Assessment of periodontal status in patients undergoing renal dialysis – A hospital-based study

Abstract

Background:

The World Health Organization (WHO) recognized chronic kidney disease as the 12^th and 17^th leading cause of death and disability in the world, respectively. End-stage renal disease (ESRD) patients undergoing dialysis are also often prone to gingival and periodontal tissue inflammation.

Aim:

The aim of this study was to assess and compare periodontal status among dialysis patients with age- and gender-matched controls in Hyderabad City, India.

Materials and Methods:

Cases (n = 165) included people who had been diagnosed with ESRD, while controls (n = 165) were subjects accompanying cases who were matched for age and gender. The oral hygiene behavior (OHB) was assessed using the OHB Index developed by Buunk et al. Periodontal status was assessed using the Community Periodontal Index modified and loss of attachment (LOA) based on the modified WHO criteria 2013.

Results:

Significantly higher means of OHB were seen among cases. Higher means of bleeding, pocket depth (PD), and LOA were seen with increasing age among males, low level of education, and presence of systemic condition among both cases and controls. The mean number of teeth with pocket depth (PD) >4 mm and the mean number of sextants with LOA >3 mm were significantly higher among cases than controls. At the same time, the gingival bleeding was significantly higher among controls. Regression analysis revealed that subjects who underwent dialysis (cases) and the presence of the systemic condition were only the significant predictors for the presence of periodontal disease.

Conclusion:

The study concludes that patients undergoing hemodialysis are more prone to periodontal diseases, which are again influenced by systemic conditions.

INTRODUCTION

Chronic renal failure or chronic kidney disease (CKD) is a life-threatening condition characterized by the progressive and irreversible loss of renal function with a glomerular filtration rate (GFR) of <60 mL/min/1.73 m² for 3 months or more.[1] CKD is the 12^th most significant cause of death and the 17^th leading cause of disability worldwide;[2] kidney and urinary tract illnesses are responsible for around 850,000 fatalities annually. Estimated at 800 cases per million, CKD disproportionately affects India’s youth.[3] End-stage renal disease (ESRD), the third most prevalent, necessitates dialysis or a kidney transplant as renal replacement therapy to prevent life-threatening uremia.[4]

Dialysis is a method that helps remove toxins and extra water from the blood, which is carried out when the GFR falls below 15 ml/min/1.73 m².[4] As per a 2018 estimate, the number of Indians on dialysis was around 175,000, with a prevalence of 129 per million.[5] However, this procedure can result in an immune-compromised state because of the imbalance between the body’s increased production of reactive toxins and its weakened defense mechanism.[6] Further, CKD patients’ physiological, metabolic, and endocrinological imbalances increase the risk for systemic complications, resulting in changes in the oral cavity, including teeth and periodontium.

The most common oral symptoms seen are pallor mucosa, sore mouth, loss of taste, and mastication difficulties due to anemia and xerostomia. Further altered salivary pH and calcium and phosphate metabolism affect the enamel formation and mineralization, thereby increasing the caries experience.[7] Furthermore, alterations in systemic and local homeostasis due to CKD could significantly alter the oral microbiota, which can induce direct and indirect bacterial-induced periodontal destruction.[8] Furthermore, the high urea content in saliva contributes to high plaque and calculus deposition, thereby providing a favorable environment for the progression of periodontal disease.[9]

Periodontitis can also be a portal for the systemic entry of microorganisms, microbial products, and potential antigens, which induce an inflammatory response at distant sites and are hypothesized to influence the incidence and progression of CKD-ESRD.[10] In addition, ESRD-related factors such as medication, stage of the condition, degree of immune suppression, and duration of dialysis also exert multiple effects, thus depicting a bidirectional relation between CKD-ESRD and periodontitis.[11]

The prevalence of periodontal disease among dialysis patients varied in previous studies, ranging from as low as 11.1% in a survey by Rodriguez-Godoy et al.,[12] to a moderate prevalence of 40%–50% in studies by Lee et al.[10] and Borawski et al.,[13] to a high prevalence of 67.3% reported by Cengiz et al.,[14] and up to a very high prevalence of 99% reported by Kim et al.[15] Further, Abou-Bakr et al.[16] also observed a high prevalence of periodontal disease (85.6%) and a significant correlation between the severity of periodontal disease and the duration of dialysis. Furthermore, Kshirsagar et al.,[17] in their preliminary study, found that moderate to severe periodontal disease was significantly associated with cardiovascular disease mortality among dialysis patients, with a hazard ratio of 5.3%.

However, more previous studies studied periodontitis as the exposure and CKD as the outcome.[10,18,19,20] Further, there is a shortage of literature regarding periodontal disease as the outcome in CKD subjects undergoing dialysis. Hence, the present study aims to assess and compare oral hygiene behavior (OHB) and periodontal status among dialysis patients with age- and gender-matched controls in Hyderabad City, India. We hypothesized that patients undergoing renal dialysis might have poor periodontal status despite having optimal OHB.

MATERIALS AND METHODS

The present case–control study evaluated periodontal status among patients undergoing dialysis and compared it to age- and gender-matched controls. Ethical clearance was obtained from the Institutional Review Board, and the research followed the ethical standards through the Helsinki Declaration and fulfilled the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines. The anonymity and confidentiality of the study participants were maintained, and participation was voluntary. The study was conducted from May 2022 to August 2022.

Sample size estimation was done using G*Power software based on findings from previous literature. At an effect size of 0.31, with a 95% confidence interval and power of 80%, the minimum estimation sample was 330, with 165 in each group. All the case group subjects were recruited from the Hyderabad Kidney Centre at Malakpet. The investigator was trained and calibrated on ten healthy controls twice daily, and the intra-examiner reliability was tested using kappa statistics, which was almost in perfect agreement (0.896).

Subjects undergoing dialysis at the age >18 years, with 20 remaining natural teeth, and who gave consent were included as cases. Control subjects were accompanying cases, matched for age and gender, with no renal failure. Individuals having deleterious personal habits (tobacco and alcohol), who used antimicrobial prophylaxis before 3 months of clinical examination, who underwent periodontal treatment in the last 3 months, and with other kidney-related diseases were excluded.

A self-reported questionnaire was used to collect information on demographics, including age, gender, level of education, systemic condition, and duration of dialysis treatment. The OHB Index, given by Buunk-Werkhoven et al.,[21] was used to measure the actual oral self-care practices of individuals. It is an 8-item questionnaire that collects data on oral hygiene practices such as toothbrushing (how often, for how long, with how much fluoride toothpaste, and for how many minutes), interdental cleaning (using floss, interdental brushes, and toothsticks), and tongue cleaning. Each item is assigned weights, which gives a total score ranging from 0 to 16, with higher scores indicating adequate OHB.

The periodontal condition was evaluated by utilizing a modified version of the Community Periodontal Index (CPI) and the loss of attachment (LOA) according to the World Health Organization (WHO) Basic Oral Health Survey Pro forma 2013.[22] In CPI modified, two indicators of periodontal status were considered: gingival bleeding and periodontal pockets. All the teeth in the oral cavity were examined for gingival bleeding and periodontal pockets. Pocket depth (PD) was further measured with a CPI periodontal probe. For gingival bleeding, a score of 0 was given for the absence and a score of 1 for the presence of the condition, while for the PD, a score of 0 was given for the absence of PD, a score of 1 for PD of 4–5 mm, and score 2 for PD of 6 mm or more. The information on the extent of LOA was collected from the index teeth in each sextant using the CPI probe: score 0 – the absence of a condition, score 1 – 4–5 mm of LOA, score 2 – 6–8 mm of LOA, score 3 – 9–11 mm of LOA, and score 4 – 12 mm or more LOA.

IBM SPSS Statistics 22.0 (IBM Corp., Armonk, NY, USA.), was used for the analysis. A descriptive statistical analysis was done to obtain information on demographic characteristics. The Mann–Whitney U-test and the Kruskal–Wallis test were used to compare the means of the OHB Index and its components and the periodontal status across categories of interest. Linear regression analysis was used to test the interrelation between periodontal disease and dialysis based on the variables studied. The probability value was set at 5% to test the significant association.

RESULTS

A total of 165 cases and 165 age- and gender-matched controls participated in the present study; the majority of the subjects were in the age group of 41–60 years (50.9%) and were males (60.6%). Comparatively, the majority of cases had primary (45.5%) and secondary (42.4%) education, while in controls, a higher number had secondary (41.2%) education. A comparable higher percentage of case subjects had systemic conditions (82.4%) than the control group (68.5%).

All the cases and controls brushed their teeth with fluoridated toothpaste once daily (at any other moment than “before sleep”). More than half of the instances brush softly (53.3%), and the remaining brush softly/forcefully (46.7%), while all the controls brush their teeth softly/forcefully. Most patients brush their teeth for longer than 3 min (53.3%), whereas control patients brush for 2–3 min (67.9%). Moreover, more cases use vertical or circular movement (14.5%), whereas controls use the bass method (21.2%) for brushing teeth. More than 90% of cases (90.3%) and controls (91.5%) never used interdental cleaning aids. However, 9.7% of cases and 8.5% of controls used interdental cleaning aids, but not daily. The majority of cases (88.5%) and controls (85.5%) do tongue cleaning sometimes, and only a few cases (11.5%) and controls (14.5%) do tongue cleaning every day.

The mean OHB was significantly higher among cases (8.07 ± 1.16) than controls (7.75 ± 0.83). Irrespective of the demographic characteristics of the study subjects, the mean OHB was also comparably higher among the case subjects. Among both cases and controls, the mean OHB was comparably lower among older subjects (7.86 ± 1.22 and 7.70 ± 0.84, respectively), subjects with lower education (7.94 ± 1.21 and 7.72 ± 0.97, respectively), and systemic condition (8.02 ± 1.18 and 7.67 ± 0.81, respectively). Nonetheless, the comparison was not statistically significant [Table 1]. Although statistically insignificant, subjects with lower mean OHB had gingival bleeding, PD ≥4 mm, and LOA.

Table 1.

Mean comparison of oral hygiene behaviour, based on variables

Variables	Cases, mean±SD	Controls, mean±SD	P
Age
20–40	8.28±1.00	7.90±0.83	0.189
41–60	8.16±1.13	7.75±0.83	0.004*
61–80	7.86±1.22	7.70±0.84	0.389
P	0.208	0.630	-
Gender
Male	8.05±1.22	7.77±0.90	0.068
Female	8.10±1.06	7.72±0.71	0.017*
P	0.756	0.726	-
Education
Primary	7.94±1.21	7.72±0.97	0.363
Secondary	8.20±1.19	7.75±0.83	0.012*
University	8.10±0.71	7.76±0.77	0.089
P	0.422	0.977	-
Systemic conditions
No	8.27±1.03	7.92±0.85	0.104
Yes	8.02±1.18	7.67±0.81	0.007*
P	0.301	0.074	-
Overall OHB	8.07±1.16	7.75±0.83	0.004*

*P≤0.05; SD – Standard deviation; OHB – Oral hygiene behavior; P – Probability value

Likewise, when the gingival bleeding status was assessed, old age, low education, and systemic condition significantly influenced the gingival inflammation among both cases and controls. Further, the mean number of teeth with GB was considerably lower among cases (10.79 ± 4.02) than controls for the overall sample and for each category of demographic variables studied [Table 2].

Table 2.

Mean comparison of number of teeth with gingival bleeding, based on variables

Variables	Cases, mean±SD	Controls, mean±SD	P
Age
20–40	8.2±5.40	8.85±6.93	0.749
41–60	10.79±3.86	17.03±7.02	0.000*
61–80	11.68±3.30	13.66±6.60	0.040*
P	0.003*	0.000*	-
Gender
Male	11.28±3.55	15.91±7.15	0.000*
Female	10.04±4.57	13.01±7.37	0.007*
P	0.054	0.013*	-
Education
Primary	11.46±3.78	15.39±6.79	0.000*
Secondary	10.67±3.56	14.77±7.16	0.000*
University	8.70±5.59	14.43±7.90	0.003*
P	0.022*	0.834	-
Systemic conditions
No	7.55±5.64	11.13±7.87	0.034*
Yes	11.48±3.20	16.44±6.48	0.000*
P	0.000*	0.000*	-
Overall GB	10.79±4.02	14.76±7.35	0.000*

*P≤0.05; SD – Standard deviation; GB – Gingival bleeding; P – Probability value

The mean PD ≥4 mm and LOA were significantly higher among cases (9.86 ± 4.99 and 4.92 ± 3.34, respectively) than controls (5.8 ± 4.93 and 2.44 ± 2.44, respectively). Older age and systemic conditions have been considerably associated with PD and LOA, which have higher means among cases. Further, education also played a significant role in LOA, where LOA increased with decreased education level [Tables 3 and 4]. GB, PD, and LOA increased significantly with the duration of dialysis (P = 0.00) [Table 5].

Table 3.

Mean comparison of number of teeth with pocket depth of 4–5 mm and 6 mm, based on variables

Variables	PD=4–5 mm			PD=6 mm
	Cases, mean±SD	Controls, mean±SD	P	Cases, mean±SD	Controls, mean±SD	P
Age
20–40	4.80±4.62	0.79±0.17	0.000*	0.23±0.88	0.00±0.00	0.227
41–60	9.55±4.73	4.34±0.47	0.000*	1.17±1.76	1.09±0.19	0.004*
61–80	12.06±4.05	5.29±0.68	0.000*	2.45±1.80	0.91±0.11	0.000*
P	0.000*	0.000*	-	0.000*	0.053	-
Gender
Male	10.64±4.51	6.00±4.63	0.000*	1.49±1.86	0.23±0.66	0.000*
Female	8.67±5.48	5.49±5.38	0.001*	1.56±1.84	0.56±1.28	0.000*
P	0.013*	0.520	-	0.789	0.643	-
Education
Primary	10.46±4.77	7.42±5.19	0.004*	1.72±1.89	0.66±1.36	0.005*
Secondary	9.85±4.66	5.30±4.92	0.000*	1.55±1.85	0.27±0.72	0.000*
University	7.65±6.41	5.48±4.71	0.105	0.65±1.46	0.29±0.93	0.206
P	0.081	0.154	-	0.070	0.133	-
Systemic conditions
No	2.44±4.02	0.28±0.93	0.000*	0.17±0.75	0.00±0.00	0.000*
Yes	11.44±3.55	8.33±3.83	0.000*	1.80±1.89	0.53±1.13	0.104
P	0.000*	0.000*	-	0.001*	0.001*	-
Overall PD 4–5 mm	9.86±4.99	5.80±4.93	0.000*	1.52±1.85	0.36±0.96	0.000*

*P≤0.05; SD – Standard deviation; PD – Pocket depth; P – Probability value

Table 4.

Mean comparison of number of sextants with loss of attachment, based on variables

Variables	Cases, mean±SD	Controls, mean±SD	P
Age
20–40	2.00±2.44	0.00±0.00	0.001*
41–60	4.45±3.09	2.58±0.28	0.002*
61–80	6.61±3.06	2.47±0.31	0.000*
P	0.000*	0.000*	-
Gender
Male	5.01±2.99	3.15±2.29	0.000*
Female	4.80±3.84	2.63±3.17	0.000*
P	0.695	0.225	-
Education
Primary	5.40±3.43	3.14±0.54	0.032*
Secondary	5.01±3.21	2.35±0.28	0.000*
University	2.85±2.77	2.65±0.33	0.263
P	0.009*	0.042*	-
Systemic conditions
No	0.44±1.91	0.01±0.13	0.239
Yes	5.88±2.75	3.56±2.18	0.000*
P	0.000*	0.000*	-
Overall LOA	4.92±3.34	2.44±2.44	0.000*

*P≤0.05; SD – Standard deviation; LOA – Loss of attachment; P – Probability value

Table 5.

Mean comparison of oral health status, based on duration of dialysis

Duration	GB, mean±SD	PD, mean±SD	LOA, mean±SD
3 months– <2 years	9.1569±5.49317	6.0392±4.12292	3.3137±2.86000
2–4 years	11.2742±3.35920	13.1774±2.55127	5.5645±2.44695
>4 years	11.4808±3.09643	16.6923±2.59365	6.5000±3.22673
P	0.048*	0.000*	0.000*

*P≤0.05; SD – Standard deviation; GB – Gingival bleeding; PD – Pocket depth; LOA – Loss of attachment; P – Probability value

Among the variables considered in the present study, the linear regression analysis revealed that only low education (P = 0.03) and the presence of systemic condition (P = 0.00) were the significant predictors of gingival bleeding, and subjects who underwent dialysis (cases) (P = 0.00) and the presence of systemic conditions (P = 0.00) were significant predictors for the presence of PD >4 mm and LOA.

DISCUSSION

The prevalence of CKD is estimated to be 13.4% worldwide, making it the most frequent form of chronic illness.[23] Periodontitis has been identified as a source of chronic inflammation in patients on dialysis, adding to the already substantial prevalence of chronic inflammation in this patient population. There has been poor periodontal status described in multiple investigations of dialysis patients.[11,12,13,14,15] It was unclear, however, what factors contributed to such poor periodontal health.

Oral hygiene is one of the factors that can independently influence inflammatory responses orally and systemically. Optimal oral hygiene relies on the effectiveness of oral self-care practices, evaluated by soft and hard deposits on tooth surfaces, which are vital contributors to periodontal diseases. Thus, the OHB Index was used to measure realistic preventive oral hygiene self-care behavior with a relatively low number of items and good internal validity. The periodontal status was evaluated using CPI modified and LOA based on codes and criteria from the 2013 WHO pro forma because of its ease of use and standardization.

The present study opted for a case–control design due to its cost-effectiveness and lower resource requirements than prospective study designs. By identifying cases with the desired outcome and matching them with controls, this design proves advantageous for investigating diseases with low incidence rates. Additionally, its relatively quick execution facilitates the generation of hypotheses and initial exploration of potential risk factors or associations. Furthermore, as case–control studies do not necessitate prolonged participant follow-up, they mitigate the risk of loss to follow-up, thereby ensuring a more comprehensive dataset.

In the present study, the mean OHB was significantly higher among dialysis patients than in the control group. These data are also comparable to other previous studies.[24,25] However, the OHB of hemodialysis patients was worse than the reference population in studies by Ziebolz et al.[25] among the German population and Klassen and Krasko[24] among the Canadian population. On the other hand, Bots et al.[26] observed no significant difference in OHB between cases and controls. As for the OHB, all the cases and control subjects brushed their teeth regularly, at least once daily. However, more Chinese[23] hemodialysis patients brushed their teeth more than once daily (98.3%). Further, studies from Turkey[27] and South Africa[28] showed that less than half of the hemodialysis patients brush their teeth regularly. These differences in findings might be due to demographic variations, less knowledge, and attitudes toward oral health.

Age, educational status, and systemic conditions significantly affected gingival inflammation among both cases and controls. Further, the mean gingival bleeding was significantly higher among controls than cases, possibly due to good OHB or periodic reinforcement of oral hygiene instructions. The results of previous studies have been inconsistent in their regard, with several reports of higher,[29,30] lower,[31,32] and equal[33] gingival inflammation in hemodialysis patients compared with controls. Further, Nishide et al.[32] reported gingival inflammation and bleeding in a 44-year-old hemodialysis female patient. The differences in the findings may be associated with oral hygiene maintenance, duration of dialysis, nutritional support, anticoagulation therapy, systemic conditions, and critical care-related factors.

The available literature provides evidence that the occurrence and severity of periodontal destruction increase with age.[34,35] Further, the potential impact of systemic conditions on the periodontium has also been well documented.[36,37] In line with the above findings, the present study also observed significantly high levels of PD in both cases and controls among older subjects and subjects with systemic conditions. This might be due to elevated levels of cytokines – interleukin, tumor necrosis factor-a, and C-reactive protein levels among dialysis patients and its impact on the pathogenesis, development, and immune response to periodontal disease, as reported by previous studies.[38,39]

Similar higher levels of PD were also observed in hemodialysis (HD) patients of Europe by Dembowska et al.,[38] Poland by Cholewa et al.,[39] and Iran by Jenabian et al.[33] However, Bayraktar et al.,[40] Cengiz et al.,[14] Kadiroglu et al.,[41] and Marakoglu et al.[42] observed no significant difference in PD between cases and controls. This difference might be due to the differences in demographic profile, periodontal measurement, or the influence of study subjects’ cultural, socioeconomic, and behavioral factors.

Likewise, the mean LOA was significantly higher among older individuals, subjects with low education levels, and subjects with systemic conditions among both cases and controls. However, LOA was more severe among cases than controls, signifying the effect of compromised immune status and the impact of inflammatory markers among dialysis patients. Further, changes in clinical attachment level and alveolar bone are also aided by impaired renal function, which is linked to altered control of Vitamin D and calcium levels. Similarly, high clinical attachment loss among cases was reported by Altamimi et al.,[43] Chhokra et al.,[44] Munagala et al.,[45] Marinho et al.,[46] and Sun et al.[47]

In the current investigation, we found that CKD patients exhibited lower levels of gingival inflammation but deeper pockets and LOA than healthy controls. This could be due to reduced immunological function, which limits the ability to mount an inflammatory response. As a result, while the illness process is still active, the conventional indications of inflammation, such as redness and swelling, may be less noticeable. Furthermore, CKD might affect wound healing and decrease tissue integrity, resulting in more significant periodontal pockets and LOA despite an apparent reduction in gingival inflammation.[30] Furthermore, CKD is a heterogeneous disease with varying symptoms and progression rates among patients. Variability in disease stage, comorbidities, OHBs, and adherence to treatment regimens can all contribute to variability in periodontal conditions among CKD patients. As a result, inconsistent findings regarding gingival inflammation and periodontal PD may represent the underlying complexity and heterogeneity of CKD-related oral health outcomes.

The mean gingival bleeding, PD, and LOA had increased significantly with the increase in the duration of dialysis. However, there was no significant relationship between HD duration and the severity of periodontal disease in previous studies.[48,49] Cengiz et al.[14] also noted that probing depth values increased significantly only during the second 5-year period and that this increase was much more pronounced after 10 years. In line with the present study, finding a significant association between HD duration and GI/PPD was reported by Bayraktar et al.,[40] Chen et al.,[34] and Ruospo et al.[50] With an increased duration of dialysis, it mediates inflammation and periodontal disease.

Linear regression analysis revealed patients undergoing dialysis and the presence of systemic conditions as significant predictors for the presence of periodontal disease. A similar, higher odds of having periodontal disease among CKD and dialysis patients were reported in previous studies.[15,46] Further, previous studies showed periodontal disease being a significant risk factor for CKD, wherein a higher strength of association was reported by Fisher et al.[18] (odds ratio) (OR = 3.93), Grubbs et al.[48] (OR = 2.5), and Kshirsagar et al.[17] (OR = 2.21). Additional longitudinal studies on the directional and nondirectional connection would strengthen the data, as periodontitis and CKD share a common risk factor and function as comorbidity to each other.

The current research admits certain caveats, including social desirability bias due to the questionnaire’s self-report format and the possibility that the study’s methodology is not optimal for establishing a causal association. Further, a smaller sample size might limit the generalizability of the findings.

CONCLUSION

Based on the present study’s findings, the mean oral hygiene behavioral practices were significantly higher among cases. The mean number of teeth with gingival bleeding was significantly higher among controls than cases. The mean PD of >4 mm and LOA were considerably higher among cases than controls. Among both cases and controls, the GB, PD, and LOA were significantly higher among older subjects, males, subjects with low education, and those with systemic conditions. The gingival bleeding and periodontal conditions increased substantially with the duration of dialysis. Linear regression analysis reveals that patients undergoing dialysis and systemic conditions are significant predictors of GB, PD, and LOA presence. Overall, patients undergoing dialysis had poor oral health despite good OHB.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.