23 Original ISSN 2413-0516 J Contemp Med Sci | Vol. 7, No. 1, January-February 2021: 23 – 27 Introduction Chronic kidney disease (CKD) is a systemic condition that adversely affects the patient’s quality of life. If left untreated, it can progress to advanced stages, which are associated with high morbidity and mortality. The American Society of Nephrology defined CKD and classified it into five stages based on the glomerular filtration rate (GFR).1-3 Given the increasing prevalence of CKD, there are ongo- ing attempts to identify and control the associated risk factors such as obesity, malnutrition, hypertension, diabetes mellitus, as well as periodontal diseases. Such attempts are imperative to decrease the burden of disease on CKD affected patients.4-7 It has been suggested that periodontitis was a potential independent risk factor for CKD.8 By definition, periodon- titis is a chronic inflammatory condition that causes peri- odontal tissue destruction. It often occurs due to poor oral hygiene, microbial plaque, and calculus accumulation around the tooth surface causing subsequent gingival inflammation, periodontal pocket formation, and loss of tooth support- ing structures.9 In this case, the local inflammatory factors and C-reactive protein (CRP) pass through the affected gin- giva into the peripheral blood circulation and exert systemic effects.4,10 Continuation of this process in CKD patients can aggravate their disease condition and even it may lead to renal failure if left untreated. Based on a cross-sectional study, a mutual correlation was reported between periodontal diseases and CKD.11 Likewise, such correlations have been assumed between periodontal diseases and a number of other systemic conditions such as cardiovascular diseases, diabetes mellitus, osteoporosis, respiratory diseases, rheumatoid arthritis, low birth weight, and immature birth.4,12-19 In general, periodon- titis is a multifactorial disease, and therefore, several factors are affecting the susceptibility and development of periodon- tal diseases.20,21 The prevalence of periodontal disease has been reported 57% in CKD patients.22 Thus, considering the role of periodontitis on systemic conditions, the purpose of this study was to assess the correlation between periodontal diseases and CKD duration. Materials and Methods This descriptive cross-sectional study was approved by the regional Research Ethics Committee with reference number “IR.SBMU.RIBS.REC.1394.170” and performed in complete accordance with the Declaration of Helsinki. Participation in this study was voluntary and written informed consent was obtained from all subjects. After explanation of the study objectives, potential questions were answered by the lead author. Likewise, oral examination was conducted by a sin- gle calibrated examiner (lead author) prior to their hospital appointments. A convenient sampling technique was used to recruit CKD adult patients who attended the “Labbafinejad Hospital” in Tehran city during 2017. For sample size calcula- tion, we used the reported prevalence (57%) with 95% confi- dence level, and 7% margin of error. Based on this calculation, at least 192 cases were needed for conducting this study. Two instruments were used for data collection in this project. The first questionnaire assessed the oral health behav- ior of CKD patients and it was a self-reported questionnaire. The second questionnaire was a standard WHO instrument which was used for clinical evaluation of the oral health sta- tus of CKD patients. Likewise, WHO recommended meth- odology was used for oral examination in order to determine the decayed, missing, and filled teeth (DMFT) in our sample population. For gingival health status, we used the clinical Periodontal and chronic kidney diseases: A modifiable association Foujan Jabbarzadehkhoei1, Soheila Bakhshandeh2, Mahshid Namdari2, Mina Pakkhesal3, Mohammad Hossein Khoshnevisan2,4* 1 School of Dentistry, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 2 Community Oral Health Department, School of Dentistry, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 3 Community Oral Health Department, School of Dentistry, Golestan University of Medical Sciences, Gorgan, Iran. 4 Dental Research Center, Research Institute of Dental Sciences, School of Dentistry, Shahid Beheshti University of Medical Sciences, Tehran, Iran. *Correspondence to: Mohammad Hossein Khoshnevisan (E-mail: khoshmh@gmail.com) (Submitted: 12 November 2020 – Revised version received: 29 November 2020 – Accepted: 07 December 2020 – Published online: 26 February 2021) Abstract Objective The purpose of this study was to assess the relationship between periodontal diseases and chronic kidney disease (CKD) duration. Methods This descriptive cross-sectional study was conducted on referral CKD patients to a teaching hospital in 2017. Two instruments were used for data collection. The first one was a self-reported questionnaire regarding oral health status and patients’ behaviors. The second questionnaire was used for the clinical assessment of oral health status. Results Out of 192 patients, 46.9% were male and 53.1% female with a mean (SD) age of 51.9 (±15.1) years. The mean duration of CKD was 7.70 (±7.34) years. About 67.7% of patients experienced toothache in the past year. Also, 67.7% had gingival bleeding (BOP), 34.4% had clinical attachment loss (CAL) > 4 mm, and over 50% of patients had a pocket depth (PD) > 4 mm. By controlling the patient’s age, a direct correlation was detected between the duration of CKD and decayed, missing, and filled teeth index (r=0.64, P<0.001). Moreover, the prolongation of the disease period was detected in patients with CAL>4 mm (P=0.02). Likewise, a direct correlation was detected between the duration of CKD and the periodontal index (r=0.48, P<0.001). Conclusions Given the direct correlation between the periodontal conditions and duration of CKD, regular biannual dental visits are essential for CKD patients. All physicians are encouraged to include regular oral health checkups in the treatment protocol for CKD patients. Keywords Periodontal disease; Chronic kidney disease; Oral health. 24 Original Periodontal & chronic kidney diseases association Mohammad Hossein Khoshnevisan et al. J Contemp Med Sci | Vol. 7, No. 1, January-February 2021: 23 – 27 attachment loss (CAL), periodontal index (PI), community periodontal index (CPI), and oral hygiene index (OHI). The CAL was used for measuring the position of the soft tissue in relation to the cemento-enamel junction (CEJ) which is a fixed point. Two measurements were used to calculate the CAL index: The probing depth and the distance from the gin- gival margin to the CEJ. The PI was used by evaluating and scoring all teeth using five well-distinguished categories (0, 1, 2, 6, and 8), represent- ing incremental degrees of disease severity. The CPI was based on three features of bleeding, den- tal calculus, and depth of gingival sulcus. A special “WHO- probe” was used for periodontal examinations. The OHI was reported as the sum of two indices; the amounts of debris, and calculus present on the tooth surface. Thus, the OHI may ranges from 0, meaning no debris or cal- culus to as high as 6. The debris index consists of the following scores: 0, no debris on the tooth surface; 1, less than one- third of tooth surface covered with soft debris; 2, more than one-third and less than two-thirds of tooth covered with soft debris; 3, over two-thirds of the tooth surface covered with soft debris. Likewise, the calculus index, composed of the follow- ing scores: 0, no calculus on the tooth surface; 1, less than one- third of the tooth surface covered with supra-gingival calculus; 2, over one-third and less than two-thirds of the tooth surface covered with supra-gingival calculus; 3, over two-thirds of the tooth surface covered with supra-gingival calculus.12 For oral health behaviors evaluation, several questions were used to assess daily tooth brushing frequency, use of fluoridated toothpaste, flossing, consuming sugary snacks between main meals, frequency of dental visits per year, the time of last dental check-up, and cigarette smoking habit. Data were collected anonymously and analyzed using SPSS version 22. The frequency of qualitative variables, and the mean and standard deviation of quantitative variables were reported for the sample population. Likewise, demographic variables, oral health-related behaviors and oral health-related indices were reported for CKD patients. The independent t-test, Mann–Whitney test, and Pearson correlation coeffi- cient were used for statistical analysis. The P-value less than 0.05 was considered statistically significant. Results Out of 192 participants, 90 (46.9%) patients were male and 102 (53.1%) were female. The mean age of patients was 51.9 (±15.1) years, ranging from 18 to 79 years. The mean duration of CKD in patients was 7.70 (±7.34) years. Additional patients’ demographic information was presented in Table 1. The fre- quency distribution of patients’ past dental experiences were provided in Table 2. Out of 67.7% of patients who experienced toothache in the past year, only 52% of them had a dental visit. As reported in Table 3, A high percent of patients had gingival bleeding (67.7%), more than half of the them had periodontal pocket higher than 4mm, and about 34% had CAL>4mm as reported in Table 4. The mean DMFT index was 11.61 (±6.23) (Table 4). Gender differences in mean DMFT and periodontal index was minimal (P=0.99). However, advance state of periodontal diseases as demonstrated by CAL index, was slightly higher among female when compared with male CKD patients (P=0.87). Although, no significant association was detected between DMFT and PI with patients’ education (P>0.05), but the prevalence of CAL>4mm and PI was higher among patients with lower education (P=0.12, P=0.92). As demonstrated in Table 5, a direct correlation was detected between duration of CKD and DMFT index (r=0.64, P<0.001) as well as the PI (r=0.48, P<0.001). Also, a longer disease duration was detected in patients with CAL>4 mm (P=0.02). Discussion Several studies have reported on the correlation between peri- odontal diseases and CKD, emphasizing on the regular oral and dental care as one of the most important strategies to decrease the burden of CKD.23,24 In other words, entry of local inflammatory factors from affected gingiva into patient’s blood stream can aggravate systemic inflammation process and exacerbate the CKD. Obviously, oral health is not only about optimal esthetics, mastication, phonetic, and speech; there is a direct and often mutual correlation between oral health and general health. Not paying enough attention to this critical Table 1. Demographic information in CKD patients. Variable Category Number Percentage Gender Male 90 46.9 Female 102 53.1 Age groups (yrs.) 18-40 46 23.9 41-60 92 47.9 61-80 54 28.2 Place of residence Tehran 138 71.9 Other provinces 54 28.1 Educational level Illiterate 22 11.5 Below high school diploma 74 38.5 High school diploma 61 31.8 Over high school diploma 35 18.2 Disease duration <5 years 85 44.3 5-10 years 49 25.5 ≥10 years 57 29.7 Underlying disease/ health conditions Hypertension 71 36.9 Anemia 40 20.8 Diabetes mellitus 30 15.6 Cardiac disease 30 15.6 Liver disease 30 2.1 Cancer 1 0.5 None 29 15.1 25 Original Periodontal & chronic kidney diseases associationMohammad Hossein Khoshnevisan et al. J Contemp Med Sci | Vol. 7, No. 1, January-February 2021: 23 – 27 point, it can impose a significant financial burden on patients and the health-care system. Financial resources are important for financing public health plans for overall health promotion. However, most developing countries have excluded oral health from the list of their priorities due to budgetary constraints. This can cause several problems and exerts additional burden on patients and the health-care system. Thus, this study aimed to assess the correlation between periodontal disease and CKD duration in order to provide further information that may be useful for medical professionals and authorities, policy makers in the health-care systems in developing countries. In 2016, Ausavarungnirun et al assessed the correlation between periodontal disease and different stages of CKD in Table 2. Dental experiences in CKD patients. Variable Score/Response Number Frequency Oral complaints Bad taste in the mouth 126 65.6 Halitosis 115 59.9 Xerostomia 114 59.4 Oral ulcers 55 28.6 Oral and dental self-assessment Good 66 34.4 Moderate 65 33.8 Poor 53 27.6 I do not know 8 4.2 Gingival self- assessment Good 84 42.7 Moderate 54 28.1 Poor 49 25.5 I do not know 7 3.6 Tooth cleaning Tooth brushing 185 96.4 Dental flossing 52 27.1 Wooden toothpick 21 19.9 Plastic toothpick 19 9.9 Toothbrush stick 4 2.1 Frequency of daily tooth brushing Twice or more 51 26.6 Once 79 41.1 Less than one a day 62 2.1 Frequency of dental visits per year Twice or more 17 8.8 Once 60 31.3 Never 113 58.9 I do not know 2 1 Time of last dental visit < 1 year ago 79 40.1 Between 1-5 years ago 87 45.6 ≥5 years ago 24 12.6 Never 2 1 Table 3. Frequency distribution of CKD patients based on dental and gingival indices. Variable Score Number Percentage DMFT <10 102 53.1 10-20 72 37.5 >20 18 9.4 Gingival bleeding No bleeding 60 31.3 Bleeding 130 67.7 Edentulous 2 1 Periodontal pocket No pocket 81 42.3 4-6 mm pocket 109 56.7 Edentulous 2 1 Clinical attachment loss 0-3 mm 126 65.6 4-5 mm 61 31.8 6-8 mm 5 2.6 Debris index 0 48 25 >1/3 111 57.8 1/3-2/3 25 13 >2/3 8 4.2 Calculus index 0 37 19.3 >1/3 95 49.5 1/3-2/3 48 25 >2/3 12 6.3 DMFT: Decayed, Missing, and Filled Teeth Table 4. Comparison of DMFT, PI, CAL indices by gender and education level DMFT P-value PI P-value CAL<4mm CAL>4mm P-value mean (SD) mean (SD) n (%) n (%) Gender Male 11.63 (6.17) 0.99 1.43 (0.92) 0.99 58 (65.2%) 31 (34.8%) 0.87 Female 11.64 (6.31) 1.43 (0.88) 67 (66.3%) 34 (33.7%) Education Level Under diploma 11.57 (6.34) 0.75 1.43 (0.91) 0.92 98 (63.2%) 57 (36.8%) 0.12 Over diploma 11.94 (5.84) 1.42 (0.87) 27 (77.1%) 8 (22.9%) DMFT (Decayed, Missing, and Filled Teeth); PI (Periodontal Index); CAL (Clinical Attachment Loss); P-value (Probability value). Level of significance: P<0.05 significant. 26 Original Periodontal & chronic kidney diseases association Mohammad Hossein Khoshnevisan et al. J Contemp Med Sci | Vol. 7, No. 1, January-February 2021: 23 – 27 Thai patients. They found that advanced periodontitis was more common in higher stages of CKD than early stages of disease.25 Also, Grubbs et al in a retrospective cohort study in 2016 evaluated the correlation between periodontal disease and kidney function and found that, the incidence of CKD was doubled in patients with advanced periodontitis.26 Grubbs et al in 2015 evaluated the correlation of periodontal disease (in different severities) with the occurrence of CKD in African- Americans and reported that patients with advanced peri- odontitis were four times more susceptible to CKD (P=0.002). They showed that periodontal diseases were more common in patients at high risk of CKD, and found a significant cor- relation with clinical impairment of renal function.8 In their study, 86.3% of patients had gingival bleeding and 29.8% had pocket depth > 4 mm. Also, CAL > 4 mm was noted in 33.8% of patients.8 In present study, 67.7% of patients had gingival bleeding and 34.4% had CAL > 4 mm. Also, 56.7% of patients had pocket depth > 4 mm. Thus, the majority of our findings are in agreement with the results of Grubbs et al.8 In the same study, smoking had a significantly higher fre- quency among patients with advanced periodontitis.8 Thus, they concluded that smoking was an aggravating factor for periodontitis. In present study, the majority of patients were non-smokers; this probably explains why some periodontal indices such as PI in our patients were not as high as those reported in other studies. A review study by Ismail et al in 2013 reported higher prevalence of moderate to severe peri- odontal diseases in CKD patients compared with healthy con- trols. Likewise, they reported that periodontitis was correlated with higher level of systemic pro-inflammatory markers.27 In another review study by Ioannidou et al in 2013, the prev- alence of periodontitis was assessed in CKD patients. In line with findings of other studies, this report also indicated higher prevalence of periodontitis in patients with CKD compared with healthy individuals. Moreover, increased prevalence of periodontitis was associated with decreased renal function in patients with CKD.28 Joseph et al in 2009 evaluated the prev- alence of periodontal disease in CKD patients in comparison with healthy controls. They compared the oral hygiene, gingival inflammation, periodontal pocket, and CAL in 77 CKD patients with different etiologies and 77 healthy controls. The patients were divided into four groups of no periodontitis, mild, moder- ate, and severe periodontitis. They reported significantly higher periodontal indices in the CKD group compared with the con- trol group. Also, the prevalence and severity of periodontal dis- eases were significantly higher in the CKD group (P<0.001).29 In present study, when comparing periodontal parame- ters measured in CKD patients with the national data, it was revealed that, most indices in CKD patients were considerably different from the national mean values reported by the latest National Oral Health Survey conducted in 2012.30 Based on WHO recommendations, in this survey, three children and two adult age groups were considered. Therefore, our data were compared with national average in two adult age groups of 35–44 and 65–74 years old. The majority of our study par- ticipants fall within these two age categories (18–40=24%, 41–60=50%, 61+=28%). Although, patients’ age in our study population was slightly younger than the mean age of patients in the national survey, the measured indices were found to be higher than the national average. One limitation of this study can be improved by using multicenter design and make further assessments in order to determine if prevention and treatment of periodontal diseases can prevent GFR decline in CKD patients. Conclusion Given the direct correlation between the periodontal condi- tions and duration of CKD, regular biannual dental visits are essential for CKD patients. All physicians are encouraged to include regular oral health check-ups in the treatment proto- col for CKD patients. Thus, the active cooperation between medical and dental teams can be helpful in minimizing the CKD progression and severity. Financial support and sponsorship Nil. Conflicts of interest There are no conflicts of interest. A list of abbreviations CKD: Chronic kidney disease CAL: Clinical attachment loss PD: Pocket depth PI: Periodontal index DMFT: Decayed, missing, and filled teeth GFR: Glomerular filtration rate CEJ: Cementoenamel junction CPI: Community periodontal index WHO: World Health Organization References 1. Levey AS, Coresh J, Bolton K, Culleton B, Harvey KS, Ikizler TA, et al. K/ DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. National Kidney Foundation. Am J Kidney Dis 2002;39:1-266. 2. Rosansky, SJ. Renal function trajectory is more important than chronic kidney disease stage for managing patients with chronic kidney disease. Am J Nephrol 2012;36:1–10. 3. Khajehdehi P, Malekmakan L, Pakfetrat M, Roozbeh J, Sayadi M. Prevalence of chronic kidney disease and its contributing risk factors in southern Table 5. Correlation of DMFT, PI, and CAL indices by CKD duration (years). 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Oral health status and healthcare system in I.R. Iran. J Contemp Med Sci 2018;4:107-18. This work is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly. https://doi.org/10.22317/jcms.v7i1.919