Skip to main content

Table 3 Summary of the included studies

From: A systematic review and network meta-analysis of the association between periodontitis and inflammatory bowel diseases

Author (Year) [Reference]

Country

Type of Study

IBD type- Diagnostic method

PD type- Diagnostic method

Follow-up Duration

Population, Sex (Female%)

 

Mean Age (SD)

Outcomes

Confounding Factors

Quality Score

Vanessa [30] [30]

Italy

Case–control

CD and UC—MC

AP- Periapical radiography (PAI)

3 years

220

%55.45 patients;

%51.81 control

NR

▪ The prevalence of Apical Periodontitis (AP): IBD patients (64%) > controls (59%)

▪ According to the gender-stratified analysis: the difference was not significant among the male groups, but the number of teeth with AP was significantly higher in female patients with IBDs than in the controls

▪ AP was more common among patients with IBDs + biological medications

Smoking, diabetes, age

8/10 (%80)

J Schmidt.J et.al et al. 2018 [2]

Germany

Cross-sectional

CD and UC—NR

MTSP- Scaled periodontal probe (PPD, CAL)

during their regular subsequent appointment

at 1 year and 4 months

118

%60 CD;

%55.17 UC;

%57.62 control

49.6 (11.9) CD

50.0 (12.4) UC

51.3 (12.0) Control

▪ More severe periodontitis and higher concentrations of active-matrix metalloproteinase-8 (aMMP-8): IBD > control

▪ Only in CD: ↑ aMMP-8 was associated with the severity of periodontal disease

▪ The role of periodontal pathogenic bacteria in the interrelation between IBD and periodontitis is unclear

Smoking, gender, IBD medication

8/8 (%100)

Manuel Poyato-Borrego et al. 2019 [31]

Spain

Case–control

CD and UC—MC

AP- Periapical radiography (PAI)

1 year

162

%42.6 patients;

%42.6 control

43.1 (14.0) IBD

43.1 (13.8) Control

▪ Teeth with radiolucent periapical lesions (RPLs): patients with IBD > controls

▪ The number of teeth and the number of root-filled teeth are significantly associated with periapical radiolucencies (the number of teeth and the number of RFT: IBD patients = controls)

▪ Higher prevalence of AP in IBD > controls

Smoking, number of teeth, root-filled teeth

7/10 (%70)

Giacomo Baima.G et.al et al. 2022 [20]

Italy

Case–control

CD and UC – ECCO

MTSP- Scaled periodontal probe (PPD, CAL)

1 year

360

%47.9 CD;

%35.0 UC;

%43.3 IBD;

%42.8 control

47.9 (13.6) CD

49.3 (17.8)

UC

47.8 (14.3) Control

▪ The prevalence of Periodontitis in IBD (no differences between CD and UC) < control periodontitis was more significantly associated in the middle age categories (36–50 and 51–65 years)

▪ Tailored interdisciplinary preventive and therapeutic programs involving the gum–gut axis

▪ Longer disease duration and IBD-associated surgery: negatively associated with periodontitis

Age, smoking, IBD duration, IBD-associated surgery

8/10 (%80)

Kristina Bertl.K et.al et al. 2023 [21]

Denmark

Case–control

CD and UC – HBI and SCCAI

SP- PESS

6 months

5786

%74.5 patient;

%79.1 control

48.0 (14.8) IBD

48.9 (13.3) Control

▪ IBD: associated with impaired patients' oral-health-related QoL (quality of life) [bilateral relationship]

▪ Two- and three-times higher prevalence of a poor oral-health-related QoL in UC and UC

▪ Fewer teeth + problems with oral lesions: CD patients > UC patients

▪ Prevalence of problems in various daily-life activities: CD patients > UC patients

▪ IBD activity and severity + depression + a stressful daily life experience (confounders): IBD-specific health-related QoL/a longer time since diagnosis: IBD-specific health-related QoL

Smoking, systemic diseases, family status, daily-life experience, BMI, age, gender, education, income

10/10 (%100)

Fernanda [27] [27]

Brazil

Case–control

CD and UC – CDAI and TWI

PD – Scaled periodontal probe (PPD, CAL)

1 year

253

%68.7 CD;

%58.7 UC;

%67.6 control

39.5 (10.5) CD

45.0 (9.3)

UC

42.1 (7.8) Control

▪ Decayed, missing, and filled teeth (DMFT) and prevalence of periodontitis: UC and CD > controls

▪ DMFT index: UC > CD

▪ Periodontitis: more common among smoking patients with UC prevalence of periodontitis: UC and CD > controls prevalence of periodontitis: smokers with UC > smokers without UC in both smokers and non-smokers a tendency of more CAL and more sites with CAL ≥ 3 mm

▪ Among non-smokers:

• Sites with plaque and deeper PPD: CD patients < controls

• DMFT score and deeper pockets: CD patients > controls

• After adjustment for race, gender, age, and plaque: UC and CD > controls

Smoking, age, gender, race, plaque, systemic diseases, medication use

7/10 (%70)

Ying-Chen [34] [34]

Taiwan

Cohort study

CD- ICD9CM and biopsy

PD- ICD9CM

2 years

33,285

%53.7

Stratified

▪ Significant difference in risk between genders or across ages was not present

▪ Steroids, aspirin, Plavix, and Vicodin have a protective effect

▪ Increased hazard ratio for subsequent periodontitis among CD patients compared to subjects without IBD

▪ Significantly worse Decayed/Missing/Filled Teeth index in IBD patients

Socioeconomic status, urbanicity, medical co-morbidities, pharmaceutical prescriptions, age, gender

6/11 (%54.5)

Hui-Chieh [14] [14]

Taiwan

Cohort study

CD and UC – ICD9CM

CP- ICD9CM

3.00 years in the IBD group;

3.15 years in the non-IBD group

135

%37 IBD patients;

%50 No IBD;

%47.4 overall

38.0 (10.8) IBD

36.3 (13.6) Control

▪ Risk of having periodontitis: IBD patients (CD > UC) > controls

▪ CD: showed a significantly higher risk for developing periodontitis

▪ UC: had borderline significance for higher risk of periodontitis

▪ Male predominant in IBD patients ☑

▪ Higher risk for developing periodontitis: female IBD patients > non-IBD group

▪ IBD group with middle-class to high-class economic status: higher risk for developing periodontitis

▪ Rapid socioeconomic development and exposure to environmental risk factors in childhood → association between IBD and periodontitis

Age, sex, urbanization level, socioeconomic status

9/11 (%81.8)

[32] [32]

Greece

Case–control

CD and UC- CDAI and TWI

PD- Periapical radiography

a long

period (> 5 years)

77

not mentioned

40 (16) IBD

43 (12) Control

▪ Three or more oral lesions: IBD patients > controls

▪ The incidence of gingivitis, periodontitis, and gingival bleeding: significant differences between patients with CD and controls ☑

▪ The same parameters between patients with UC and controls: no significant differences

▪ Other lesions such as leukoplakia, perioral erythema, buccal space, abscess, perioral erythema, and erythema migrants, fissured and geographic tongue and aphthous-like ulcer: no significant differences between patients and controls is observed

▪ Lymphadenopathy and salivary gland involvement in IBD patients: ☑

▪ Multiple oral manifestations: CD > UC

▪ Oral manifestations in patients with IBD (especially in CD) are a frequent and underestimated event that needs further clinical validation

Age, sex, smoking habit, duration of disease

6/10 (%60)

Limin [33] [33]

China

Cross-sectional

CD and UC—ECCO

PD- Scaled periodontal probe (PPD, CAL)

almost one year

54

%35.8 CD;

%39.5 UC;

%43.4 control

26 (16.3) Control

29 (9.63) CD

39 (9.62) UC

▪ The decayed, missing, and filled surfaces indices and percentages of sites with probing pocket depth ≥ 5 mm and clinical attachment loss ≥ 4 mm: CD and UC > Controls

▪ Differences in dental caries and periodontal disease between the CD and UC patients:

▪ Values for DMFT, DMFS, DT, DS, and MT: IBD patients (UC and CD) > controls

Age, sex, education level, smoking, daily frequency of tooth-brushing, and dietary habits

8/8 (%100)

Juan J [23] [23]

Spain

Case–control

CD and UC—MC

AP- Periapical radiography (PAI)

4 years

56

%71.4 IBD;

%71.4 control

59.1 (10.9) IBD

58.6 (11.9) Control

▪ Prevalence of RFT and percentage of RFT with periapical lesions: UC and CD > controls

▪ A similar mean number of teeth between the Control group and study group was observed

Age, sex, number of teeth, periapical status, smoking, diabetes,, cardiovascular disease

9/10 (%90)

Vassiliki [29] [29]

Turkey

Case–control

CD and UC – PC

PD- Probe and CPITN (PPD)

6_12 months

110

%50 CD;

%63.2 UC;

%54.5 IBD

12.32 (3.41) IBD

12.21 (3.96) Control

▪ This study deals with children and adolescents with IBD

▪ DMF-T and the mean value of GI-S (the simplified gingival index): IBD patient > controls

▪ Mean values of PCR: no difference between groups

▪ Patients with IBD on immunomodulators: severe periodontal disease + ↑ periodontal treatment

▪ Healthy periodontium is not present in IBD patients

Age, sex, oral hygiene habits, smoking, systemic conditions, medications, dietary habits

8/10 (%80)

R A Habashneh et al. 2011 [28]

Jordan

Case–control

CD and UC—ECCO

PD- Scaled periodontal probe (PPD, CAL)

7 months

260

%44.1 CD;

%39.6 UC;

%38.0 control;

%40.0 overall

Stratified

▪ Prevalence and severity and extent of periodontitis: IBD patients > controls

▪ No significant difference in the prevalence of periodontitis between the three groups but much higher among patients with CD and UC compared with subjects without IBD in the age groups < 36 and 36–45 years old only

▪ The average plaque index and average gingival index: UC and CD > controls

▪ Difference in average plaque index and average gingival index is not observed

▪ The average gingival recession: UC > CD > Controls

Age, sex, education level, occupation, smoking habits, oral hygiene behaviors, number of missing teeth

10/10 (%100)

  1. Symbols: ↑: Increase, : Decrease; Abbreviations: MC: Montreal Criteria for IBD, ECCO: European Crohn´s and Colitis Organization criteria, HBI: Harvey-Bradshaw index, SCCAI: Simple Clinical Colitis Activity Index, CDAI: Clinical Disease Activity Index, TWI: work time impairment, PC: Porto Criteria, AP: Apical Periodontitis, SP: Severe Periodontitis, MTSPD: Mild to severe periodontitis, PPD: Pocket probe depth, CAL: Clinical attachment level, PAI: The periapical index, PESS: Periodontal Screening Score, BOP: Bleeding on probing, ICD9CM: ICD-9-CM diagnosis code, CPITN: Community Periodontal Index of Treatment Needs screening method