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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2017  |  Volume : 28  |  Issue : 5  |  Page : 1099-1105
Oral health in diabetic and nondiabetic patients with chronic kidney disease


1 Department of Oral Medicine and Diagnostic Sciences, Al Farabi Colleges, Riyadh, Saudi Arabia
2 Department of Preventive Dental Sciences, Al Farabi Colleges, Riyadh, Saudi Arabia
3 King Saud Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia

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Date of Web Publication21-Sep-2017
 

   Abstract 


The objective of our study is to assess the subjective and objective oral manifestations and salivary pH in diabetic and nondiabetic uremic patients at a nephrology clinic. A total of 194 diabetic and nondiabetic patients with chronic kidney disease (CKD), who were divided into four groups, Group A, B, C, D, and who were attending a nephrology clinic were included in the study. Predialytic unstimulated whole salivary pH was recorded using pH- measuring strips. Subjective and objective findings were evaluated and recorded in the specially designed pro forma. Dental health assessment consisted of decayed, missing, and filled teeth index and community periodontal index (CPI). Dysgeusia was found to be significantly more prevalent in nondiabetic patients on dialysis. Uremic odor showed high significance (P <0.05) with 75% patients being positive in diabetic dialysis. There was no significant difference in the incidence of tongue coating between the four groups. A statistically high significance was observed with the objective oral manifestation of mucosal petechiae, with P = 0.01. There was an increased periodontal pocket depth among diabetic CKD patients as compared to that in nondiabetic patients. A moderate significance was found, with a CPI score showing P <0.05. Increased prevalence of caries was noticed among the diabetic CKD patients (Groups A, B). Recorded salivary pH showed no significant difference among diabetic and nondiabetic CKD patients. Findings suggest that these patients are at risk of developing complications, related to systemic health causing morbidity and mortality. Hence, these patients are to be motivated for comprehensive professional oral care and self oral hygiene instructions. Additional research is necessary to elucidate and correlate the combined influence of diabetes, CKD, and dialysis on oral health.

How to cite this article:
Swapna LA, Koppolu P, Prince J. Oral health in diabetic and nondiabetic patients with chronic kidney disease. Saudi J Kidney Dis Transpl 2017;28:1099-105

How to cite this URL:
Swapna LA, Koppolu P, Prince J. Oral health in diabetic and nondiabetic patients with chronic kidney disease. Saudi J Kidney Dis Transpl [serial online] 2017 [cited 2019 Jan 17];28:1099-105. Available from: http://www.sjkdt.org/text.asp?2017/28/5/1099/215123



   Introduction Top


Chronic renal failure (CRF) is a slow, irreparable, and progressive process that occurs over a period of years that leads to death in the absence of medical intervention. CRF is caused by many diseases that destroy the nephron mass of kidneys, such as diabetes mellitus (DM), hypertension, glomerulonephritis, interstitial nephritis, pyelonephritis, and polycystic kidney disease. Out of these, the most common cause of CRF is DM. Despite the improvements in patient care and renal replacement therapy, the impact of chronic kidney disease (CKD) on patient’s morbidity and mortality is extremely high.[1],[2],[3]

Patients presenting with CKD are at high risk to develop oral health complications such as tapering of pulp chamber,[4] enamel abnormalities,[5] xerostomia,[6] premature tooth loss,[7] increased prevalence of calculus,[8] and periodontal disease,[9] when compared to the general population. Since CKD patients present medical, psychological, and socioeconomical characteristics that may predispose to odontological problems, oral health in dialysis and transplant patients has been projected to be poor, with a potential impact on patient’s quality of life.[6],[10] Uremic halitosis is a well-known clinical characteristic of CKD patients, and assessment of this complication in patients with renal replacement therapy has not been described. In addition, poor oral hygiene and development of dental calculus are risk factors for periodontal disease, which in turn is a potential cause of sustained systemic inflammation in patients with CKD.[11] Only few studies have been conducted on a limited number of patients reporting oral health status in CKD patients.[7],[8]

CKD has received increasing attention since publication of the National Kidney Foundation’s CKD guidelines in 2002.[9] This document described a 5-stage CKD classification system, using microalbuminuria with estimated glomerular filtration rate to define the level of kidney damage and the clinical situation of the patient [Table 1].[4],[9]
Table 1: Stages of chronic kidney disease.

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CRF patients, receiving hemodialysis (HD) or renal transplants, are vulnerable to a number of diseases because of the depression of the immune functions and masking of the classic signs of inflammation and infection. Lymphocyte number and function are reduced; neutrophil chemotaxis and phagocytosis are impaired.[2],[3] There can be temporary bacteremias which are caused by various dental treatments, especially which are involved with mucosal intervention. There is evidence of increased bleeding tendency in the HD patients because of usage of anticoagulants.[11],[12] The oral manifestations of CRF appear with severity of the disease and the consequence of its treatment upon the oral cavity; these patients require special considerations and precautions while undergoing dental treatment.

Not much literature is available comparing the evaluation of oral health status among CRF patients who were under HD and those who were not under HD. Therefore, the aim of this study was to report some parameters of oral health status in a population of patients undergoing different modalities of CKD treatment.


   Materials and Methods Top


The study consisted of 194 male and female patients with CKD under treatment by nephrologist at Bhimavaram Hospitals who were divided into four groups: (Group A) diabetic CKD patients on HD, (Group B) diabetic CKD patients not on HD, (Group C) nondiabetic CKD patients on HD, and (Group D) nondiabetic CKD patients not on HD. CKD stage 4 patients were not under HD but were under continuous medication and were monitored by a nephrologist. The study protocol was approved by the institutional ethical review board, before the commencement of the study. The patients were informed completely about the study and were asked to sign a written consent, if willing to participate. Patients who were on medications such as tricyclic antidepressants, anticholinergics, and antihistamines, and those who received irradiation therapy for head and neck cancer, and patients with diabetic history of <6 months were excluded. Medical history and results of laboratory investigation were recorded by one clinician, and examination for uremic oral manifestations and dental condition was performed by another clinician who was ignorant of the medical record of each patient. Each participant underwent an intraoral examination, performed by the oral physician, who used a mouth mirror and light at the bedside for those patients attending the HD clinic. The other CKD patients who were not still undergoing HD were checked for the oral health status in a separate room after they finished their regular evaluation by the nephrologist.

Oral manifestations

The specific oral manifestations were classified into subjective and objective findings. Subjective findings that were included were dry mouth, change in taste of tongue, and/or burning sensation on the mucosa. To assess the subjective findings, each patient was asked questions about the symptoms. Objective findings that were included were uremic odor, tongue coating, mucosal petechiae or ecchymosis, and ulceration. Uremic odor was recorded by smelling the odor when the patient was talking. Tongue coating, mucosal petechiae or ecchymosis, and ulceration were recorded under a torch light illumination. Enamel hypoplasia was noted as diffuse opacities on the surface of the teeth, assessed by using the criteria which were determined by Alaluusua et al.[11] The number of decayed, missed, and filled teeth (DMFT) was calculated by means of an index, documented by DMFT. DMFT is a numerical representation that indicates the prevalence of tooth decay individually. It is an evaluation method, which is accepted by the international community as an oral health indicator. It is calculated by adding the number of decayed (D), missing tooth/unerupted (M) and filled (F) teeth (T) which is recommended by the World Health Organization (WHO).[12] Community periodontal index (CPI) was done for assessment of periodontal status, using mouth mirror and CPITN probe, which is specifically designed periodontal probe, with a 0.5 mm ball tip and black band between 3.5 and 5.5 mm and rings at 8.5 and 11.5 mm from the ball tip. According to the WHO protocol,[13] the dentition is divided into six sextants defined by tooth numbers: 18–14, 13–23, 2428, 38–34, 33–43, and 44–48 and was coded as following: Code 0 - healthy periodontium, Code 1 - bleeding on gentle probing, Code 2 - calculus deposits felt on probing, Code 3 - pocket 4–5 mm (black band on the probe partially visible), Code 4 - pocket 6 mm or more (black band on probe not visible), and Code x - excluded (less than two teeth present). For all the patients, unstimulated, whole salivary pH was recorded by using pH- measuring strips. Patients were instructed to rinse the mouth with water and then to pool the saliva on the tongue. The pH strip was placed on the tongue to wet it. The color change was immediately matched directly with scale which was provided with the strip, and the pH value was documented in the specially designed pro forma.


   Statistical Analysis Top


Statistical analysis was done by using the software, Statistical Package for Social Sciences (SPSS) version 15.0 (SPSS Inc., Chicago, IL, USA) and SAS 9.2, and Microsoft Word and Excel were used to generate graphs and tables. Chi-square test was used to find the significance of frequency distribution of study parameters between diabetic and nondiabetic patients.


   Results Top


In the study group, the youngest patient was 24 years old and the eldest patient was 72 years old. Male patients were more in number in both nondiabetic and diabetic groups. In nondiabetic group, 62.4% were male patients and in diabetic group, 60.4% were males.

Dysgeusia was found to be significantly more prevalent in nondiabetic patients on dialysis (Group C), where 90% of them were found to be positive for an altered taste sensation as compared to diabetic patients, with 68% being positive for an altered taste sensation among Group A, 74% under Group B, and 65% under Group D. Dry mouth showed moderate significance statistically, with 62% of patients being positive among nondiabetics and 78.7% of diabetic patients being positive for dry mouth who were under dialysis. Uremic odor showed high significance with 75% patients positive in diabetic dialysis (Group A), 76% among Group B, with 90% among Group C, and 91% among Group D patients with P <0.05. Tongue coating was present among 18 patients of diabetic dialysis group and nine patients of nondiabetic group. A statistically high significance was observed with the objective oral manifestation of mucosal petechiae, with10% patients in nondiabetic group as compared to 31.9% in diabetic group, who showed mucosal petechiae with P <0.01. Enamel hypoplasia was found to be negative in both the diabetic and nondiabetic groups, with a zero percent prevalence in the patients [Table 2].
Table 2: Summary of the oral manifestations among the CKD patients.

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Mouth ulceration was not significantly seen in these patients. Only 2% of the diabetic dialysis patients showed positive findings [Figure 1]. The objective finding of dry mouth was present in almost all the patients with a presentation of 100% in Group A, 98% in Group B, 96% in Group C, and 98% in group D.
Figure 1: Mucosal petechiae in four groups.

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The total DMFT score demonstrated a highly significant difference between the groups with mean value of 17.7, 17.1 among diabetic CKD patients and 7.1, 6.2 for nondiabetic CKD patients with a standard deviation of 4.9, 5.6, 7.8, 7.3, respectively, with P <0.001 [Figure 2].
Figure 2: Comparison of DMFT score between the groups.
DMFT: Decayed, missed, and filled teeth.


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There was an increased periodontal pocket depth among diabetic CKD patients as compared to that in nondiabetic patients. A moderate significance was found, with a CPI score showing P <0.05 [Figure 3]. There was a no suggestive significance statistically, with the recorded salivary pH among diabetic and nondiabetic CKD patients.
Figure 3: Comparison of community periodontal index scores between two groups.

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   Discussion Top


Oral health could be explained as a status of complete normality of teeth and supporting structures in both morphology and function always and also of the perioral components and structures related to mastication and maxillofacial complex.[13],[14] Especially in compromised individuals, such as CKD patients, oral health also has an effect on general health.[15] In our study, dry mouth was seen both in diabetic and nondiabetic patients, with no significant statistical difference. This was not in accordance with the previous literature reports, which had shown that dry mouth was severe in the diabetic group than in the nondiabetic group.[16],[17],[18],[19],[20] There are several reasons for the prevalence of dry mouth. The decreased salivary flow may be caused by a direct uremic involvement of salivary glands, chemical inflammation, dehydration, mouth breathing (Kussmaul’s respiration), or the medications which were being used and restricted fluid intake.[15] A previous study had reported that the taste change was more in diabetic uremic patients.[20] In our study, dysgeusia was found to be significantly more in nondiabetic patients than diabetic patients. The cause of metallic taste in uremic patients has been reported to be due to urea content in the saliva and its subsequent breakdown to ammonia and carbon dioxide by bacterial ureases.[8],[15] The reason for taste change can be because of metabolic disturbances, the use of medications, diminished number of taste buds, and changes in the salivary flow and composition. Although some authors have reported that the prevalence of periodontal disease is high among patients on HD, these reports are usually poorly substantiated, as the studies often lacked a control group.[3],[11],[15] Our results agree with previous publications in which the periodontal disease in diabetic patients with CKD is slightly more in terms of the prevalence and depth of pockets.[16],[17],[20] Enamel hypoplasia was found to be negative in all the study groups, with a zero percent prevalence in the patients, as the patients who were considered in our study were all adults. In the previous studies which were done on children, the authors reported that 47.4% of their renal patients had enamel defects.[18],[19],[21]


   Conclusion Top


The diabetic patients on hemodialysis were at high risk for developing periodontal disease and exhibited a potential threat for dental decay and tooth loss. Previous literature suggests that diabetes with high uremic status has a potential adverse effect on periodontal health and periodontal infection in turn having an unfavorable effect on glycemic control leading to incidence of other systemic complications. Further rigorous study is necessary to establish unequivocally that treating periodontal infections can contribute to the reduction of the burden of diabetes complications and thus improving the overall health of these patients. Furthermore, other correlating factors such as duration of dialysis, period of CKD, the medications which are being used by patients, and salivary pH and urea levels have to be evaluated, to accurately identify and correlate the oral manifestations. Supportive dental programs must be established for these patients to identify the influence of pathogens, which may predispose to systemic complications. Visit to dental clinics by these patients was primarily made only due to a dental problem rather than any orientation toward prevention of dental disease. Hence, these patients should be well educated about the importance of oral health on systemic health and should be motivated to have a regular dental checkup while undergoing the treatment for kidney disease.

Conflict of interest: None declared.



 
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Fauci AS, Braunwald E, Kasper DL, Hauser SL, Longo DL, Jameson JL, et al. Harrison’s Principles of Internal Medicine. 7th ed. USA: McGraw-Hill Access Medicine; 2008. p. 271-83.  Back to cited text no. 2
    
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Borawski J, Wilczyńska-Borawska M, Stokowska W, Mysliwiec M. The periodontal status of pre-dialysis chronic kidney disease and maintenance dialysis patients. Nephrol Dial Transplant 2007;22:457-64.  Back to cited text no. 3
    
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Woodhead J, Nowak A, Crall J, Robillard J. Dental abnormalities in children with chronic renal failure. Pediatr Dent 1982;4:281-5.  Back to cited text no. 6
    
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Klassen JT, Krasko BM. The dental health status of dialysis patients. J Can Dent Assoc 2002;68:34-8.  Back to cited text no. 7
    
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Löcsey L, Alberth M, Mauks G. Dental management of chronic haemodialysis patients. Int Urol Nephrol 1986;18:211-3.  Back to cited text no. 8
    
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Atassi F. Oral home care and the reasons for seeking dental care by individuals on renal dialysis. J Contemp Dent Pract 2002;3:31-41.  Back to cited text no. 9
    
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Duran I, Erdemir EO. Periodontal treatment needs of patients with renal disease receiving haemodialysis. Int Dent J 2004;54:274-8.  Back to cited text no. 10
    
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Alaluusua S, Lukinmaa PL, Koskimies M, et al. Developmental dental defects associated with long breast feeding. Eur J Oral Sci 1996;104:493-7.  Back to cited text no. 11
    
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Greenberg MS, Glick M. Burket’s Oral Medicine – Diagnosis and Treatment. 11th ed. USA: B C Decker Inc.; 2003.  Back to cited text no. 12
    
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Joint WHO/FAO Expert Consultation on Diet, Nutrition and the Prevention of Chronic Diseases Diet, Nutrition and the Prevention of Chronic Diseases: Report of a Joint WHO/ FAO Expert Consultation (WHO Technical Report Series; 916); 2002.  Back to cited text no. 13
    
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World Health Organization. Oral Health Surveys – Basic Methods. 3rd ed. Berlin: Springer; 1987.  Back to cited text no. 14
    
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Proctor R, Kumar N, Stein A, Moles D, Porter S. Oral and dental aspects of chronic renal failure. J Dent Res 2005;84:199-208.  Back to cited text no. 15
    
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Swapna LA, Reddy RS, Ramesh T, et al. Oral health status in haemodialysis patients. J Clin Diagn Res 2013;7:2047-50.  Back to cited text no. 16
    
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Kho HS, Lee SW, Chung SC, Kim YK. Oral manifestations and salivary flow rate, pH, and buffer capacity in patients with end-stage renal disease undergoing hemodialysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;88:316-9.  Back to cited text no. 17
    
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Ertugrul F, Elbek-Cubukçu C, Sabah E, Mir S. The oral health status of children undergoing hemodialysis treatment. Turk J Pediatr 2003;45:108-13.  Back to cited text no. 18
    
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Nakhjavani YB, Bayramy A. The dental and oral status of children with chronic renal failure. J Indian Soc Pedod Prev Dent 2007;25:7-9.  Back to cited text no. 19
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Chuang SF, Sung JM, Kuo SC, Huang JJ, Lee SY. Oral and dental manifestations in diabetic and non-diabetic uremic patients receiving hemodialysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;99:689-95.  Back to cited text no. 20
    
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Asha V, Latha S, Pal A, Srinivas K, Ganapathy KS. Oral manifestations in diabetic and nondiabetic chronic renal failure patients on hemodialysis. J Indian Acad Oral Med Radiol 2012;24:274-9.  Back to cited text no. 21
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Correspondence Address:
Lingam Amara Swapna
Department of Oral Medicine and Diagnostic Sciences Al Farabi Colleges, Riyadh
Saudi Arabia
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