Inflammatory bowel disease and periodontitis: A retrospective chart analysis

Abstract Objectives This study examined the variation in prevalence of periodontitis among different sexes, age groups, smoking status, and oral hygiene adherence in patients affected by either Crohn's disease (CD) or ulcerative colitis (UC). Materials & Methods This study was a retrospective chart analysis that collected data from the School of Dentistry's Oral Health Clinic at the University of Alberta, Edmonton, Canada. Patients' electronic health records between the years of 2013 and 2019 were analyzed. Multiple keywords such as IBD, CD, UC, and periodontal disease with various spelling combinations were used for searching and gathering pertinent data, which was then further assessed. After applying the inclusion and exclusion criteria, a total of 80 patient charts were included. These patient charts were thoroughly screened to gather information such as age, sex, smoking status, and a variety of periodontal parameters. Collected data were analyzed using SPSS software by using Pearson's χ2, Pearson's correlation, and Mann–Whitney U‐test. Results IBD had an impact on the severity of periodontitis in patients between the ages of 50 and 64 years with higher odds ratio (OR). Biological sex or history of smoking in IBD patients did not have higher odds of developing periodontitis. Plaque score derived from this retrospective study was used to estimate the patient's oral hygiene status and showed no impact. Also, prevalence of periodontitis did not differ between UC and CD. We anticipated some of these findings because of the retrospective nature of the study. Conclusions Within the limitation of the retrospective study, IBD patients in the 50–64 age group years showed a higher odds ratio for a greater prevalence of periodontitis. Thus, a closer periodontal recall and evaluation in these patients is recommended for early diagnosis and preventive care. It is advised that periodontists work closely with gastroenterologists to maintain periodontal health in IBD‐affected individuals.

has also been reviewed as a potential factor that might be accountable for the altered predisposition to periodontitis in IBD patients (Brito et al., 2013;Van Dyke et al., 1986). A higher prevalence of Treponema denticola and other bacteria, in connection with opportunistic infections in subgingival sites, was reported in IBD patients (Brito et al., 2013). Immune-inflammatory response studies demonstrated elevated levels of TNF-α (tumor necrosis factor-alpha) in the gastrointestinal tract of CD patients, as well as in the gingival crevicular fluid of periodontitis patients (Figueredo et al., 2011).
A cohort study was conducted to explore the association between IBD and periodontitis. The study concluded higher prevalence, severity, and extent of periodontitis in IBD patients when compared with non-IBD individuals (Vavricka et al., 2013). Several efforts are continuously being made to explore the association of these two conditions.
Given the high prevalence of IBD in Canada in the absence of a clear genetic etiology, we asked if this connection is also seen in a population with higher susceptibility to IBD. We present a retrospective study aimed to estimate the risk of developing periodontitis considering variables like sex, age, smoking status, oral hygiene adherence in a population affected by different forms of IBD, that is, CD or UC.

| Study design and data collection
This study evaluated patient records from the School of Dentistry's Oral Health Clinic consisting of a history of IBD (IBD, Inflammatory bowel syndrome, CD, UC, indeterminate colitis) between January 2013 and December 2019. All data for this study were obtained from existing axiUm clinic records. AxiUm Dental is a HIPAA-compliant (Health Insurance Portability and Accountability Act), ONC-ATCB (Office of the National Coordinator-Authorized Testing and Certification Body) certified system. It involves applications such as electronic health records (EHR), billing, and practice management designed to address the needs of educational programs in dentistry. No personal data, including name, that could reveal the patient identity was accessed. Since the study was designed to access the complete pool of patients who visited the School of Dentistry clinic from January 2013 to December 2019, unique keywords were used to define the search in the patient records (Table 1).
The screening process is displayed in  (Fukuda et al., 2008;Hamp et al., 1975;Miller, 1950). Bone loss was radiographically determined by subtracting 2 mm from the cementoenamel junction (CEJ) and measuring up to the alveolar bone crest (X). The percentage bone loss was calculated by dividing X with length from CEJ to the apex of the tooth multiplied by 100 (Brito et al., 2013). All calculations were done in axiUm software using radiographs available in the patient records. Periodontal charts were analyzed to determine the presence and severity of periodontitis. If absent (healthy periodontium), it was denoted as N. If present, it was recorded as Y and the stage of periodontitis (Stages I-IV) was noted according to World Workshop 2017 (Tonetti et al., 2018). Oral hygiene adherence was estimated from plaque scores due to the retrospective nature of the study. Plaque scores (using the O'Leary plaque scoring method) were recorded on four tooth surfaces, three on buccal (mesial, mid, distal) and one on palatal/lingual.
The scores range from 0 to 1; 0 means no plaque, and 1 represents the presence of plaque. The percentage of plaque is calculated by dividing the total surfaces with score one by the total number of surfaces recorded multiplied by 100 (O'Leary et al., 1972). Lastly, the patients' smoking status was recorded as current smokers, past smokers, or non-smokers.
Parameters recorded from each patient chart are listed in Table 3.

| Data analysis
Once all the data were retrieved, grouping was done to conduct statistical analysis. Records were divided according to periodontal severity (Stages I-IV). For comparison of biological sex data were grouped into males (denoted as M) and females (denoted as F there were significant differences in incidence of periodontitis between the five different age groups computed the p value of 0.009, which implies a significant difference in copresenting periodontitis and IBD between the age groups. Odds ratios among different age groups (Table 7) showed consistent higher odds of periodontitis with ages ≥50 years compared to those less than 50 years of age.

| Smoking status
Pearson's χ 2 test was applied to determine a significant difference between two groups divided based on their smoking status, past and current smokers as one group and nonsmokers as the second group.
A p = .698 was determined, which implies no significant difference in these groups in presenting with periodontitis in IBD patients.

| Oral hygiene adherence
Pearson's correlation test was conducted to evaluate the variation in severity of the periodontitis based on plaque percentage. The analysis revealed no statistically significant difference (p = 0.339), suggesting that the presence of plaque did not lead to a prevalence of periodontitis in individuals with IBD.

| Disease type
Mann-Whitney U test was used to establish if there was a difference in periodontitis presentation between the two forms of IBD (UC and CD). With a p value of 0.420 no significant difference was observed.

| Summary of results
We found no sex predilection for periodontitis in patients presenting with IBD. When patients were grouped into five groups according to NHANES criteria (Borrell & Talih, 2012)

| DISCUSSION
The present study examined incidence and severity of periodontitis in IBD individuals. We found no difference in incidence between the two sexes. Previous studies indicated that males have a higher risk for periodontitis; thus, a sex predilection has been determined to be associated with periodontitis (Eke et al., 2015;Heitz-Mayfield, 2005). A sex prevalence was also previously noted between patients with IBD depending on the type of IBD (UC and CD) (Rossomando et al., 1990). A study that looked at sex variation in IBD stated that in patients with CD, | 1031 a greater prevalence of females with the disease was noticed, while in patients with UC, no significant differences between prevalence of the disease in females or males were observed (Brant & Nguyen, 2008). It was also stated that the sex ratios in CD varied with age and geographic region (Brant & Nguyen, 2008). In spite of the male predilection for periodontitis and female predilection for CD, our study failed to establish any sex predilection for the two diseases. A likely reason for this difference is the comparatively small sample size in this study. A larger study with more patients in each age group of both the sexes is needed to explore this further.
According to the NHANES study periodontitis has a higher incidence in the elderly (age groups over 65 and 75) (Billings et al., 2018;Eke et al., 2015). Our study showed the highest odds of presenting with periodontitis in the age range of 50-64. This group had a higher risk of presenting with periodontitis (OR 11.10) when compared to ages 20-34 years. NHANES data similarly established that the prevalence of periodontitis was positively associated with age (Billings et al., 2018;Eke et al., 2015). Literature supports the association between IBD and periodontitis on account of their similar etiologies, that is, dysbiotic microbiota, deregulation of the immune response, and chronic inflammation in genetically susceptible individuals (Lira-Junior & Figueredo, 2016;She et al., 2020). The association stated thus corroborates with the increased odds of periodontitis in the elderly age group, since age is a risk factor for periodontitis itself and with a history of IBD, the odds may tend to increase (Flemmig et al., 1991;Indriolo et al., 2011;Lira-Junior & Figueredo, 2016;Papageorgiou et al., 2017;She et al., 2020;Van Dyke et al., 1986). In the present study no linear relationship between the patient's age and these two disease conditions was observed. This could be due to the fact that periodontitis tends to peak in the elderly group, that is, >50 years (Billings et al., 2018). IBD has a bimodal incidence pattern, with the main peak of occurrence between 15 and 25 years of age and a second, smaller rise in IBD occurrence during the fifth to seventh decades of life (Johnston & Logan, 2008). It is likely that patient records included our study represented this second peak of IBD presentation and thus formed most of the data. explaining the increased odds of periodontitis in this age group. On the other hand, another it might also be the result of the cumulative effect of age-related periodontal changes and peak occurrence of IBD. A study with equal group distribution of patients for each age group should be able to address this.
Smoking is an established risk factor for periodontitis and tends to increase the prevalence and severity of the disease (Bergström et al., 2000;Haber et al., 1993;Kibayashi et al., 2007;Linden & Mullally, 1994;Tomar & Asma, 2000;Van Winkelhoff et al., 2001). The results of the present study did not have the same finding. This could be because the smoking group comprised both past smokers and current smokers.
It is well established that the number of years of smoking and years of cessation are crucial elements in determining the effects of smoking on developing periodontitis. The negative effects of smoking can be observed for up to 11 years following cessation (Tomar & Asma, 2000). There is also an established dose-response between how many cigarettes per day were being consumed and disease T A B L E 7 Odds ratio in different age groups Group 2 versus Group 1 = 1.00 Group 3 versus Group 1 = 11.10 Group 4 versus Group 1 = 8.00 Group 5 versus Group 1 = 2.44 severity (Tomar & Asma, 2000). These correlations were not observed in our study. Due to the nature of the study, years of cessation and years of smoking, as well as the number of cigarettes could not be taken into consideration. Thus, there was expected variability in periodontal disease presentation.
We also attempted to assess oral hygiene adherence with the odds of developing periodontitis. We used the plaque score as proxy as this was a retrospective study. We did not observe an effect of plaque on the rates of periodontitis in IBD-affected individuals. It should be noted that the plaque score might not be a good indicator. If oral hygiene adherence were to be recorded in person using standardized established questionnaires, it would have been assessed differently. This was not possible in this retrospective chart review (Oral Health Questionnaire, 2020).
There was no significant difference in periodontitis incidence in patients with UC versus CD. Therefore, it can be derived that although the clinical presentation of CD and UC vary in terms of periodontitis, there is no variation between these two forms. This could be explained by the fact that both forms of IBD share the common pathogenesis with periodontitis and thus no difference in prevalence of periodontitis was seen in the present analysis.

| Limitations
The present study had a few limitations. The first and foremost being the nature of the study design. Retrospective data mining limited the review of patient charts, since the data available were not originally designed to collect information for research conducted. This also limited the number of patient records included, since incomplete patient chart records with missing baseline data were excluded from the study. Secondly, there was a variation in sample size in subgroups, especially in age groups.

| CONCLUSION
The key finding of this study is that patients in the 50-64 years age group with IBD have significantly greater odds of developing periodontitis. Since age has a significant effect on IBD-affected individuals in developing periodontitis and its severity, it is advised to keep them under regular recall for early diagnosis and maintenance.
No sex predilection for periodontitis in patients presenting with IBD was seen. The present study did not state increased odds of periodontitis in patients with IBD with a smoking history. When oral hygiene adherence was assessed in the present study, it did not affect the occurrence of periodontitis in patients presenting with IBD.
However, since plaque is an etiological factor in periodontitis, plaque control regimes should be encouraged. Although there is a variation in the clinical presentation of UC and CD, the prevalence of periodontitis did not differ between UC and CD. Patients who have either UC or CD should be examined with the same assessment measures for determining their regime for periodontal care. Since the increased prevalence of periodontitis was seen in IBD, it is advised for gastroenterologists to collaborate with periodontists and possibly other dental professionals to ensure periodontal health is maintained in IBD-affected individuals.

AUTHOR CONTRIBUTIONS
Nazia Abrol: contributed to conception, design, data acquisition, and interpretation, performed all statistical analyses, drafted, and critically revised the manuscript. Monica P. Gibson: contributed to conception, design, data acquisition, and interpretation, drafted, and critically revised the manuscript. Sharon M. Compton: contributed to data acquisition and critically revised the manuscript. Daniel Graf, Pallavi Parashar, and Giseon Heo: contributed to data acquisition and critically revised the manuscript. All authors gave final approval and agree to be accountable for all aspects of the work.

This project was funded by a Network for Canadian Oral Health
Research (NCOHR) New Frontier Seed Grant.