Open Access Journal of Dental Sciences

Oral Health Parameters of Diabetic and Non-Diabetic

Patients Undergoing Heamodialysis- A Comparative Study

Anjum YM1*, Mohsin H1, Sidra F1, Maria M1 and Ambrina Q1 Research Article

1Department of community dentistry, Dow University of Health Sciences, Karachi, Volume 1 Issue 2
Received Date: August 15, 2016
Pakistan
Published Date: September 20, 2016
*Corresponding author: Anjum Younus Mirker, Department of community
dentistry, DIKIOHS, Dow University of Health Sciences, Karachi, Pakistan, E-mail: [email protected]

Abstract
Objective of study: There is rising incidence of chronic kidney disease (CKD) worldwide. Although the oral health
parameters have been examined and reported among CKD patients, investigations of diabetic heamodialytic patients are
limited. Therefore, the aim of this study is to assess and compare dental and periodontal health parameters between
diabetic and non diabetic heamodialysis patients in Karachi.
Materials & methods: A total of 100 heamodialysis patients were allocated as diabetic and non diabetic as per their
HbA1c level and examined for dental caries and periodontal health using DMFT, PI, CPI and CAL indices with protocol
given by WHO. Socio-demographics and medical history was recorded. All examinations were performed in pre-dialysis
phase and by single-blinded examiner. Statistical tests of Chi square and student-tests were used for comparing
percentages and mean differences between groups (p-value <0.05).
Findings: Among all socio-demographic variables, distribution of gender and duration of dialysis were not significantly
different in between groups. There is a significant difference in all indices between both groups. DMFT mean was high
among non diabetic patients and plaque scores were high among diabetics. Bleeding was more among diabetic patients
and CAL showed more than 6mm attachment loss in same group.
Discussion: This study reveals that diabetic patients exhibit higher tendency for bleeding on probing, moderate level of
attachment loss and abundance of plaque deposits as compared to non diabetic group. There is a need of further research
to establish associations between diabetic nephropathy and oral health.
Abbreviations: PI: Plaque Index; CAL: Clinical Attachment Loss; CKD: Chronic Kidney Disease; DM: Diabetes Mellitus;
ESRD: End-Stagerenal Disease; IRB: Institutional Review Board; CPI: Community Periodontal Index

Introduction Pakistan. Delay in treatment resulting from lack of

screening and risk identification which ultimately hinders
The burden of chronic kidney disease (CKD) has a implementation of preventive measures [1]. This often
progressive increase in south Asian countries including leads to more complicated condition, End-stage renal
failure, which requires organ transplantation and dialysis
therapy [2]. Periodontal diseases in association with other

Oral Health Parameters of Diabetic and Non-Diabetic Patients Undergoing Heamodialysis- A Comparative Study J Dental Sci
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Open Access Journal of Dental Sciences
systemic diseases have increased drastically from past diabetic and non-diabetic patients on heamodialysis
few decades and if considered with chronic kidney therapy.
diseases (CKD) it is of no exception. In literature, there is
an established relationship of systemic conditions like Materials and Methods
cardiovascular disease, pulmonary diseases, osteoporosis,
anemia as chronic kidney disease (CKD) and especially This is a cross sectional analytical study conducted
diabetes mellitus (DM) with oral diseases [3]. Presence of over a period of 3 months (April 2016 to June 2016) at
one condition increases the chances of others. According heamodialysis units of Dow University of health sciences
to a survey, frequency of 40 years or older persons with Ojha campus and Nephrology department of Jinnah
reduced estimated glomerular filtration rate ranges from Postgraduate Medical Centre. The study protocol was
15%to 20% [4]. Such a high burden is consistent with reviewed and approved by institutional review board
high prevalence of diabetes and hypertension, the leading (IRB) at Dow University of health sciences. All patients
causes of end-stage renal disease (ESRD). It is estimated were informed before enrollment to a predefined protocol
that annual incidence of ESDR in Pakistan is about 150 and written consent was taken. All the examinations of
patients per million of population. Therefore, each year, patients were in accord with the Declaration of Helsinki
we shall have 16000 patients with ESRD [5]. and its revisions. An inclusion criterion of the study was
ESRD patients who were on maintenance hemodialysis
A recent local survey results showed that, diabetes was therapy for not less than 3 months and were able to give
the leading cause of CKD, confirming previous results informed consent. The exclusion criteria consisted of
from Pakistan [6]. These findings are consistent with patients who had history of periodontal therapy or the
those reported from Western countries. According to the use of antibiotics during the last three months prior to
United States Renal Data System (USRDS), the commonest examination, pregnancy or lactation, diabetes diagnosed
cause of ESRD was diabetes (42.9%) [7]. Compared to in less than 6 months, patients who were undergoing
Western countries, diabetes is more prevalent in peritoneal dialysis, edentulous patients, patients who
subcontinent and it would likely to multiply over the next didn’t agreed to participate in the study with inform
two decades [8]. A study from UK demonstrates the high consent, and patients who have index teeth extracted due
prevalence of diabetes mellitus in the South Asian to caries or mobility. Sample size was calculated using
population in East London, with both a higher overall openepi version 3, 2-sample t-test for CPI mean with the
prevalence and earlier onset compared to both the Black power of 80% and confidence interval of 95% [11]. The
and White populations [9]. Similar to ESRD, diabetes mean difference was 0.31 for both the groups. Hence, the
mellitus (DM) is also a contributor of oral pathological sample size for each group was maximum 55 subjects. As
changes. Poorly controlled diabetes is also marked as per inclusion criteria, there were 50 participants in the
systemic risk factor for many types of periodontitis. The diabetic group and 50 in non diabetic group, respectively.
findings of a comparative study revealed that diabetic Subjects were age and gender matched. Subsequently, the
hemodialysis patients presented an increased prevalence diabetic patients with ESRD were further classified into 2
of caries and noticeable oral manifestations like dry subgroups according to their glycemic control:
mouth and oral mucosal inflammation, compared to HbA1C≤6.5% as good controlled and HbA1C>6.5% as
nondiabetics [10]. Also, patients with poorly controlled poor controlled [12]. Data collection tool was a self-
diabetes with HbA1c level > 9% had a higher incidence of designed Performa consisting of three parts. The first
dry mouth and other oral symptoms than fairly or good portion recorded the socio-demographics details. The
controlled ones [10]. The association of periodontal second portion recorded medical and dental history.
disease with diabetes is well documented but its Participant’s Glomerular Filtration Rate was calculated
contribution in CKD is still debatable. Although the oral from serum creatinine using Cockcroft-Gault equation
and dental changes of the individual diseased condition [13]. While the third portion of the perform a included the
(i.e. DM or ESRD) have been examined, there is scarcity of clinical dental examination.
data investigating periodontal health measures among
diabetic hemodialyzed patients. Studies mostly reported The indices used were DMFT index for dental caries
oral condition associated to uremia in the general and Plaque Index (PI) according to Silness and Loe and
population of ESRD patients. The influence of coexisting the WHO indices of Loss of Attachment (CAL) and
medical conditions (i.e. DM and ESRD) on the dental community periodontal index (CPI) [14]. The oral
health also needs inspection. The aim of this study was to examination was done by a single blinded examiner who
assess and compare the oral health parameters between had no knowledge of the patient’s medical history and
oral hygiene practices. For reliability (calibration), the

Anjum YM, et al. Oral Health Parameters of Diabetic and Non-Diabetic Copyright© Anjum YM, et al.
Patients Undergoing Heamodialysis- A Comparative Study. J Dental Sci 2016,
1(2): 000110.
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Open Access Journal of Dental Sciences
examiner has been calibrated against gold standard were isolated with cotton and examination was
periodontologist with percent agreement of 86%. The performed using standard cross infection control
DMFT index was recorded as decayed (D), missing (M), protocol. Probing on index teeth was recorded using
and filled (F) teeth according to the criteria of WHO. The examination instruments and CPITN Probe in the
overall DMFT score was taken as the sum of all 3 presence of artificial light (LED torch).
components for each patient. The CPI and CAL indices
were selected to minimize discomfort and lengthy Statistical Analysis
periodontal assessment of these patients. The criteria for
CPI was: Code 0 for healthy periodontium, code 1 for The data was entered and analyzed in SPSS version 16
bleeding on gentle probing, code 2 for calculus deposition, (Chicago IL, US). Descriptive analysis of socio-
code 3 for probing depth of 4 to 5 mm and code 4 for demographic data was performed with mean and
probing depth 6 mm or deeper and Code X for 3 or more standard deviation for quantitative variables and
teeth missing. The criteria of attachment loss was percentages for categorical variables. For the evaluation
calculated as 0= 0-3mm, 1= 4-5mm (cementoenamel of significance of diabetes on dental and periodontal
junction (CEJ) within black band), 2=6-8mm (CEJ between health, Chi square and fisher exact tests were used for CPI,
upper limits of black band an 8.5 mm long), 3= 9-11mm CAL and PI, whereas student T-test used for comparing
(CEJ between 8.5mm and 11.5mm rings), 4= 12mm or mean difference of DMFT. A value of p < 0.05 was
more (CEJ beyond 11.5 mm ring), X= excluded sextant, 9= considered statistically significant.
not recorded. The periodontal condition for each sextant
was identified with the highest recorded code. The teeth Results
Diabetic Non Diabetic
Characteristics P-value
N=50 N=50
Gender
Male: female n (%) 31:19 (62%: 38%) 22:28 (44%:56%) 0.251
Mean Age(years, SD) 45.8 ±14.8 54.7 ±8.27 0.007
Education (n, %) 0.003
Illiterate 14 (28%) 3 (6%)
literate 36 (72%) 47 (94%)
Marital Status (n, %)
Unmarried 7 (14%) 0
Married 43 (86%) 50
Monthly income (PKR) 0.005
None 5 (10%) 16 (32%)
Less than 10, 000 PKR 11 (22%) 6 (12%)
10 – 20, 000 PKR 22 (44%) 25 (50%)
More than 20,000 12 (24%) 3 (6%)
Brushing Frequency (n, %) <0.001
None 8 (16%) 0
Once a day 30 (60%) 20 (40%)
Twice a day 12 (24%) 30(60%)
Dental visit (n, %) 0.005
Never 30 (60%) 14 (28%)
Less than 6 months 8 (16%) 12 (24%)
More than 6 months 12 (24%) 24 (48%)
Co-morbid (n, %) 0.003
none 22 (44%) 11 (22%)
Hypertension 15 (30%) 33 (66%)
Hepatitis C 8 (16%) 6 (12%)
Cardiovascular disease 5 (10%) 0
Mean duration of dialysis (years, SD) 2.43 ±0.718 2.19 ±0.785 0.278
Table 1: Socio-demographic characteristics of study population undergoing heamodialysis.

Anjum YM, et al. Oral Health Parameters of Diabetic and Non-Diabetic Copyright© Anjum YM, et al.
Patients Undergoing Heamodialysis- A Comparative Study. J Dental Sci 2016,
1(2): 000110.
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Open Access Journal of Dental Sciences
The characteristics of patients undergoing groups along with significance of association are
hemodialysis are presented in (Table 1). Among these presented in Table 2. Non Diabetic patients exhibit
100 patients, 50 were diabetic and 50 were nondiabetic. significantly higher decayed (D) component than those in
The mean age was 45.8 years (±14.8) in the diabetic the diabetic group (p-value= 0.003). The resulting DFMT
group and 54.7 years (±8.27) in the nondiabetic group. index in non diabetic patients (6.02 ±5.08) also
Ratio of male to female shows more men in diabetic group significantly higher than diabetic patients (3.84 ± 3.43)
compared to women. Majority of patients were educated (p-value = 0.005). The statistics of CPI index depicted that
and married in both groups. Among all socio-demographic both study groups had minimum incidence of Code 4. The
variables, distribution of gender and duration of dialysis non diabetic group showed greater percentage for
were not significantly different in between groups. calculus (46%), labelled as Code 2, compared to the
diabetic group (34%). While codes 0 (healthy) and 1
Non (bleeding) were more frequent in diabetic group (26% &
Diabetic P- 18%). Another index of CAL showed that majority of
Diabetic
N = 50 value patients had code 0 in both groups (68% in diabetics and
N = 50
70% in nondiabetics). Code 2 was only exhibited by
DMFT Index (Mean, diabetic group in low frequency (6%). While assessing
SD) Plaque index, code 2 (mild accumulation) was most
Decayed 1.6±1.85 3.0±2.69 0.003 common in both groups (42%). Diabetic group had higher
Missed 2.22±2.46 2.78±2.83 0.330 incidence (16%) of code 3 (abundance of plaque)
< compared to nondiabetics. Statistical analysis using the
filled 0.02±0.14 0.24±0.59
0.001 chi-square and student t-tests showed significantly
DMFT 3.84 ±3.43 6.02±5.08 0.005 differences for the CPI, CAL and PI assessments between
CPI codes (n, %) 0.025 the diabetic and nondiabetic group (p-value <0.05).
0 13 (26%) 9 (18%)
1 9 (18%) 4 (8%) Discussion
2 17 (34%) 23 (46%)
3 11 (22%) 11 (22%) This study was conducted among 100 heamodialysis
4 0 0 patients- 50 were in diabetic group and 50 were non
X 0 3 (6%) diabetic. The diabetic group was matched with
nondiabetic group in age and gender. The aim of study
LOA Index (n, %) 0.015
was to assess and compare the oral health status of
0 34 (68%) 35 (70%) diabetic and nondiabetic patients who were undergoing
1 13 (26%) 15 (30%) heamodialysis therapy. Both of these conditions, diabetes
2 3 (6%) 0 and end-stage renal disease have major effects on oral
3 0 0 health, but no comparative study has been reported to
4 0 0 assess the combined effect of DM and ESDR on oral health
X 0 0 in Karachi, Pakistan. Age is the well known risk factor for
Plaque Index (n, %) 0.028 both chronic kidney disease [15,16] as well as periodontal
0 5 (10%) 6 (12%) diseases [17]. The mean age was 45.8 years (±14.8) in the
1 16 (32%) 19 (38%) diabetic group and 54.7 years (±8.27) in the non diabetic
2 21 (42%) 21 (42%) group. Both the groups have mean age lower than
3 8 (16%) 4 (8%) previous studies [9,16]. The mean age of the dialysis
patients in this study was higher in this study than the
Table 2: Prevalence of dental caries and periodontal
subjects of an Indian and Turkish study of heamodialysis
condition in hemodialysis patients with and without DM.
patients [10,18]. Participants of this study were more
Comparison of DMFT index between diabetics and non literate in both groups compared to a local study [19].
diabetics groups was analyzed by the Student t-test; D- Mean duration of heamodialysis was less than 3 years in
decayed; M-missing; F- filled; T-total. Comparisons of CPI, both groups which was lower than a similar study in
CAL and PI were analyzed by chi-squared test. Turkish population [15] while diabetic group has slightly
higher duration compared to non diabetic group in both
The distributions of DMFT index, Plaque index (PI); studies. There was significant difference between the
clinical attachment loss (CAL) and CPI codes in both diabetic and non diabetic groups in terms of brushing

Anjum YM, et al. Oral Health Parameters of Diabetic and Non-Diabetic Copyright© Anjum YM, et al.
Patients Undergoing Heamodialysis- A Comparative Study. J Dental Sci 2016,
1(2): 000110.
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Open Access Journal of Dental Sciences
habit and visit to dentist and it is in agreement with higher value of clinical attachment loss. Based on these
previous studies [19-21]. Majority of patients in diabetic findings, also reported by Chuang, et al. [8] there is an
group (60%) had never visit a dentist in life. This elevated risk for advanced periodontitis in diabetic
difference might be showing their negligent behavior patients undergoing heamodialysis and need more
toward their oral health. Longer and tiring process of attention to their periodontal health. In another study
dialysis is itself a cause of lowered self-esteem among with control group, that CPI values were significantly
patients of ESDR. It would be more desirable to facilitate higher in peritoneal and heamodialysis groups [21]. A
provision of dental health education within the dialysis recent similar study with diabetic and non diabetic
centers and institutes. This will be much helpful for groups, demonstrated a borderline significant difference
dialysis patients to awareness and instructions about the in investigation of CPI between those groups [10]. The
fate of poor dental health. There is a high rate of dental limitations of this study include its performance in two
caries in patients with diabetes mellitus possibly due to dialysis centers and relatively small sample, but
alteration in oral microflora, oral Ph and their potential comparable with most of the previous studies. Also, bed
xerostomia [22]. In our study, there was a significant side measurements of all indices were made and no
difference in DMFT scores of diabetic and non diabetic radiological assessment was done for periodontal
groups. DMFT mean score was almost double in non investigations. We also not made comparison of effect of
diabetic group than diabetic group which was in contrast biochemical indicators on oral health between both
with previous studies [9,10]. This might be reflecting the groups. There may be important differences in the host
eating habits and oral health awareness in diabetic response to bacterial challenges. Also we did not have the
patients. Diet of diabetic patients is usually restricted to oral health status prior to the heamodialysis for the
sugary and refined food and those also undergoing estimation of the actual severity of caries and
haemodialysis might be more cautious about their feeding periodontitis during the heamodialysis.
pattern. This could be a possible reason of lowered DMFT
score among diabetic group along with their optimum Conclusion
brushing practices in our study.
In conclusion, this study is first to compare oral health
Diabetes is a well known risk factor for periodontitis findings between diabetic and non diabetic patients with
and it has been reported by various investigators that heamodialysis therapy in Karachi. These findings within
extent and severity of periodontal disease might be limitations of study, suggest that diabetic patients exhibit
increased in diabetic patients [22,23]. Assessment of higher tendency for bleeding on probing, moderate level
plaque in our study revealed significant difference of attachment loss and abundance of plaque deposits as
between both groups. Data from other countries reported compared to non diabetic group. There were significant
a higher value of plaque index in heamodialysis patients differences for socio-demographic variables as well as all
as compared to controls [21,24]. Similar findings were dental indices between both groups. Maintenance of ideal
established in our study which showed mild to moderate oral hygiene could have positive effects in this high-risk
plaque deposits in both groups while abundant plaque group of patients. Prophylaxis and early dental care
scores were found among diabetic group. In terms of CPI should be implemented in chronic renal disease patients;
and LOA index, diabetic group exhibited more bleeding this would also be beneficial for their general health.
and deeper pockets than non diabetic group. Also, there There is need of longitudinal studies and larger samples
were significant statistical differences in both indices in order to establish a causal relationship among diabetes,
between diabetic and non diabetic heamodialysis heamodialysis therapy and oral health status.
patients. Bleeding on probing was also seen by
researchers [20,21] among heamodialysis patients. It was References
suggested due to effect of certain medications, such as
anti-coagulant therapy that could result in increased 1. Yaqub S, Kashif W, Raza MQ, Aaqil H, Shahab A, et al.
bleeding on probing among heamodialysis patients. This (2013) General practitioners' knowledge and
finding also shows that the increased bleeding on probing approach to chronic kidney disease in Karachi,
may not be taken as reflection of the level of inflammation Pakistan. Indian J Nephrol 23(3): 184-190.
(gingivitis or periodontitis) in heamodialysis patients.
Diabetes mellitus is a known systemic factor of 2. Bokhari SA, Khan AA (2009) Growing burden of non-
periodontitis and tooth loss. Both of study groups showed communicable diseases: the contributory role of oral
loss of periodontal attachment but diabetic group had

Anjum YM, et al. Oral Health Parameters of Diabetic and Non-Diabetic Copyright© Anjum YM, et al.
Patients Undergoing Heamodialysis- A Comparative Study. J Dental Sci 2016,
1(2): 000110.
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diseases, Eastern Mediterranean Region perspective. 13. Parmar SM (2002) Chronic renal disease. Br Med J
East Mediterr Health J 15(4): 1011-1020. 325(7355): 85-90.

3. Jafar TH, Schmid CH, Levey AS (2005) Serum 14. Meguid El, Nahas A, Bello AK (2005) Chronic kidney
creatinine as marker of kidney function in South disease: the global challenge. Lancet 365(9456): 331-
Asians: a study of reduced GFR in adults in Pakistan. J 340.
Am Soc Nephrol 16(5): 1413-1419.
15. Kinane DF (2001) Causation and pathogenesis of
4. Naqvi SAJ (2009) Renal diseases in Pakistan - ‘time to periodontal disease. Periodontol 2000 25: 8-20.
act.’ J Nephrol Renal Transplant 2(1): 133-135.
16. Yoshihara A, Deguchi T, Hanada N, Miyazaki H (2007)
5. Ullah K, Butt G, Masroor I, Kanwal K, Kifayat F (2015) Renal function and periodontal disease in elderly
Epidemiology of Chronic Kidney Disease in a Japanese. J periodontal 78(7): 1241-1248.
Pakistani Population. Saudi J Kidney Dis Transpl
26(6): 1307-1310. 17. Parkar S, Ajithkrishnan C (2012) Periodontal status
in patients undergoing hemodialysis. Indian J Nephrol
6. National Kidney Foundation (2002) K/DOQI clinical 22(4): 246-250.
practice guidelines for chronic kidney disease:
Evaluation, classification, and stratification. Am J 18. Wahid A, Chaudhry S, Muhammad AB, Ayyaz AK,
Kidney Dis 39(2 Suppl 1): S1-266. Ayesha W (2014) Assessment of periodontal health
status of chronic kidney disease patients undergoing
7. Dreyer G, Hull S, Aitken Z, Chesser A, Yaqoob MM hemodialysis; a cross sectional descriptive study.
(2009) The Effect of Ethnicity on the Prevalence of JUMDC 5(1): 13-19.
Diabetes and Associated Chronic Kidney Disease. QJM
102(4): 261-269. 19. Marakoglu I, Gursoy K, Demirer S, Sezer H (2003)
Periodontal status of chronic renal failure patients
8. Chuang SF, Sung JM, Kuo SC, Huang JJ, Lee SY (2005) receiving hemodialysis. Yonsei Med J 44(4): 648-652.
Oral and Dental Manifestations in Diabetic and
Nondiabetic Uremic Patients Receiving Hemodialysis. 20. Bayraktar G, Kurtulus I, Duraduryan A, Cintan S,
Oral Surg, Oral Med, Oral Pathol, Oral Radiol, Endod Kazancioglu R, et al. (2007) Dental and periodontal
99(6): 689-695. findings in hemodialysis patients. Oral Dis 13(4): 393-
397.
9. Abubekir E, Ummuhan T, Mustafa K, Varol C (2012)
Assessment of Oral Health in Peritoneal Dialysis 21. Lin BP, Taylor GW, Allen KJ, Ship JA (1999) Dental
Patients With and Without Diabetes Mellitus. Perit caries in older adults with diabetes mellitus. Spec
Dial Int 32(1): 81-85. Care Dentist 19(1): 8-14.

10. Ahmed El Lithy, Rana M Abdella, Yahia M El-Faissal, 22. Morioka T, Emoto M, Tabata T, Shoji T, Tahara H, et al.
Ahmed M Sayed, Rasha M Samie (2014) The (2001) Glycemic control is a predictor of survival for
Relationship between Low Maternal Serum Vitamin D diabetic patients on hemodialysis. Diabetes Care
Levels and Glycemic Control in Gestational Diabetes 24(5): 909-913.
Assessed by HbA1c Levels: An Observational Cross-
sectional Study. BMC Pregnancy Childbirth BMC 23. Castillo A, Mesa F, Liebana J, GarciaMartinez O, Ruiz S,
Pregnancy and Childbirth 14: 362. et al. (2007) Periodontal and oral microbiological
status of an adult population undergoing
11. Cockcroft DW, Gault MH (1976) Prediction of haemodialysis: a cross-sectional study. Oral Dis
creatinine clearance from serum creatinine. Nephron 13(2): 198-205.
16(1): 31-41.
24. Klassen JT, Krasko BM (2002) The dental health
12. WHO (1997) World Health Organization Oral Health status of dialysis patients. J Can Dent Assoc 68(1): 34-
Surveys-Basic methods. Geneva WHO Oral Health 38.
Country/Area Profile Program.

Anjum YM, et al. Oral Health Parameters of Diabetic and Non-Diabetic Copyright© Anjum YM, et al.
Patients Undergoing Heamodialysis- A Comparative Study. J Dental Sci 2016,
1(2): 000110.