Alveolar Bone Loss in Diabetic Patients: A Case–Control Study

Abstract Objectives  Based on literature, very few case–control studies have been executed to confirm the relationship between diabetes mellitus and the severity of mean alveolar bone loss. Therefore, the aim was to assess the differences in mean alveolar bone loss among diabetic (type 2) and nondiabetic patients in the Saudi population. Materials and Methods  Nine-hundred eighty-two patient records were seen in this retrospective study. Patient demographic data and medical records were examined. The mean alveolar bone loss was measured in posterior teeth by calculating the distance from the base of cementoenamel junction to the alveolar crest using the bitewing radiographs. SPSS 20.0 was used for data analysis. An unpaired t -test was utilized to analyze the mean alveolar bone loss across multiple variables. p -Value less than or equal to 0.05 was contemplated as significant. Results  The overall mean alveolar bone loss for all 124 patients was 2.83 ± 1.13 mm. Diabetic patients had greater mean alveolar bone loss measured in millimeters than nondiabetic patients (3.07 ± 1.14mm vs. 2.59 ± 1.08mm, respectively), and the difference was significant ( p  = 0.018). In terms of the severity of mean alveolar bone loss, diabetic patients experience statistically higher mean alveolar bone loss as compared with nondiabetic patients. Conclusion  In our study population, the overall mean alveolar bone loss prevalence was greater in diabetes patients than in nondiabetic individuals. According to the severity of bone loss, the distribution of moderate and severe periodontitis was higher in diabetic patients. To enhance patients' quality of life, the awareness and education among patients regarding the association among diabetes mellitus and oral health, particularly periodontal disease, should be promoted.

Introduction linked to several oral health-related disorders, including periodontal disease (PD), xerostomia, halitosis, fungal infections, and oral mucosal lesions. 3,8,9 PD is an oral infection that is distinguished by the loss of alveolar bone support around teeth. 10,11 Severe periodontitis can lead to tooth loss and affects approximately 5 to 20% of the world's adult population. The association between DM and periodontitis has been reported in the literature. [12][13][14] DM is linked to alveolar bone loss and is known as a risk factor for PD. 15 A higher clinical attachment loss (CAL), alveolar bone loss, a greater percentage of furcation lesions and tooth mobility are correlated with diabetes. [14][15][16] Persistent hyperglycemia causes extravagant immune responses in the presence of periodontal pathogens and is expected to be accountable for the increased risk and severity of alveolar hone loss in diabetic patients. 17,18 Diabetes has a significant impact on osteoclastogenesis and increases osteoblast apoptosis. 19 Nevertheless, a bidirectional relationship has been reported between periodontitis and DM. 20 PD negatively affects the glycemic control of the patients and it has been reported that host-derived inflammatory mediators released due to increasing bacterial load in PD play a vital role. 15 Furthermore, Heji et al reported that periodontal examination findings can help to identify patients at risk of undiagnosed diabetes or prediabetes. 21 By performing a comprehensive radiographic and periodontal examination, dental practitioners can identify patients who have a risk factor for diabetes, particularly if they have a family history of diabetes, and earlier referral to the medical can be established. This relationship must be understood not only by dentists but also by physicians who work to improve the lifestyle and well-being of diabetic patients. Matrooshi et al demonstrated that, despite having good knowledge, physicians seldom refer diabetic patients for appropriate periodontal care. 22 Based on the literature, very few case-control studies have been executed to confirm the relationship between DM and the severity of mean alveolar bone loss (MABL). Furthermore, no such study has been conducted in Saudi Arabia's Eastern province. There is a substantial need to investigate the differences in MABL among diabetic and nondiabetic individuals. This study aimed to evaluate the mean differences in alveolar bone loss among diabetic (type 2) and nondiabetic patients in the Saudi population.

Ethical Approval
Ethical approval for this retrospective study was acquired from the Institutional review board of Imam Abdulrahman bin Faisal University (IAU), Dammam, Saudi Arabia (IRB approval number: IRB:2020-02-109). This study was conducted according to the Helsinki Declaration guidelines.

Patient Selection
The College of Dentistry, IAU, database was searched for patients who had a clinic visit in the last 3 years. Inclusion criteria for patient records were availability of complete intra, extraoral, and radiographic examinations of the patient.

Inclusion Criteria
Patient inclusion criteria for this study were (1) patient age (18 years old or older), (2) complete medical and dental records of the patients, and (3) Bitewing (BW) radiographs of the patients.

Exclusion Criteria
Following were the study's patient exclusion criteria: (1) patients with an incomplete medical history, (2) the patient's whose BW radiographs were missing, and (3) patients who did not have at least two adjacent teeth or whose interproximal space between teeth was narrow, and the crest of the bone was not visible. The information gathered includes the patient's age, gender, medical history, nationality, and radiographs.

Radiographic Examination
In this study, BW radiographs were utilized to assess MABL. The BW radiographs were used to reduce angular distortion. Alveolar bone loss was calculated on the mesial and distal surfaces of the mandibular and maxillary posterior teeth using ImageJ software (Wayne Rasband, version 1.47, National Institutes of Health, Bethesda, Maryland, United States). Mean of mesial and distal bone loss was calculated and used for further analysis as MABL. All of the measurements were standardized using a radiograph of an implant of known diameter as a reference.
To calculate alveolar bone loss, a line was drafted along the long axis of tooth on the mesial and distal sides from apical part of the cementoenamel junction (CEJ) to the top of the alveolar crest (►Fig. 1). A distance greater than or equal to 2 mm between the CEJ and the alveolar crest was contemplated as a radiographic sign of interproximal bone loss. [13][14][15]17 The severity was categorized based on case definition by task force classification from the American Academy of Periodontology into normal (MABL< 2mm), mild (MABL >2mm 3mm), moderate (MABL >3mm 5mm), and severe periodontitis (MABL >5mm). 13 All the BW radiographs were examined in a dark room for accurate measurements. The convenient sample size was considered for this study.
Statistical Analysis SPSS 20.0 was used for data analysis (IBM product, Chicago, Illinois, United States). Gender, nationality, and age were among the categorical variables that were provided as frequencies and percentages. Age and bone loss measurements were included in the numerical data, which were displayed as mean standard deviation. Unpaired t-test was used to compare the MABL in different groups of teeth and maxilla versus mandible between diabetic patients and nondiabetic individuals. To evaluate effect of categorical variables, the MABL was compared in relation to gender, nationality, and age between the groups by employing unpaired t-test. A p-value less than or equal to 0.05 was considered significant.

Results
The 982 patient records were examined and out of which 264 were excluded due to incomplete records. Seven-hundred eighteen records were examined and only 62 of these individuals, as indicated by their medical histories, had type 2 DM (►Fig. 2). Patients in the control group (n ¼ 62) were chosen randomly from age and gender-matched computer-generated table with no prior history of DM. The secondary matching criterion was nationality. The average age of all the patients was 48.02 AE 12.90. In the diabetic group, there were 40 Saudi (67%) and 22 non-Saudi nationals (33%). The patients' average age was 48.21 AE 13.03 years. There were 44 Saudi (71%) and 18 non-Saudi nationals (29%) in the control group. The patients' average age was 47. 8 12.9 years. In both diabetic and control groups, there was 42 male (67.7%) versus 20 female patients (32.3%).
The overall MABL for all 124 patients was 2.83 AE 1.13 mm. Diabetic patients had greater MABL loss measured in millimeters than nondiabetic patients (3.07 AE 1.14 mm vs. 2.59 AE 1.08mm, respectively), and the difference was significant (p ¼ 0.018). In terms of the severity of MABL, diabetic patients experience statistically higher bone loss compared with nondiabetic patients. ►Table 1 represents the variations in MABL based on severity among diabetic and nondiabetic patients. The average prevalence of MABL was significantly greater in diabetic (85.5%) than nondiabetic patients (71%).
The MABL in various groups of teeth in diabetic patients versus nondiabetic patients is shown in ►Fig. 3A and ►Table 2.
There was a significantly greater MABL in both premolar (p ¼ 0.039) and molar (p ¼ 0.003) groups of teeth in diabetic versus nondiabetic subjects. When the teeth were divided into groups of maxillary and mandibular teeth, a statistically significant difference was observed showing that diabetic patients had a higher MABL in both the maxilla (p ¼ 0.002) and the mandible (p ¼ 0.006) (►Fig. 3B). Gender-wise differences in overall MABL among the diabetic and nondiabetic individuals were found to be significant for male patients, but nonsignificant for female patients (►Table 3). Age-wise differences in MABL among the diabetic and nondiabetic individuals were found to be higher for diabetic patients in both age groups; however, statistically it was determined to be nonsignificant (►Table 3). Furthermore, nationality-wise differences of mean bone loss among the diabetic and nondiabetic patients were higher in the Saudi diabetic population; however, the differences were observed to be nonsignificant (►Table 3).

Discussion
This study found a link between type 2 diabetes and MABL in a cohesive study population. This relationship remained consistent regardless of the severity of mean alveolar bone loss, its prevalence, site (maxilla or mandible), or position of the teeth. Gender, age, and ethnicity statistical analyses were performed in this study to account for the effect of age, gender, and ethnicity. This allowed for a more accurate assessment of the relationship between MABL and type 2 diabetes compared with nondiabetic subjects.
In this study, a case-control study design was used due to its distinct advantages over other study designs. Case-control studies are relatively reliable and low cost. The controls were chosen with age and gender as primary matching criteria and nationality as a secondary matching criterion' between the test and control groups. Marginal bone loss was    assessed using BW radiographs. Other diagnostic tools, such as periapical and panoramic radiographs, have been used to detect bone loss, but they provide limited diagnostic information. Several studies have confirmed that BW radiography is still the most effective diagnostic radiography for crestal bone examination. 23,24 It is a faster, less expensive method with a lower radiation dose.
Our findings are consistent with previous research. Diabetes is a known risk factor for PD. PD is common (34-68%) in diabetic patients, as well as increased pocket probing depths and CAL. 25,26 Patients whose glycemic control is poor have a higher risk of PD compared with healthy individuals. 27 Periodontitis is considered a sixth oral manifestation of diabetes. 15 In addition, diabetic patients have a greater susceptibility to periodontitis development and advancement in comparison to healthy individuals. 28,29 Antibodies produced against microorganisms in periodontal tissues and predisposing genetic factors lay the foundation for an autoimmune role in PD pathogenesis. 30 Diabetes causes autoimmunity because of a breakdown in the normal defense process caused by by-products of tissue breakdown and chronic infection. PD and diabetes are linked epidemiologically because both conditions have autoimmune components. 31 Because PD and diabetes have a bidirectional relationship, proper periodontal care can improve metabolic control in DM patients. 32 The results of a meta-analysis that included nine randomized clinical trials confirmed the effectiveness of nonsurgical periodontal therapy in glycemic control and a moderate decrease in hemoglobin A1c among diabetic patients was observed. 33 Concerning the severity and prevalence of MABL, this study showed that 50 and 45.2% of participants had mild, 16.1 and 33.8% had moderate, and only 4.8 and 6.5% had severe mean alveolar bone loss among nondiabetic and diabetic individuals, respectively. Correspondingly, Zahid et al observed a prevalence of mild, moderate, and severe alveolar bone loss comparable to our results, that is, 57.4% of the participants with mild, 36.6% moderate, and 4.95% severe alveolar bone loss. 34 Furthermore, the nationality-wise differences in overall mean bone loss among diabetic and nondiabetic patients were higher in Saudi diabetic patients, but the differences were not significant. The non-Saudis nationals were mainly from Pakistan, India, Bangladesh, and Philippines. Delgado-Angulo et al discovered a complex link between ethnicity, socioeconomic status, and PD. 35 The role of variables in determining ethnic disparities in oral health, however, has not been assessed. 35 Further research should be conducted to examine the comparative roles of various factors that might aid in identifying variables which are more appealing to take necessary actions to reduce ethnic disparities in adult oral health care. 35 The gender-related differences in mean alveolar bone loss among diabetic and nondiabetic patients were found to be significant for male patients but nonsignificant for female patients in this study. These findings are consistent with previous research that found males to be more likely to suffer from alveolar bone loss or periodontitis. 14,40 The causes of these gender differences are unknown; however, they may be related to males' poor compliance with oral hygiene practices. 43,44 Our study's limitations were that our sample size was relatively small and the fact that we only studied patients who visited a single dental hospital. As a result, future multicenter studies should be conducted, with a larger study population. In addition, the relationship between clinical parameters of periodontitis such as periodontal probing depth (PPD) and CAL was not investigated in this study. More research is needed to determine the relationship between clinical parameters (PPD and CAL), DM severity, and radiographic alveolar crestal bone loss.

Conclusion
In our study population, the overall mean alveolar bone loss prevalence was greater in diabetic patients than in nondiabetic individuals. According to the severity of bone loss, the distribution of moderate and severe alveolar bone loss was higher in diabetic as compared with nondiabetic patients. Oral complications of DM are numerous and alveolar bone loss or PD is one of them. It is possible to avoid PD and enhance patients' quality of life by raising awareness and education among patients regarding the relationship between DM and oral health. Diabetic patients should be motivated to practice good oral hygiene and manage their blood sugar levels appropriately to prevent oral problems.