Type 1 Diabetes Mellitus Patients' Self-perception of Periodontal Diseases

Abstract Objectives  The study aimed to evaluate type 1 diabetes mellitus (T1DM) patients' self-perceived periodontal health status and to identify the association between periodontal disease (PD) and DM. Materials and Methods  This cross-sectional study included 113 T1DM children between 3 and 18 years old from the Universiti Teknologi MARA and the University of Malaya. Periodontal health parameters, including plaque index, gingival index, probing pocket depth, simplified basic periodontal examination, and clinical attachment loss, were recorded. Self-perceived periodontal health status was assessed with questionnaires. Statistical Analysis  Statistical analysis was performed to evaluate the sensitivity of the questionnaire and the relationship between T1DM and periodontal parameters. Results  The median age was 11.4 years. Half of them (50.4%) were females. A total of 83.5% rated their oral condition as good, whereas 27.5% reported a history of gingival bleeding. Clinical examination revealed that 48.7% had healthy gingiva, whereas 47.8% had gingivitis. The question “Do you have bleeding when brushing, flossing, or eating food?” showed good accuracy in the evaluation of PD ( p  < 0.001). Conclusion  The questionnaire has a high potential to be used by medical professionals in identifying T1DM patients at risk of PD to guide nondental health care providers in making appropriate referrals to dental services.


Introduction
Diabetes mellitus (DM) is a metabolic disease characterized by the dysregulation of carbohydrate metabolism.It commonly manifests as hyperglycemia due to diminished insulin secretion, impaired insulin action, or both. 1 Type 1 diabetes mellitus (T1DM) makes up 5 to 10% of all DM cases worldwide. 2The disease stems from cell-mediated autoimmune destruction of the pancreatic β-cells that produce insulin.Depending on the degree of β-cell destruction, T1DM patients can experience reduced or absence of insulin secretion, as indicated by low or negligible levels of plasma C-peptide.The chronic hyperglycemic status can lead to long-term damage, dysfunction, and failure of different organs in DM patients, especially the eyes, kidneys, nerves, heart, and blood vessels. 3Treatment modalities for T1DM include subcutaneous injections of insulin, maintenance of a healthy diet, and regular exercise. 4eriodontal disease (PD) is a condition resulting from the infection and inflammation of the tooth-supporting tissues. 5n the early stages of the disease, gingival inflammation may cause the gingival tissues to appear erythematous, or edematous, and potentially result in bleeding.Worse, gingivitis can progress into periodontitis that presents as attachment loss, alveolar bone resorption, and tooth mobility. 6PD is one of the most common causes of tooth loss. 7DM is associated with an increase in the prevalence, severity, and progression of periodontitis. 8,9DM patients are three times more likely to suffer from periodontitis as compared with nondiabetics. 10urthermore, 10% of children with T1DM were reported to have higher rates of attachment loss and bone loss compared with their nondiabetic peers despite having comparable plaques score. 11Moreover, a recent study showed that children with DM have twice the number of periodontal sites that eventually developed into periodontitis as compared with non-DM children. 12he bidirectional association between DM and PD has been established in previous literature. 13,14DM is known as one of the modifying factors of periodontitis that can accelerate the progress of PD 14 as DM can impair the periodontal tissue growth and matrix formation with fibroblasts, osteoblasts, and osteoclasts. 15,16In addition, increased thickness of the gingival basement membrane in DM patients could also impair the vasculature of the periodontal tissues. 17,18It has also been postulated that DM complicates PD by tipping the balance of oral microbiota, resulting in the dominance of periodontal pathogens. 19,20However, more in-depth studies are needed to ascertain the differences in the biofilm of diabetics and nondiabetics.The latest evidence indicated that chronic inflammation in PD can aggravate complications of DM by worsening glycemic control.
The American Dental Association recommendation for diabetic patients is to receive medical follow-up on a 3-monthly basis. 21During these visits, evaluation of hemoglobin A1c (HbA1c) and reassessment of diabetes management are recommended.However, T1DM patients with unsatisfactory glycemic control should be arranged for more frequent follow-ups to enhance their adherence to the treatment regime.During this quarterly visit, T1DM patients would be able to obtain the maximum benefits from the other multidisciplinary team of specialists, thus reinforcing good self-care practices, such as routine dental visit. 22,23Apart from having known risk of PD, poor oral hygiene was observed in youngsters with T1DM especially those with uncontrolled HbA1c, which eventually could increase the risk of future oral disease(s). 24n 2020, a study by Moore et al on professional health care workers in pediatric diabetes care teams showed that 76.2% of them were aware that periodontitis is a possible complication of diabetes.However, in 2022 Siddiqi and Zafar recorded a contradicting finding in which they found that the majority of medical practitioners (89%) were aware of the bidirectional association and knew that the glycemic index of patients with DM and suffering PDs could be improved by providing periodontal therapy. 25However, as low as 4.8% had received training in recognizing patients who require dental care.This study reinforced the need for further training in this area to provide holistic care to DM patients. 26,27There is an urgent need for accurate and reliable means of surveillance, detection, and diagnosis of periodontitis among children suffering from T1DM.In addition to that, referral to dental care professionals for appropriate and timely management is crucial, therefore appropriate screening tools for medical professionals to initiate referral of patients with DM is needed. 28Hence, it is vital to establish an effective system for nondental health providers to identify individuals in need of dental care. 29However, with limited resources available for regular screening and timely examination by dental practitioners, other options should be explored.
In 2022, a study by Mohd Said from Malaysia recommended the use of validated simplified digital periodontal health screening software for identification of PD at early stage in dental practice. 30This identification tool appeared simple and appropriate to be used for screening of PDs.This showed an effort have been made to initiate the link from the general dental practice to specialist care.Nevertheless, the initiation from the medical practitioner has yet to be established.Hence, there is a need of questionnaires is of detecting populations at risk of oral diseases, which can be initiated from the medical professionals.On top of that, the accuracy and effectiveness of using a questionnaire when compared with the clinical examination ranged from moderate to high in various studies, thus indicating its potential to be can be administered to instil awareness, facilitate early detection, and predict the disease. 31Therefore, in this context, a selfself-reported perception and the clinical parameters could contribute to the prevention and earlier diagnosis of PD, especially in individuals requiring complex clinical care. 32herefore, the use of adapted self-report measures for PD can be considered a low-cost alternative for the early detection and prevention of PD in DM patients.It can be beneficial for epidemiological studies and population surveillance of the periodontal condition. 33This study aimed to compare the selfperceived periodontal health status using a guided questionnaire (GQ) with the clinical measurement by dental professionals among children and adolescents with T1DM.The study also set out to determine if the GQ is a valid tool to be used by nondental professionals to evaluate periodontal health status.

Materials and Methods
This two-part study was a cross-sectional study conducted from October 2020 to May 2022 at two centers, Universiti Teknologi MARA (UiTM), Selangor, and the University of Malaya (UM), Kuala Lumpur.Content validity index for item (I-CVI) and face validity was conducted to validate the questionnaire.A reliability study of 20 participants and intraexaminer training and calibration was performed prior to the study.
All children and adolescents below 18 years old with T1DM diagnosis at UM and UiTM were invited to participate in the study.They must be able to communicate in English and or Bahasa Melayu.However, those undergoing active orthodontic therapy or using any antibiotics or medications in the last 3 months that might cause gingival alteration, such as drug-induced gingival enlargement, were excluded.
The sample size was determined using Epi-Info StatCal software based on the total number of the eligible T1DM patient (n ¼ 166) 34 and the prevalence of diabetes test knowledge was 50.4% (11.6/23Â 100). 35Considering an attrition rate of 10% with a 95% confidence level and an acceptable margin of error of 5.6%, the final sample calculated was 118 (108 þ 10%).A total of 113 T1DM patients were recruited.The participants and their parent(s) or caregiver(s) answered the questionnaire during their follow-ups.The questionnaire would be answered by parents of children below 16 years old.Subsequent appointments were arranged for the participants to undergo a dental examination.

Definition Body Mass Index
Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared, i.e., BMI ¼ weight (kg)/ height2 (m 2 ).The calculated BMI was plotted on the Centers for Diseases and Prevention (CDC) BMI-to-age chart for the respective gender 36 (►Table 1).

Blood Pressure
In this study, blood pressure (BP) was reported as systolic (SBP) and diastolic (DBP) percentiles for age/sex/height.The classification is based on the individual's age plotted against the percentile of height in SBP or DBP (mm Hg) of the respective gender. 37The height percentile was obtained using the CDC height-for-age percentile of the respective gender.Based on American Academy of Pediatrics, BP categories and stages are as follows 38 (►Table 2).

Lipid Profile
According to the International Society for Pediatrics and Adolescent Diabetes and the American Diabetes Association recommended low-density lipoprotein cholesterol (LDL-C) of < 100 mg/dL (2.6 mmol/L) in youth with DM. 39 High-density lipoprotein cholesterol (HDL-C), total cholesterol, triglycerides can be categorized according to NHLBI 2011. 40

Hemoglobin A1c
HbA1c is a glycoprotein formed by a direct reaction between blood glucose and hemoglobin.It is routinely in clinical research and clinical practice to evaluate diabetes control.For children, adolescents, and young adults 25 years old.With access to comprehensive care, HbA1c of < 53 mmol/dL (7.0%) is recommended. 41

Study Instrument
Guided Questionnaire Self-reported questionnaires adopted from two recent studies were translated and validated to be used in this study. 42,43he GQ consisted of 14 items with 8 items on patients' baseline characteristics (Part A) and 6 items on symptoms of PD (Part B).The GQ was used to screen for any PD comorbidity among the study participants.

Simplified Basic Periodontal Examination
The simplified basic periodontal examination (sBPE) codes formed the basis of the assessment for patients under 18 years old.The examined teeth included one tooth from each sextant, i.e., the upper right six (tooth 16), the upper right one (tooth 11), upper left six (tooth 26), lower left six (tooth 36), lower left one (tooth 31), and lower right six (tooth 46).The WHO 621 probe with a light probing force of 20 to 25 g was used for this assessment.The sBPE codes were as follows: 0, healthy; 1, bleeding on gentle probing; 2, calculus present and/or plaque retention factors; 3, the presence of 4-to 5-mm pocket; and 4, the presence of 6 mm or more pocket; and Ã , furcation. 44n children between 12 and 17 years with erupted permanent teeth, the full range of sBPE codes (0-4) was used.For children aged between 7 and 11 years with mixed dentition, the sBPE codes 0,1, and 2 were used.In the full primary dentition, sBPE similar to the one used for children as young as 3 years of age was performed. 45Apart from that, plaque index (PI) 46 and gingival index (GI) 47 were also assessed.

Statistical Analysis
Data analysis was performed using the Statistical Package for the Social Sciences Version 20.0.Association between the GQ and the clinical examination was assessed using the Pearson chi-square test and Fisher's exact test.A p-value < 0.05 was considered statistically significant.Diagnostic tests (sensitivity, specificity, accuracy, positive predictive value, negative predictive value, and receiving operating characteristic curve) were performed to measure the performance of each question with the basic periodontal examination (BPE) as the reference for the periodontal evaluation.For this purpose, the periodontal status was dichotomized as "0" for healthy and "1 and above" for having PD.

Results
Questionnaire I-CVI value 0.96 indicate high value of all items.And, following changes made based on expert opinion, a good face validation could be seen.Intraexaminer training and calibration (intraclass correlation coefficient revealed a good value of 85%) with acceptable reliability Cronbach's α of 0.77.►Table 3 outlines the sociodemographic, clinical parameters, and oral hygiene care characteristics of the participants.From the 113 participants, 24.8% (n ¼ 28) presented with stage 1 hypertension, whereas another 18.6%Further analysis revealed that 40.9 and 53.8% of participants with healthy BMI exhibited high LDL-C and low HDL-C, respectively (►Table 4).In addition, uncontrolled HbA1c was observed among 91.2% of participants despite normal BMI.A higher percentage of uncontrolled HbA1c was also reported among participants with acceptable LDL-C (87.5%), acceptable HDL-C (90.7%), and less than 5 years of DM (90.9%).However, all these associations were not statistically significant (p > 0.05) (►Table 5).
►Table 6 shows that 27.5% of participants who reported bleeding from gingiva upon brushing, flossing, and eating were found to have BPE during the clinical examination.This finding indicated a high sensitivity (50%) and specificity of the questionnaire (94.5%).In addition, 90% of T1DM presented with gingival bleeding were at risk of having PD (p < 0.001).
As presented in ►Table 7, the mean PI and GI were 0.37 AE 0.31 and 0.27 AE 0.32, respectively.In other words, 48.7% of the participants had healthy periodontal status.Among 47.8% of participants with unhealthy gingiva, 7% of them were found to have periodontitis.

Discussion
PD is the sixth most common complication among DM patients. 48As T1DM patients face an increased risk of PD, 49 it is vital to improve the awareness of medical professionals and patients on the prevention and identification of oral diseases.Medical-dental coordinated care needs to be strengthened for this purpose.The use of self-reported questionnaires can increase T1DM patients' awareness and self-perception of oral diseases.During most medical consultations, physicians and other nonoral health professionals often overlook the need for oral clinical examination. 32ence, the use of a self-reported questionnaire can also evoke their attention to DM patients at risk of PD.Following that, health care providers can refer the patients to a dentist for further management to prevent oral diseases. 50n this study, it was found that respondents who answered "yes" to the question "Do you have bleeding when brushing, flossing, or eating food?" were associated with a high score of BPE compared with those who answered "no."The sum of sensitivity plus specificity for this item was 144%, which is considered as a "good validity." 33Agreed by study in Japan population, inclusion of the question on gum bleeding would improve the predictive performance of the questionnaire as it is less confusing than other items. 51This finding also echoed a few other studies in which the term gum bleeding should be used rather than gingivitis when interacting with patients [52][53][54] as not all may be familiar with the dental term of gingivitis, especially children and adolescents.In addition, Elhassan et al (2017) also suggested that patients could relate to bleeding better than the appearance of swollen gum. 55ccording to the Nelson's validity classification, self-reported PD (painful gums, tooth mobility, and people's opinions whether they have gums disease) can be classified as having moderate to high validity. 33,56However, in our study, the items "Do you think you have gum disease," "Swelling, red, or painful gums for no apparent reason," and "Loosening or shifting of teeth in the affected area" were found to have low sensitivity of 16.7, 13, and 3%, respectively.The reason probably due to this set of questionnaire has good predictive ability for periodontitis, especially in the severe cases rather than gingivitis alone, as only 3.5% patients in our study presented with periodontitis. 51Supported by one study where the prevalence of periodontitis is high, the predictive performance of similar self-reported questions presented reported to be more accurate. 57n this study, the questionnaire on the perception of oral health for participants aged less than 16 years old (72.6%) was answered by their parents or caregiver.With a low sensitivity (18.7%) and high specificity (86%), it can be Type 1 Diabetes Mellitus Patients' Self-perception of Periodontal Diseases Abidin et al.
regarded as having parents may have good perception of the child's oral health rather than poor perception.9][60][61] In addition, parental perceptions of oral health are often dependent on clinical conditions with recognizable symptoms, such as dental caries with toothache rather than other less obvious oral conditions such as gum problems, malocclusion, or dental trauma. 62Similarly, in an earlier study by Cyrino et al (2011), the patient's perception of health was found to be better than the actual presentation of the disease. 63The remaining 27.4% of the questionnaire answered by 16-and17-year-olds showed slightly higher sensitivity (27.3%) and specificity (100%).More studies reported that younger individuals may not be able to identify PD. 32,64 However, contradicting to the statement, adult age more than 60 were less likely to report gingival bleeding symptom correctly compared with less than 40 years old, which probably due to more serious manifestation occur rather than gingival bleeding. 65ccording to a new classification of PD, 3.5% or four patients in this study had periodontitis. 66All four participants answered "yes" for gum bleeding even though only three of them claimed that they have gum disease.One of them with an advanced stage  Type 1 Diabetes Mellitus Patients' Self-perception of Periodontal Diseases Abidin et al.
(stage III) of gum disease answered "yes" to people's opinions on whether they have gum disease.The individual also answered "yes" for bad gum condition, painful swollen gums, and tooth mobility.This means that, our findings agree that more value was seen pertaining to self-reported PD if severe stage periodontitis was encountered. 67Thus, this questionnaire would be able to exclude healthy individuals from periodontal clinical examination at a cheaper cost and would be an alternative of gold standard periodontal examination in cost-limited epidemiology survey. 68More importantly, this can expedite the early diagnosis and treatment of PD.The HbA1c of most participants showed uncontrolled T1DM as many of them did not achieve the target HbA1c of < 53 mmol/mol (<7.0%) for children and adolescents who have access to comprehensive care. 41In this study, almost half of the patients were diagnosed with gingivitis (47.8%).However, there was no significant association between HbA1c and gingivitis (p ¼ 0.271).In contrast, a significant correlation was detected between PI and sBPE (p < 0.00).This shows that periodontal condition was more associated with the presence of visible plaque rather than the underlying metabolic status.According to a recent study, HbA1c in children and adolescent has a low correlation with the gingival condition compared with adult DM patients. 69ven though the prevalence of T1DM in children and adolescents is increasing, 70 we faced certain challenges in recruiting eligible patients during the pandemic in view of limited follow-up appointments available during the lockdown period.Furthermore, more than 10 patients or their parents declined to participate.

Conclusion
This study concluded that the GQ has a high potential to be used in identifying T1DM children at a greater risk for PD and in need of an oral examination.It can be adopted as a tool for nondental health care providers to screen for PD before making appropriate dental referrals for the patients.In the long term this will ensure a seamless and coordinated care pathway for DM patients requiring dental care

Table 1
Body Mass Index classification Abbreviation: BMI, body mass index.

Table 3
Sociodemographic, clinical parameters, and oral hygiene care of participants Type 1 Diabetes Mellitus Patients' Self-perception of Periodontal Diseases Abidin et al.
European Journal of Dentistry © 2023.The Author(s).

Table 4
Association between low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, and body mass index

Table 5
Association between selected variables and hemoglobin A1c European Journal of Dentistry © 2023.The Author(s).

Table 6
Frequency of responses for periodontal health questionnaire and diagnostic tests for each question in relation to simplified basic periodontal examination : ACC, accuracy in percentage; AUC, area under the curve; NPV, negative predictive value in percentage; PPV, positive predictive value in percentage; SP, specificity in percentage; SS, sensitivity in percentage. Abbreviations

Table 7
Ethical Approval StatementEthical approval was obtained from the Research Ethics Committee of UiTM (REC/07/2020(MR/169) and from Medical Ethics Committee, Faculty of Dentistry, UM (DF RD2018/0110 (L).UiTM Research Ethics Committee and Medical Ethics Committee, UM operates in accordance with the International Council for Harmonization Good Clinical Practice Guidelines, Malaysia Good Clinical Practice Guidelines, and the Declaration of Helsinki.Written informed consent was obtained from the parents and assent was obtained from the child for participation and for the purpose of publication.The research was performed in accordance with a named standard.Clinical parameters of the periodontal health status of participants Type 1 Diabetes Mellitus Patients' Self-perception of Periodontal Diseases Abidin et al.
European Journal of Dentistry © 2023.The Author(s).