had any of the following oral conditions? (Bleeding gums)

Moderate CDC-AAP28

18.1, 83.4

15.5, 90.3

15.9% (13.9- 18.0)

86.7% (83.5- 89.4)

1.11 (0.67- 1.83)

1.72 (1.10- 2.68)

1.40 (0.91 -2.16)

40.0 (0.197)

Taylor (2007)42

Genco (2007)41

Severe CDC-AAP28

21.4, 83.5

22.4, 88.7

17.5% (15.7- 19.4)

87.0% (85.4- 88.5)

1.38 (0.69- 2.75)

2.25 (1.64- 3.10)

1.95 (1.25 -3.03)

38.3 (0.203)

Taylor (2007)42

Genco (2007)41

Table 3 Quality assessment for all included studies depending on QUADAS2.

Author sure name , Year

Coburn, 201539

LaMonte, 201440

Wu, 201343

Balappanavar, 201146

Cyrino, 201145

Akaji, 201047

Vered, 200948

Yazdani, 200849

Genco, 200741

Taylor, 200742

Dietrich, 200544

Random sampling

Yes

Unclear

Yes

Yes

Yes

Yes

Yes

Unclear

yes

Yes

Yes

Case-control design avoided

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

yes

Yes

Yes

Inappropriate exclusions avoided?

Yes

Yes

Yes

No

Yes

Yes

Yes

Unclear

Unclear

Yes

Yes

Is there concern that the included patients do not match the review question?

Concern: Low

Unclear

Concern: Low

Concern: Low

Concern: Low

Concern: Low

Concern: Low

Concern: Low

Concern: Low

Concern: Low

Concern: High

Were the index test results interpreted without knowledge of the results of the reference standard?

Yes

Yes

Yes

Yes

Unclear

Unclear

Unclear

Unclear

Yes

Yes

Yes

If a threshold was used, was it pre-specified?

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Unclear

Yes

Yes

Yes

Reference standard likely to correctly classify the target condition.

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Reference standard results interpreted without knowledge of the results of the index test.

Yes

Unclear

Yes

Yes

Unclear

Yes

Unclear

Unclear

Unclear

Unclear

Yes

Appropriate interval between index test(s) and reference standard?

Yes

No

Yes

Yes

Unclear

Unclear

Yes

Unclear

Yes

Unclear

Yes

Did participants receive the same reference standard?

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

All participants included in the analysis

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

General assessment

good

fair

good

good

good

good

good

bad

good

good

good

Table 4 Quality assessment of systematic review by Blicher et al.31 using AMSTAR criteria33.

1. Was an a priori design provided?

Yes

2. Was there duplicate study selection and data extraction?

Yes

3. Was a comprehensive literature search performed?

Yes

4. Was the status of publication (i.e. grey literature) used as an inclusion criterion?

Cant answer

5. Was a list of studies (included and excluded) provided?

No

6. Were the characteristics of the included studies provided?

Yes

7. Was the scientific quality of the included studies assessed and documented?

No

8. Was the scientific quality of the included studies used appropriately in formulating conclusions?

Yes

9. Were the methods used to combine the findings of studies appropriate?

No

10. Was the likelihood of publication bias assessed?

No

11. Was the conflict of interest stated?

No