Assessment of periodontal health status in patients undergoing renal dialysis: A descriptive, cross-sectional study.

OBJECTIVE: An inter-relationship between periodontal disease and systemic health has been suspected for centuries, but evidence to explain the connection has only been elucidated in the past few decades. Among the systemic diseases, end stage renal disease has been shown to affect not only the general health of the patient but also oral and periodontal health. This study was undertaken to gain an insight into whether duration of dialysis therapy influences the oral and periodontal health of these patients and also to see if these parameters reflect their biochemical values.
MATERIALS AND METHODS: The study was conducted on 75 patients undergoing dialysis and a control group of 25 subjects. The study group was divided into three subgroups depending upon the duration of dialysis. Oral hygiene and periodontal disease status were measured by Simplified Oral Hygiene Index by Greene and Vermillion and Periodontal Disease Index by Ram-fjord. Biochemical parameters measured were blood urea nitrogen and salivary urea levels. Comparison of these parameters was made between the study and control groups through analysis of variance (ANOVA) and student's t-test.
RESULTS: Prevalence of periodontal disease was evident in the dialysis group. Oral hygiene status was poor in comparison with the control group. Clinical and biochemical parameters showed statistically significant difference between the groups rather than within the groups.
CONCLUSION: Oral and periodontal health appeared to be compromised. Their deteriorating general health is anticipated to cause negligence towards oral health care. This population needs comprehensive oral and periodontal care right from the diagnosis of chronic renal failure. There exists a need for communication between nephrologists and oral health care professionals. Longitudinal studies warranted in this regard.

INTRODUCTION

Periodontitis, a chronic infectious disease, affects most of the population at one time or the other and its expression is a combination of hosts, microbial agents, and environmental factors. It does not appear to be a single disease with variations in clinical symptoms, but a group of diseases with overlapping symptomatology.[1] Etiology is however complex with many factors at risk, of which, few are biological such as age, systemic conditions, and others are behavioral factors such as smoking and oral cleanliness. However, variation in disease severity cannot be explained taking only these factors, the remaining variance may be explained by the importance of psychosocial factors which remain associated with systemic diseases. A number of possible mechanisms of action between psychosocial factors on periodontal disease have been proposed which include neglect of oral hygiene, changes in saliva, endocrine imbalances, and lowered host resistance. By examining these mechanisms, it may be evident that some may involve psychologically related changes in behavior which enhance vulnerability to periodontal breakdown.[2]

Extensive literature exists for the relationship between periodontal disease and diabetes mellitus, cardiovascular diseases and adverse pregnancy outcomes.

Recently, several studies have been published in the literature, providing evidence for an increased prevalence of periodontal disease in patients with renal disease, especially in dialysis patients and renal transplant recipients.[3-9] End stage renal disease has been shown to affect not only general health of the patient but also oral and periodontal health.

Literature on research has shown that the number of patients undergoing dialysis is increasing rapidly and these patients frequently complain of number of symptoms related to oral cavity. Such findings are: Uremic stomatitis, insidious oral bleeding, xerostomia, high salivary urea, increased calculus deposition, increased incidence of gingivitis, periodontitis, and secondary renal hyperparathyroidism.

Few studies have shown 100% prevalence of periodontal disease in these patients, and in contrast, others have not. A change in salivary composition regarding urea has also been reported.[910]

Hence, the aim of the study was to gain an insight into whether the duration of dialysis therapy has any influence on the oral and periodontal condition of these patients and to see if these clinical parameters reflect the biochemical values like blood urea nitrogen (BUN) and salivary urea levels.

MATERIALS AND METHODS

Study population

The study was conducted in two multi-specialty hospitals of Bagalkot district, Karnataka, India. After approval from the institution committees of dialysis centers and obtaining informed consent, 75 patients ranging from 18-74 years undergoing dialysis were selected as the study group. A fourth group consisting of 25 systemically healthy patients ranging from 19-69 years, serving as controls, was also included in the study. For this cross-sectional study, a purposive sampling technique was used to identify patients who were undergoing dialysis for varying length of time.

The patients were divided into four groups of 25 each.

Group 1: Patients’ undergoing dialysis therapy for less than one year

Group 2: Patients’ undergoing dialysis therapy from one to three years

Group 3: Patients’ undergoing dialysis therapy for more than three years

Group 4: Systemically healthy individuals those attending the outpatient department of periodontics, who matched with age and sex of the study group.

Data collection

Details of patients’ renal status as depicted by BUN values and duration of the dialysis period were obtained from hospital records for groups 1, 2, and 3. Estimation of BUN and salivary urea analysis were also done for the control group. All the groups were examined for oral hygiene status, periodontal disease status, salivary urea, and BUN. Demographic data, clinical, and biochemical parameters were recorded in a proforma.

Oral and periodontal examination

A single trained examiner carried out the oral and periodontal examination fulfilling the criteria of Simplified Oral Hygiene Index (OHI-S) by Greene and Vermillion 1964. The index for OHI-S was calculated using six index teeth: 16, 11, 26, 36, 31, and 46. The periodontal disease index (PDI) (Ram-fjord 1959) was calculated using six index teeth 16, 21, 24, 36, 41, and 44.

Biochemical evaluation of salivary urea

About 1 ml of whole saliva was collected by spitting method from both the study and control groups in a sterile disposable container and then transferred to the laboratory in an ice container for urea analysis. Salivary urea was estimated with the help of an automatic analyzer by-GLDH UREASE METHOD. This method utilizes the action of enzyme urease on urea produced in saliva to produce ammonia and carbonic acid. Ammonia liberated reacts with alpha ketoglutaric acid in the presence of glutamate dehydrogenase. The decrease of absorbance at 340 nm corresponding to the oxidation of nicotinamide adenine dehydrogenase (NADH) to nicotinamide adenine (NAD) and is proportional to the amount of urea concentration in the sample.[11]

Statistical analysis

Data are presented as mean, standard deviation (SD), and 95% confidence interval of the mean difference. Comparison for clinical and biochemical parameters between the study groups and the control group was carried out using ANOVA-one way (Analysis of Variance). Pairwise comparison was done by using Student's t-test. All levels of significance were set at P<0.05.

RESULTS

A total of 100 subjects were included in the study, of which, 75 were patients undergoing renal dialysis and 25 were systemically healthy individuals. Distribution of study subjects according to the duration of dialysis and gender is depicted in Figure 1 and Table 1. Comparison of four groups with respect to OHI-S values, PDI values, salivary urea, and BUN values are depicted in Figures 2–5. The summary statistics of OHI-S, PDI, salivary urea and BUN values are shown in Tables 2–5. When all the four parameters were compared between the study and the control group, significant statistical difference was noted at P=0.0000 [Tables 6–13]. However, when pairwise comparison was made between the four groups, statistical significant difference was noted between the study and controls. There was no statistical significant difference noted for salivary urea and BUN values within the study groups, but OHI values and PDI values were significant between the groups 1 and 2, and 1 and 3 [Tables 8 and 9]. The present study revealed (0%) of patients had good oral hygiene (37%) had fair oral hygiene and (63%) patients had poor oral hygiene scores in the study group, whereas the control group showed 96% of subjects with fair oral hygiene scores and 4% with good oral hygiene scores. Periodontal examination revealed 24% of patients exhibiting gingivitis with various degrees of inflammation and 75% of patients exhibited with several degrees of attachment loss as measured from CEJ. Salivary urea and BUN were higher in the dialysis group.

Figure 1

Distribution of study subjects according to duration of dialysis and gender

Table 1

Distribution of study subjects according to duration of dialysis and gender

Figure 2

Comparison of four groups with respect to OHI-S values

Figure 5

Comparison of four groups with respect to blood urea nitrogen values

Table 2

Summary statistics of OHI-S index values according to groups

Table 5

Summary statistics of blood urea nitrogen values according to groups

Table 6

Comparison of four groups with respect to OHI-S values by ANOVA test

Table 13

Pair wise comparison of four groups by students t-test for BUN values

Table 8

Comparison of four groups with respect to PDI values by ANOVA test

Table 9

Pair wise comparison of four groups by students t-test for PDI values

Comparison of four groups with respect to PDI values

Comparison of four groups with respect to salivary urea values

DISCUSSION

It is well documented that systemic conditions may affect the oral cavity; in contrast to the oral conditions affecting the systemic health remains speculative. Since oral health is intimately related to systemic health, as mouth is truly connected to the rest of the body, the directionality of special relationships has to be clarified. The possibility that mortality and morbidity from systemic disease may be reduced at improving periodontal health makes it imperative that this relationship be examined more closely.

The susceptibility of periodontal disease varies among people and is not even, as various factors such as host response, pathogenic flora, age, gender, education, and the frequency of dental visits.

End stage renal disease (ESRD) encompasses a wide range of metabolic disorders affecting every system of the body leading to a very immunocompromised situation. The incidence of ESRD continues to rise worldwide and in India, a conservative estimate of ESRD burden, based on a population of 1.1 billion is that 1,650,000-2,200,000 people develop ESRD annually and as a consequence, increasing number of individuals with such disease will probably continue to require oral health care.[12]

The pooled sample in the study group of 75 dialysis patients revealed 0% patients with good oral hygiene (0.0-1.2), 28 patients (37%) with fair oral hygiene scores (1.3-3.0), and 47 (63%) patients with poor oral hygiene scores (3.0-6.0). The control group showed 96% of subjects with fair oral hygiene scores and 4% with good oral hygiene scores. A significant statistical difference (P=0.0000) through ANOVA and pairwise comparison was observed for oral hygiene scores between the groups, indicating dialysis patients, in general, had poor oral hygiene status in comparison with controls. Regarding periodontal disease status, the study group showed (24%) n=8 of individuals exhibited gingivitis with various degrees of gingival inflammation. The control group showed 60% (n=15). The subject of gingival inflammation in chronic renal failure (CRF) patients appears to be controversial in the literature. Reports by Tollefsen indicated reduced gingivitis due to immunosupression and uremia that might inhibit gingival reaction to plaque stimulation,[1314] while Naugle et al. in his study indicated opposite findings.[4]

Prevalence of periodontitis was 75% as denoted by several degrees of attachment loss. The findings support reports of Naugle et al. suggesting that individuals on dialysis do not receive adequate periodontal care and the disease progresses unchecked. Self reported information revealed ignorant attitude as well as lack of awareness towards oral health care and its importance seemed to be a trivial matter in comparison with their systemic illness. They seek dental treatment only on an emergency basis. As the procedure of dialysis is time consuming, a time factor may also be involved in getting dental treatment. It is also suggested that as a consequence of renal failure, these patients exhibit decreased bone mineral density that would increase the risk for alveolar bone loss from subsequent periodontal infection. However, a single study of 35 ESRD patients on maintenance therapy with secondary hyperparathyroidism failed to find an association between parathyroid hormone level and alveolar bone loss or periodontal pocket depth when compared with 35 case matched non-ESRD controls.[15] Periodontal disease progression in CRF patients has also been related to impaired white cell function, but our study did not involve any immunological tests. However, studies by Oshrain et al. found no difference in clinical parameters between different immune status patients when measurements were made in a single examinations study, suggesting that non immune mechanism such as direct effect of bacterial products on supporting tissues could account for some of the clinical manifestation of periodontal disease.[16]

Most dialysis patients have complex medical outcomes such as hypertension, diabetes, and increased bleeding tendency which could play the role of important confounding factors in giving a conclusive diagnosis of periodontal disease status. It can also be justified that poor oral hygiene and its cumulative effect over the years might have caused increased periodontal attachment loss in these patients. Frequent evaluation of oral cavity in a longitudinal study, right from the beginning of dialysis therapy could give more meaningful and conclusive results.

Many studies have reported biochemical changes in the saliva of patients undergoing dialysis with regards to urea. In the present study, higher salivary urea values were found in the dialysis group than in the control group (P=0.0000), thus supporting findings of Epstein, Hong Seop Kho, and Thomas Mathew.[101718] In fact, in one of the studies, salivary urea has been used as index to asses renal function.[19] Urea values observed in saliva were lower than in blood, may be considered as measure of efficiency of blood and saliva to purify themselves. Comparison between the two values showed significant statistical difference between the groups, but not within the groups as denoted by ANOVA and pairwise test. This finding suggests that time duration may influence salivary urea values. The self reported complaints of dialysis patients were dryness of oral cavity and altered taste sensation. This could be attributed to altered salivary gland function, especially in diabetics, and the overall volume status as these patients are discouraged from drinking excess fluids. Dysguesia uremic fetor and bad taste in these patients have been described by Klassen et al.[20] The taste disturbances in these patients could also be attributed to metabolic disturbances, use of medication, diminished number of taste buds, changes in salivary flow rate and composition.[21] Burge et al.,[17] has suggested high levels of urea along with di- and tri-methyl amines with low level of zinc might also contribute to decreased taste perception in these patients. Salivary substitutes can be of help to overcome dry mouth manifestations.

Invariably patients undergoing dialysis have increased BUN values. Renal function depends on glomerular filtration rate (GFR). BUN will not be increased until GFR is decreased by 50%. Dialysis patients showed high values than controls as expected, but within the groups, group 1 showed higher values than groups 2 and 3.

CONCLUSION

The patients undergoing renal dialysis showed poor oral hygiene and higher prevalence of periodontal disease. Lack of awareness and negligence toward oral health care was noted. They do not visit the dentist on regular basis. Since these patients aspire to receive transplants, it becomes mandatory for them to undergo extensive oral and dental therapy to remove probable source of infection, which may lead to failure of transplant. Salivary urea levels and BUN values were elevated in the dialysis patients. The dental community's awareness of implications of poor health within this population should be elevated.

Table 3

Summary statistics of PD index values according to groups

Table 4

Summary statistics of salivary urea values according to groups

Table 7

Pair wise comparison of four groups by students t-test for OHI-S values

Table 10

Comparison of four groups with respect to salivary urea values by ANOVA test

Table 11

Pair wise comparison of four groups by Students t-test for salivary urea values

Table 12

Comparison of four groups with respect to blood urea nitrogen values by ANOVA test