Sociodemographic, Clinical, and Laboratory Parameters Related with Presence of Regular Toothbrushing in Hemodialysis Patients

Abstract

Introduction: Regular toothbrushing (TB) has been shown to be related with better oral health. Studies have shown that various sociodemographic and clinical factors were related with regular TB in general population with normal renal function. However, no study had analyzed the factors related with regular TB in hemodialysis (HD) patients. Methods: The laboratory parameters, depressive symptoms, health-related quality of life, sleep quality, and cognitive function were measured for all patients. Self-reported TB frequency was determined from all patients. Results: The frequency of patients TB were as follows: More than once a day (n = 20), once a day (n = 39), 2–5 times a week (n = 7), at most once a week (n = 16), at most once at 15 days (n = 21), at most once a month (n = 24), and never brushers (n = 8). Patients were dichotomized mainly into two groups: Group 1 was composed of 59 patients with regular TB (sum of patients with TB more than once a day and once a day) and Group 2 was composed of other 76 patients with irregular TB. In most of the domains of short form 36 (SF-36), cognitive function was higher, whereas depressive symptoms were lower in Group 1 patients when compared with Group 2 patients. Backward logistic regression analysis demonstrated that lower depression scores, lower high-sensitive C-reactive protein levels, higher cognitive function, and being middle school graduate or higher were independently related with regular TB. Conclusion: Regular TB is relatively low in HD patients. Preventive measures should be taken to improve regular TB in HD patients.

• cognitive function
• depression
• hemodialysis
• quality of life
• toothbrushing

INTRODUCTION

Oral health is regarded as a major global public health problem in the twenty-first century by the World Health Organization.¹ In adolescents, dental health is a useful indicator of general health.² Thus, it is important to take preventive measures for poor oral health behavior. However, to formulate better preventive measures, epidemiological data on social and behavioral risk factors of dental health problems are to be clarified.³ Indeed, it was hypothesized that neglecting dental health care may be connected with a wider complex of problems in adolescent lifestyles and problematic behaviors are correlated and form several dimensions.⁴ These issues may even be more important in hemodialysis (HD) patients by variety of reasons. First, the incidence of many of dental conditions, such as periodontal disease, narrowing of the pulp chamber enamel abnormalities, premature tooth loss, and xerostomia, seems greater than healthy population.⁵ Second, poor oral hygiene has been shown to be related with variety of conditions such as malnutrition, inflammation, and atherosclerosis.^5–7 Third, poor oral health has been shown to be related with morbidity and mortality in these patients.^5,8 Lastly, ensuring healthy dentition becomes increasingly important when a patient is a candidate for renal transplantation and on renal transplantation waiting list, given the fact that immunosuppressive protocols that may further predispose to oral and possibly disseminated infection.⁵ Although these issues are well known, there are very scarce data in the literature regarding the dental care as well as primary preventive measures in HD patients.⁵ As toothbrushing (TB) is a good measure of oral health behavior, the current study was performed to analyze two issues: first, to determine regular TB frequency in HD patients and second, to determine factors related with regular TB in HD patients.

MATERIALS AND METHODS

The observational study was performed on regular HD patients with end-stage renal disease receiving HD therapy weekly thrice. The study was in accordance with the declaration of Helsinki and local ethical approval and informed consent was obtained before enrolment. We recorded the sociodemographic and clinical characteristics of the patients including age, gender, living status (living alone or with partner), education status (illiterate, elementary school, secondary school, high school, and university graduate), marital status, economical status (whether monthly income is satisfactory or unsatisfactory), smoking status, previous renal transplantation (present or absent), etiologies of renal disease, presence of coronary artery disease, presence of diabetes mellitus, and presence of cerebrovascular disease. None of the patients were taking antidepressants and nutritional support during the study period. There were no patients in our study showing antibodies against human immunodeficiency virus, and there were no intravenous drug users. None of the patients were reported alcohol intake.

Body mass index (BMI) was calculated as the ratio of dry weight in kilograms (end-dialysis weight) to height squared (in square meters).

Patients with Alzheimer disease, patients who were taking antidepressants, and patients who did not want to participate were excluded. Coronary artery disease was defined as the presence of previous myocardial infarction, angina pectoris, or coronary revascularization procedure. All included HD patients were undergone complete physical examination. The dialysis prescription in our study included 4–5 h of HD, weekly thrice for all patients with flow rates of 300–400 mL/min, using standard bicarbonate dialysis solution. All patients were clinically euvolemic. Urea kinetic modeling was performed in order to assess the delivered equilibrated dose of dialysis. Hemodialysis dose was evaluated using the following formula: where spKt/V is a single-pool Kt/V, R is the ratio of post-dialysis to pre-dialysis serum urea nitrogen, t is the time of dialysis in hours, UF is the amount of ultrafiltration in liters, and W is the post-dialysis body weight in kilograms.

The laboratory parameters including pre-dialysis blood urea nitrogen and creatinine, hemoglobin, albumin, high-sensitive C-reactive protein (hs-CRP), calcium and phosphorus, serum iron, ferritin, total cholesterol, high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, triglyceride, and intact parathyroid hormone (iPTH) were measured before the beginning of HD session. Post-dialysis serum urea nitrogen levels, used to calculate urea reduction ratio, were also measured.

After being given a brief explanation, measurements of depressive behavior using Beck Depression Inventory (BDI), health-related quality of life (HRQOL) using short form 36 (SF-36), and cognitive function using standardized mini-mental state examination (SMMSE) were performed for each patient during regularly scheduled dialysis treatments. Sleep disturbance was also assessed for all patients (defined in terms of frequent awakenings, difficulty falling asleep, or poor quality of sleep). Assistance was available for patients who were illiterate.

Beck Depression Inventory

The BDI, which was originally introduced by Beck et al., is a 21-item self-reported inventory that measures characteristic attitudes and symptoms of depression.⁹ The 21 items are answered on a 4-point Likert scale, in which 0 represents the absence of a problem and 3 represents the extreme severity of a problem. The total score ranges from 0 to 63. The BDI is documented as a valid index of depression and the BDI scores correlate well with the diagnostic criteria for depression. It has been found to be a useful screening tool in HD patients.¹⁰

Quality of Life Assessment

In order to evaluate the HRQOL of the patients, a short form of medical outcomes study (SF-36) was used.¹¹ The test consists of 36 items, which are assigned to eight subscales. Each subscale is scored with a range from 0 to 100. The higher the scale, the better is the HRQOL. These eight subscales can be summarized in a Physical Component Summary (PCS) score and Mental Component Summary (MCS) score. SF-36 has been commonly used and validated in patients with end-stage renal disease.¹²

Measurement of Cognitive Function

The SMMSE was used for the analysis of cognitive function. The SMMSE scores range from 30 (unimpaired) to 0 (impaired).¹³ It provides a global score of cognitive ability that correlates with function in activities of daily living. The SMMSE is a reliable instrument that allows practitioners to accurately measure cognitive deficits and deterioration over time.¹⁴ The Turkish version of the SMMSE has been validated and shown to be reliable in the Turkish population.¹⁵

Statistical Analysis

Statistical analysis was performed using SPSS 15.0 for Windows (SPSS Inc., Evanston, IL, USA). The normality of the data was evaluated by the Kolmogorov–Smirnov test (Lilliefors modification). Data are shown as mean ± standard deviation and percentage (%). Results were considered statistically significant if two-tailed p value is less than 0.05. Comparisons between two groups were assessed by means of t test for normally distributed continuous variables and by Mann–Whitney U test for non-normally distributed continuous variables. For the analysis of categorical variables, chi-square test was used. Backward multivariate logistic regression analyses were performed to assess the independent association of several variables with regular TB. The effects were measured by odds ratios (ORs) and 95% confidence intervals (CIs) based on logistic regression models.

RESULTS

Initially, 200 patients were recruited. One patient with Alzheimer disease, three patients taking antidepressants, and 61 patients who did not want to participate were excluded. The response rate was 68.9%. The final population consisted of 135 patients. The etiologies of end-stage renal disease were as follows: diabetes mellitus (n = 44), hypertension (n = 29), glomerulonephritis (n = 14), amyloidosis (n = 7), vesicourethral reflux and pyelonephritis (n = 11), nephrolithiasis (n = 3), polycystic kidney disease (n = 3), ischemic nephropathy (n = 2), analgesic nephropathy (n = 1), contrast nephropathy (n = 1), and unknown (n = 20). Four patients had hepatitis B surface antigen (Hbs) positivity and nine patients had antihepatitis C anticore (anti-HCV) positivity. The dialysis access was arteriovenous fistula for 110 patients, arteriovenosa graft for 8 patients, and central venous catheter for 17 patients. The frequency of TB were as follows: more than once a day (n = 20 patients), once a day (n = 39), 2–5 times a week (n = 7), at most once a week (n = 16), at most once at 15 days (n = 21), at most once a month (n = 24), and never brushers (n = 8).

For the sake of simplicity and performing statistical analysis, patients were dichotomized into two groups: Group 1 and Group 2. Group 1 is composed of 59 patients with regular TB (sum of patients with TB more than once a day and once a day) and Group 2 is composed of 76 patients with irregular TB (sum of patients with frequency of TB 2–5 times a week, at most once a week, at most once at 15 days, at most once a month, and never brushers. In Group 1, 22 (37.3%) patients had a dentist visit in last year, and in Group 2, 17 (22.4%) patients had a dentist visit in last year (p = 0.058). The baseline data of whole patient population, Group 1, and Group 2 are shown in Table 1. The comparative clinical and laboratory data of 135 HD patients are shown in Table 2. The comparative data of quality of life, depression scores, and cognitive function of HD patients are shown in Table 3.

Table 1.  The baseline demographic characteristics of 135 hemodialysis patients.

Parameter	Total	Group 1 (n = 59)	Group 2 (n = 76)	p
Gender (male/female) (n)	73/62	42/17	31/45	<0.0001**
Age (years)^a	52.4 ± 13.6	46.9 ± 11.9	56.7 ± 13.4	<0.0001***
Hemodialysis duration (months)^a	63.6 ± 53.6	66.0 ± 58.4	61.81 ± 49.9	0.852
Presence of coronary artery disease (yes/no) (n)	43/92	14/45	29/47	0.074**
Presence of hypertension (yes/no) (n)	91/44	38/21	53/23	0.512**
Presence of diabetes (yes/no) (n)	44/91	13/46	31/45	0.021**
Presence of cerebrovascular disease (n)	17/118	3/56	14/62	0.021**
Smoker/non-smoker (n)	41/94	20/39	21/55	0.432**
Presence of transplantation history (yes/no) (n)	8/127	7/52	1/75	0.01**
Educational status (illiterate/primary school/secondary school/tertiary school/university) (n)	41/50/11/25/8	1/25/8/17/8	40/25/3/8/0	<0.0001**
Monthly money income (satisfactory/non-satisfactory)	83/52	40/19	43/33	0.184**
Sleep disturbance (yes/no) (n)	76/59	37/22	39/37	0.185**
Married/non-married (n)	118/17	51/8	67/9	0.765**
Living status (alone or not) (n)	13/122	5/54	8/68	0.689**
Body mass index (kg/m^2)^a	24.4 ± 3.9	23.6 ± 3.4	24.9 ± 4.2	0.05***
Systolic BP (mmHg)^a	134.6 ± 21.1	135.1 ± 24.5	134.2 ± 17.9	0.819
Diastolic BP (mmHg)^a	79.3 ± 9.9	80.5 ± 11.2	78.3 ± 8.5	0.214***

Notes: BP, blood pressure.

^aMean ± standard deviation.

*p-Value depends on Mann–Whitney U test, **p-Value depends on chi-square test, ***p-Value depends on Student’s t test.

Table 2.  The comparative clinical and laboratory data of 135 hemodialysis patients.

	Total	Group 1 (n = 59)	Group 2 (n = 76)	p
Pre-dialysis hemoglobin (g/L)^a	113.0 ± 13.0	116.2 ± 14.1	110.7 ± 116.9	0.015
Pre-dialysis blood urea nitrogen (mmol/L)	23.67 ± 6.57	24.42 ± 6.89	23.06 ± 6.28	0.164
Pre-dialysis creatinine (μmol/L)^a	697.5 ± 221.0	743.4 ± 223.7	662.1 ± 213.9	0.034
Pre-dialysis albumin (g/L)^a	36.9 ±.5.8	37.2 ±.5.9	36.6 ±.5.7	0.485
Pre-dialysis serum iron (μmol/L)^a	12.3 ± 5.5	13.4 ± 5.1	11.4 ± 5.7	0.008
Pre-dialysis ferritin (ng/mL)^a	571.5 ± 424.7	516.6 ± 382.5	614.0 ± 452.6	0.200
hs-CRP (mg/dL)^a	4.05 ± 8.0	2.44 ± 2.99	5.25 ± 10.22	0.027
Intact parathyroid hormone (pg/mL)^a	349.3 ± 367.6	395.1 ± 440.3	313.9 ± 298.3	0.520
Pre-dialysis sodium (mmol/L)^a	137.4 ± 2.8	137.3 ± 2.6	137.4 ± 2.9	0.928
Pre-dialysis potassium (mmol/L)^a	5.21 ± 0.65	5.24 ± 0.60	5.18 ± 0.69	0.644
Pre-dialysis glucose (mmol/L)^a	6.90 ± 2.78	6.52 ± 2.19	7.21 ± 3.15	0.514
Pre-dialysis total cholesterol (mmol/L)^a	4.46 ± 1.0	4.35 ± 0.97	4.55 ± 1.01	0.282
Triglyceride (mmol/L)^a	1.96 ± 0.83	2.01.8 ± 0.81	1.93 ± 0.84	0.725
HDL-cholesterol (mmol/L)^a	0.95 ± 0.41	0.89 ± 0.30	0.98 ± 0.48	0.192
LDL-cholesterol (mmol/L)^a	2.62 ± 0.81	2.53 ± 0.82	2.70 ± 0.81	0.118
Pre-dialysis calcium (mmol/L)^a	2.23 ± 0.23	2.25 ± 0.25	2.20 ± 0.20	0.197
Pre-dialysis phosphorus (mmol/L)^a	1.64 ± 0.51	1.71 ± 0.48	1.59 ± 0.53	0.166
spKt /V^a	1.45 ± 0.25	1.42 ± 0.25	1.47 ± 0.25	0.266

Notes: hs-CRP, high-sensitive C-reactive protein; HDL, high-density lipoprotein; LDL, low-density lipoprotein.

^aMean ± standard deviation.

Table 3.  The comparative data of quality of life, depression scores, and cognitive function of 135 HD patients.

	Total	Group 1 (n = 59)	Group 2 (n = 76)	p
Physical functioning^a	39.6 ± 20.1	45.5 ± 21.2	35.0 ± 18.1	0.002
Role-physical limitation^a	34.5 ± 26.5	41.8 ± 28.1	28.8 ± 23.9	0.002
Bodily pain^a	25.0 ± 18.2	25.9 ± 17.6	24.3 ± 18.6	0.496
General health perception^a	37.6 ± 21.0	44.2 ± 22.7	32.5 ± 18.1	0.001
Vitality^a	36.2 ± 21.1	42.5 ± 21.7	31.4 ± 19.2	0.001
Social functioning^a	36.0 ± 26.9	42.2 ± 27.8	31.2 ± 25.3	0.018
Role emotional^a	36.1 ± 29.2	42.2 ± 29.3	31.3 ± 28.4	0.017
Mental health^a	43.9 ± 21.0	48.5 ± 21.3	38.7 ± 19.7	0.005
PCS^a	41.0 ± 14.3	45.8 ± 15.9	37.3 ± 11.6	0.002
MCS^a	39.8 ± 17.1	44.5 ± 18.2	36.0 ± 15.2	0.006
BDI score ^a	16.6 ± 10.7	13.2 ± 7.6	19.2 ± 11.9	0.003
SMMSE score^a	22.0 ± 5.1	24.5 ± 4.2	20.1 ± 4.8	<0.0001**

Notes: PCS, physical component summary score of SF-36; MCS, mental component summary score of SF-36; BDI, Beck Depression Inventory; SMMSE, standardized mini-mental state examination.

^aMean ± standard deviation.

*p-Value depends on Mann–Whitney U test, **p-Value depends on Student’s t test.

Table 4.  Independent factors related with regular toothbrushing.

	B	Exp (B)	95% Confidence interval	p
BDI score	−0.080	0.923	0.878–0.969	0.001
hs-CRP	−0.103	0.902	0.819–0.994	0.037
Being middle school graduate or higher	1.801	6.060	2.066–17.857	0.001
SMMSE score	0.118	1.124	1.016–1.245	0.023

Notes: Exp (B), odds ratio; BDI, Beck Depression Inventory; hs-CRP, high-sensitive C-reactive protein; SMMSE, standardized mini-mental state examination.

Backward logistic regression analysis were performed to determine the independent factors including age, gender, BMI, HD vintage, presence of dentist visit in last year, marital status, smoking status, presence of diabetes mellitus, presence of coronary artery disease, presence of cerebrovascular disease, monthly income, presence of sleep disturbance, presence of transplantation history, living status, spKt/V, albumin, hs-CRP, PCS score, MCS score, BDI score, SMMSE score, and educational status (dichotomized as middle school graduate or higher vs. illiterate or primary school) related with regular TB (dependent parameter). The results of the regression analysis are shown in Table 4.

DISCUSSION

In the current study, it was firstly demonstrated that HRQOL were better in patients with regular TB compared to patients without regular TB. Additionally, depressive behavior, cognitive function, educational status, and hs-CRP levels were independently associated with regular TB in HD patients.

Previously various studies have demonstrated that apart from diseases themselves, various sociodemographic and behavioral correlates of oral health status were present.¹⁶ Indeed, it was concluded that “total tooth loss is a social–behavioral issue as much as it is disease related”.¹⁷ It was reported that there were associations between total tooth loss and low income, education, perceived poor oral health, smoking, and negative health behavior.¹⁸ However, it was also concluded that the factors mentioned above may not be important in all populations.¹⁶

Hemodialysis patients are very specific group of patients, entirely different from general population. They have various co-morbidities (high prevalence of cardiac diseases, anemia, hypertension, etc.) and non-traditional pathologies (high prevalence of depression, malnutrition, inflammation, etc.). Additionally, these patients have to cope with various difficulties in daily living related with both dialysis therapy (such as regularly attending hospital for HD and taking multiple pills) and other social factors (such as sexual dysfunction, non-satisfactory, money income, and unemployment). Thus, it is not surprising that most of HD patients exhibit cognitive impairment, depression, sleep disorders, and impaired quality of life. All these factors may negatively impact oral health status in HD patients. Surprisingly, however, no previous study have examined the relationship between demographic characteristics, cognitive impairment, depression, sleep disorders, quality of life, and laboratory parameters with regular TB as a measure of better oral health behavior in HD patients.

In the current study, regular TB was found to be independently and inversely related with depressive behavior as evaluated by BDI. These findings were in accordance with the previous findings in general population.^19–21 Although the exact mechanisms regarding the depression and non-TB are not known, it was concluded that adolescents who do not brush regularly give up one possibility for achieving social acceptance and prestige. This may indicate the existence of other problems, such as indifference, low self-esteem, and underestimation of their abilities and depression.²²

Higher educational status and better cognitive function were related with regular TB in the present study. These findings are not surprising since previous studies have also shown very strong relationship between educational status and better oral hygiene.^4,23,24

Lastly, serum hs-CRP levels showed inverse association with regular TB in the current study. It is well known that TB is effective for removing the main etiologic factor in periodontal disease, plaque, from all surfaces of the teeth.²⁵ Thus, it was concluded that regular TB behavior can be regarded as a proxy of periodontal disease including periodontitis.²⁶ Since periodontitis is a chronic inflammatory disease of the periodontal tissues and absence of regular TB may be related with peritonitis,²⁷ finding of inverse relationship between hs-CRP and regular TB makes also sense in HD patients.

The present results should be interpreted in light of limitations that include a cross-sectional design and use of self-reported measures. As this is a cross-sectional study, cause and effect relationship cannot be suggested. Second, results were based on self-reported frequency of TB and periodontal status was not assessed by a dentist. However, it was suggested that regular TB behavior can be regarded as a proxy of periodontal disease.²³ Additionally, measures of oral hygiene such as TB have been associated with clinically confirmed periodontal disease.²⁸ Detailed dietary intake, lifestyles involving eating habits of sweets, and so on may confound the relationship. We could not analyze this point since information was unavailable.

In conclusion, the present study firstly demonstrated that regular TB is relatively infrequent in HD patients. Depression, cognitive function, educational status, and chronic inflammation were closely related with TB in HD patients.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.