BioMed Research International
Volume 2015 (2015), Article ID 897674, 7 pages
http://dx.doi.org/10.1155/2015/897674

Clinical Study

Oral Tori in Chronic Hemodialysis Patients

Pei-Jung Chao,¹ Huang-Yu Yang,2,3 Wen-Hung Huang,2,3 Cheng-Hao Weng,2,3 I-Kuan Wang,⁴ Aileen I. Tsai,¹ and Tzung-Hai Yen2,3,5

¹Department of Pediatric Dentistry, Chang Gung Memorial Hospital and College of Medicine, Chang Gung University, Linkou 333, Taiwan
²Department of Nephrology and Division of Clinical Toxicology, Chang Gung Memorial Hospital and College of Medicine, Chang Gung University, Linkou 333, Taiwan
³Kidney Research Center, Chang Gung Memorial Hospital, Linkou 333, Taiwan
⁴Department of Nephrology, China Medical University Hospital and College of Medicine, China Medical University, Taichung 404, Taiwan
⁵Center for Tissue Engineering, Chang Gung Memorial Hospital, Linkou 333, Taiwan

Received 11 January 2015; Accepted 16 March 2015

Academic Editor: Takashi Saku

Copyright © 2015 Pei-Jung Chao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Background. This study investigated the epidemiology of torus palatinus (TP) and torus mandibularis (TM) in hemodialysis patients and analyzed the influences of hyperparathyroidism on the formation of oral tori. Method. During 2013, 119 hemodialysis patients were recruited for dental examinations for this study. Results. The prevalence of oral tori in our sample group was high at 33.6% (40 of 119). The most common location of tori was TP (70.0%), followed by TM (20.0%), and then both TP and TM (10.0%). Of the 40 tori cases, most (67.5%) were <2 cm in size; moreover, the majority (52.5%) were flat in shape. In symmetry, most (70.0%) occurred in the midline, followed by bilateral sides (20.0%). Notably, the levels of intact parathyroid hormone did not differ in patients with or without tori (). Furthermore, patients with tori did not differ from patients without tori in inflammatory variables such as log high-sensitivity C-reactive protein () or nutritional variables such as albumin (). Finally, there were no differences between patients with and without tori in adequacy of dialysis (). Conclusions. Neither hyperparathyroidism nor inflammation malnutrition syndrome was found to contribute to the formation of oral tori in chronic hemodialysis patients. Further studies are warranted.

1. Introduction

Tori or exostoses are described as nonpathologic, localized bony protuberances that arise from the cortical bone and sometimes the spongy layer. The two most common exostoses that occur in two specific intraoral locations, on the midline of the hard palate and the lingual aspect of the mandible in the cuspid/premolar region, are termed TP and TM [1]. TP is an exophytic nodular mass of bone that rises along the midline suture of the hard palate. In contrast, TM is a bony exophytic growth located on the cuspid/premolar area of the lingual surface of the mandible and superior, usually bilaterally, to the mylohyoid ridge [1]. Morphologically, tori are classified as flat, spindle, nodular, and lobular [1].

The discovery of these exostoses usually occurs incidentally during a routine dental examination, as they generally do not produce any symptoms (except in cases of significant growth or in edentulous patients, in which case they can hinder the construction of the prosthesis) [2]. Despite the numerous studies, their origin is unclear [3]; numerous potential causes are presented in literature, but none are definitive. Certain prevalence with respect to ethnic groups, sex, and age has also been observed [4–18].

The exact etiology of oral tori has eluded investigators for decades, but it is believed that the trait is expressed when a certain threshold of genetic and local environmental factors is surpassed [19–21]. Historically, studies on the etiology of these bony lesions have focused on genetic and environmental influences, but they have neglected to investigate the broad scope of interdependent factors involved in bone or mineral metabolism.

Taiwan continues to report the highest rate of prevalent end-stage renal disease (ESRD) in the world. According to 2014 Annual Data Report of United States Renal Data System [22], the number of ESRD patients per million receiving chronic dialysis in 2012 varied more than 20-fold across countries, from 2,902 and 2,365 in Taiwan and Japan, respectively, to 133–185 in South Africa, Russia, and the Philippines [22]. Therefore, it is speculated that many of our hemodialysis patients might have a different epidemiology of oral tori due to an underlying chronic kidney disease-mineral and bone disease or inflammation malnutrition syndrome.

Abnormal calcium, phosphorus, and vitamin D metabolism are very common in patients with ESRD [23]. Metabolic disturbances in these patients result in the prolonged stimulation of the parathyroid glands. This results in the increased synthesis and release of parathyroid hormone and causes secondary hyperparathyroidism. Hyperparathyroidism causes the skeletal disturbances that are characteristic of renal osteodystrophy [23].

In a pilot study, Sisman et al. [16] investigated the prevalence, size, location, and shape of TP in 91 ESRD patients receiving peritoneal dialysis. A higher prevalence of TP (41.7%) and the significant relationship between duration of renal dialysis and size of TP were reported. They attributed the development of TP to an underlying disorder, such as renal osteodystrophy [16].

Therefore, the objective of this study was to undertake a broader assessment of potential environmental influences and, in doing so, address the following question: in hemodialysis patients with oral tori, are there associations with molar relationships, medical conditions, chronic kidney disease-mineral and bone disease, or inflammation malnutrition syndrome?

2. Material and Methods

2.1. Ethical Statement

This clinical study followed the Declaration of Helsinki and was approved by the Medical Ethics Committee of Chang Gung Memorial Hospital.

2.2. Patients

All hemodialysis patients were recruited from Chang Gung Memorial Hospital at Linkou, Taiwan. This observational study included 119 patients. All patients who agreed to participate in this study were enrolled, excluding those with malignancies [24], active infectious diseases, hospitalizations, or surgery or kidney transplants in the past 3 months and those on hemodialysis for less than 3 months or intoxicated by lead [25, 26] or cadmium [27, 28]. All enrolled patients underwent 4 hours of hemodialysis, 3 times a week. Hemodialysis was performed with single-use hollow-fiber dialyzers equipped with modified cellulose-based polyamide or polysulfone membranes. The dialysate used was a standard ionic composition and bicarbonate-based buffer. Patients with hypertension took antihypertensive medications regularly, except diuretics. Blood sugar was controlled with insulin therapy and the glucose level regularly monitored. Smoking habits and alcohol consumption were also recorded.

2.3. Groups

Patients who met the inclusion criteria were classified into 2 groups according to the presence or absence of oral tori.

2.4. Laboratories

Blood specimens were collected within a few days of a clinical examination that occurred during stable hemodialysis sessions to minimize the effect of any acute events. Blood was drawn from the arterial end of the vascular access immediately before hemodialysis, centrifuged, and then stored at −70°C until used in assays. Serum levels of albumin, blood urea nitrogen, and creatinine, transferring saturation, and normalized protein catabolic rate were measured and used as nutritional markers. The high-sensitivity C-reactive protein, which was used as an inflammatory biomarker, was analyzed by immunonephelometry (Nanopia CRP; Daiichi, Tokyo, Japan). The lowest detection limit was 0.15 mg/L. All other data were obtained with standard laboratory procedures using an automatic analyzer. The normalized protein catabolic rate in hemodialysis patients was calculated using validated equations, and it was normalized to body weight. Dialysis clearance of urea was expressed as , as reported by Daugirdas [29]. Serum levels of calcium, phosphate, and intact parathyroid hormone were also measured and the corrected serum calcium level was calculated as follows: calcium (mg/dL) = [0.8 (4.0 − albumin [g/dL])].

2.5. Diagnosis of Oral Tori

The same dentist examined all patients and used mouth mirrors or tongue blades to check the oral condition of these patients. The examination for oral tori consisted of inspection and palpation. TP (Figure 1) was defined as a raised bony exostosis along the midline of the hard palate whereas TM was defined as exostosis that develops along the lingual aspect of the mandible. The maximum elevation of the outgrowth of tori was used to measure the size of tori. Tori were graded according to previous description as being >2 cm or <2 cm using a periodontal probe, as described by Gorsky et al. [4]. The shape of tori was classified as flat, spindle, nodular, or lobular according to the criteria described by Jainkittivong et al. [5]. The locations of tori were classified as being in the upper arch, lower arch, or upper and lower arches. The molar relationship was classified as Class I, Class II, or Class III, as defined previously [30].

Figure 1: Torus palatinus. Intraoral view of one of the hemodialysis patients with a flat torus palatinus (asterisk) which is an exophytic nodular bony mass that arises along the midline of the hard palate.

2.6. Statistical Analysis

Continuous variables were expressed as a mean with a standard deviation, while categorical variables were expressed as numbers and percentages in brackets. All data were tested for normality of distribution and equality of standard deviation before analysis. As the high-sensitivity C-reactive protein data were not normally distributed, these data were log transformed before being entered into the regression model. Comparisons between the 2 groups of patients were performed using Student’s -test for quantitative variables and Chi-square or Fisher’s exact tests for categorical variables. The criterion for significance was a 95% confidence interval to reject the null hypothesis. All analyses were performed using IBM SPSS Statistics Version 20.0.

3. Results

3.1. Subject Characteristics

The patients were aged years with roughly equal sex distribution (Table 1). Of the 119 patients with ESRD, 40 were found to have oral tori, and the prevalence rate in our hemodialysis population was 33.6%. Nevertheless, there were no significant differences in baseline demographic variables between both groups ().

Table 1: Baseline characteristics of hemodialysis patients with or without oral tori formation (n = 119).

Variable
All patients (n = 119)
Patients with oral tori (n = 40)
Patients without oral tori (n = 79)
value

Age, year
59.8 ± 14.7
60.0 ± 13.2
59.7 ± 15.5
0.905

Male sex, (%)
60 (50.4)
18 (45.0)
42 (53.2)
0.400

Body mass index, kg/m²
22.3 ± 3.4
22.7 ± 3.7
22.1 ± 3.2
0.360

Diabetes mellitus, (%)
47 (39.5)
19 (47.5)
28 (35.4)
0.204

Hypertension, (%)
66 (55.5)
23 (57.5)
43 (54.4)
0.750

Smoking habit, (%)
27 (22.7)
8 (20)
19 (24.1)
0.618

Alcohol consumption, (%)
20 (16.8)
5 (12.5)
15 (19.0)
0.371

3.2. Laboratory Findings

Patients with oral tori did not differ from patients without tori in their level of intact parathyroid hormone ( pg/mL versus  pg/mL, , Table 2). Furthermore, patients with and without oral tori did not differ in inflammatory variables such as log high-sensitivity C-reactive protein ( mg/L versus  mg/L, ) or nutritional variables such as albumin ( g/dL versus  g/dL, ).

Table 2: Laboratory findings of hemodialysis patients with or without oral tori formation (n = 119).

Variable
All patients (n = 119)
Patients with oral tori (n = 40)
Patients without oral tori (n = 79)

Blood urea nitrogen, mg/dL
73.4 ± 20.3
73.5 ± 14.6
73.4 ± 22.7
0.976

Creatinine, mg/dL
10.3 ± 2.2
10.1 ± 2.3
10.5 ± 2.2
0.370

Uric acid, mg/dL
7.1 ± 1.3
6.8 ± 1.2
7.2 ± 1.3
0.117

Sodium, mEq/L
137.9 ± 3.1
137.8 ± 3.3
138.2 ± 2.7
0.521

Potassium, mEq/L
4.8 ± 0.8
4.8 ± 0.8
4.8 ± 0.7
0.767

Chloride, mEq/L
97.8 ± 3.5
97.8 ± 3.2
97.9 ± 3.7
0.916

Calcium, mg/dL
9.6 ± 1.0
9.6 ± 0.9
9.7 ± 1.0
0.571

Inorganic phosphorus, mg/dL
5.3 ± 1.6
5.1 ± 1.3
5.4 ± 1.7
0.346

Bicarbonate, mmol/L
23.0 ± 2.7
23.0 ± 3.1
23.0 ± 2.5
0.942

Fasting glucose, mg/dL
126.4 ± 69.9
125.4 ± 52.9
126.9 ± 77.4
0.912

Albumin, g/dL
3.9 ± 0.3
4.0 ± 0.3
3.9 ± 0.1
0.247

Total bilirubin, mg/dL
0.3 ± 0.2
0.3 ± 0.1
0.3 ± 0.2
0.547

Aspartate aminotransferase, U/L
20.6 ± 9.1
19.3 ± 6.3
21.3 ± 10.1
0.241

Alanine aminotransferase, U/L
16.6 ± 12.0
17.5 ± 15.4
16.1 ± 10.0
0.544

Alkaline phosphatase, U/L
95.7 ± 86.1
96.9 ± 94.0
95.1 ± 82.5
0.917

Gamma-glutamyl transferase, U/L
42.8 ± 62.6
41.9 ± 51.6
43.2 ± 67.8
0.918

Total cholesterol, mg/dL
168.7 ± 42.1
173.5 ± 29.2
166.2 ± 47.3
0.379

High-density lipoprotein, mg/dL
44.0 ± 17.7
42.2 ± 15.5
44.9 ± 18.7
0.434

Low-density lipoprotein, mg/dL
95.1 ± 35.9
99.2 ± 27.9
93.0 ± 39.3
0.383

Triglyceride, mg/dL
149.9 ± 99.4
162.5 ± 87.1
143.4 ± 105.0
0.325

Red blood cell count, 10⁶/uL
3.5 ± 0.6
3.6 ± 0.6
3.4 ± 0.5
0.038*

Hemoglobin, g/dL
10.2 ± 1.4
10.5 ± 1.3
10.0 ± 1.3
0.058

Hematocrit, %
31.2 ± 4.1
32.2 ± 4.0
30.6 ± 4.0
0.048*

Mean corpuscular volume, fL
91.0 ± 6.6
90.2 ± 7.3
91.3 ± 6.2
0.367

Red blood cell distribution width, %
14.4 ± 1.4
14.2 ± 1.2
14.5 ± 1.4
0.230

Platelet count, 10³/uL
190.8 ± 58.7
199.7 ± 61.1
186.2 ± 57.3
0.239

White blood cell count, 10³/uL
6.5 ± 1.9
7.1 ± 2.0
6.2 ± 1.9
0.025*

Intact parathyroid hormone, pg/mL
379.7 ± 390.1
354.0 ± 477.3
392.7 ± 340.3
0.611

Iron, ug/dL
63.9 ± 26.6
69.8 ± 29.0
60.9 ± 25.0
0.086

Total iron binding capacity, ug/dL
251.6 ± 52.0
253.2 ± 55.9
250.8 ± 50.3
0.816

Transferrin saturation, %
26.1 ± 11.5
28.2 ± 11.9
25.0 ± 11.2
0.153

Ferritin, ng/mL
361.3 ± 297.2
284.3 ± 263.7
400.8 ± 307.2
0.043*

Log high-sensitivity C-reactive protein, mg/L
0.6 ± 0.6
0.6 ± 0.6
0.6 ± 0.6
1.000

Note: *.

3.3. Dialysis-Related Data

There were no significant differences in hemodialysis adequacy between patients with and without oral tori (, versus , , Table 3).

Table 3: Dialysis-related data of hemodialysis patients with or without torus formation (n = 119).

Variable
All patients (n = 119)
Patients with oral tori (n = 40)
Patients without oral tori (n = 79)
value

Residual glomerular filtration rate, mL/min
2.8 ± 3.25
3.1 ± 3.5
2.7 ± 3.2
0.569

Urea reduction ratio
0.8 ± 0.1
0.8 ± 0.1
0.8 ± 0.1
1.000

Kt/V (Daugirdas [29])
1.7 ± 0.3
1.7 ± 0.4
1.7 ± 0.3
0.577

Normalized protein catabolic rate, g/kg/day
1.4 ± 0.6
1.4 ± 0.7
1.3 ± 0.5
0.460

Time-averaged concentration of urea, mg/dL
45.2 ± 13.9
44.6 ± 9.7
45.5 ± 15.6
0.742

3.4. Clinical Findings of Oral Tori

As shown in Table 4, the most common location of tori was TP (70.0%), followed by TM (20.0%). The incidence of tori that occurred in both upper and lower arch was 10.0%. Of the 40 tori cases, most (67.5%) were <2 cm in size and, in addition, most (52.5%) were flat in shape. In symmetry, most (70.0%) were in the midline, followed by bilateral sides (20.0%).

Table 4: Clinical findings of oral tori (n = 40).

Variable
Findings, (%)

Location

    Upper
28 (70.0)

    Lower
8 (20.0)
Unilateral
2 (5.0)
Left
1 (2.5)

Right
1 (2.5)

Bilateral
6 (15.0)

    Upper and lower
4 (10.0)
Unilateral
2 (5.0)
Left
1 (2.5)

Right
1 (2.5)

Bilateral
2 (5.0)

Size

    <2 cm
27 (67.5)

    >2 cm
13 (32.5)

Shape

    Flat
21 (52.5)

    Spindle
1 (2.5)

    Nodular
16 (40.0)

    Lobular
2 (5.0)

Symmetry

    Unilateral
4 (10.0)

    Bilateral
8 (20.0)

    Midline
28 (70.0)

3.5. Molar Relationship

The molar relationship could not be defined in most patients (50.4%) due to the loss of first molars (Table 5). There was no significant difference in molar relationship between both groups ().

Table 5: Comparison of molar relationship between hemodialysis patients with and without oral tori formation (n = 119).

Variable
All patients
(n = 119)
Patients with torus (n = 40)
Patients without torus (n = 79)
value

Molar relationship

    No, (%)
60 (50.4)
21 (52.5)
39 (49.4)
0.400

    Class I, (%)
50 (42.0)
14 (35.0)
36 (45.6)

    Class II, (%)
3 (2.5)
2 (5)
1 (1.3)

    Class III, (%)
6 (5.0)
3 (7.5)
3 (3.8)

4. Discussion

Few data are available regarding the prevalence rate of oral tori in chronic hemodialysis patients; this is the first study examining the prevalence of oral tori in patients with ESRD in Taiwan. Our data revealed that 40 out of 119 (33.6%) hemodialysis patients had oral tori. TP generally occurs in anywhere from 4.1 to 60.5% of the population, and different studies have reported marked differences among various ethnic groups (Table 6). Chiang et al. [17] investigated oral mucosal anomalies in 2050 dental patients of a hospital in Taiwan and reported that the prevalence rate of TP was 21.1%. Thus, this study showed the slightly higher prevalence of TP (23.5%) in patients receiving hemodialysis. Our results also demonstrated a high prevalence of TP, similar to the results of a study by Sisman et al. [16]; 41.7% of the patients had TP.

Table 6: Comparison of prevalence rate of oral tori from different studies.

Study
Year
Geographic area
Sample size,
Population
TP, %
TM, %

Reichart et al. [6]
1988
German
1317
Nonuremic
13.5
5.2

Reichart et al. [6]
1988
Thailand
947
Nonuremic
23.1
9.2

Shah et al. [8]
1992
India
1000
Nonuremic
9.5
1.4

Gorsky et al. [4]
1996
Israel
1002
Nonuremic
21.0

Ruprecht et al. [15]
2000
USA
1600
Nonuremic

16.9*

Bruce et al. [9]
2004
Ghana
926
Nonuremic
4.3
12.1

Yildiz et al. [10]
2005
Turkey
1943
Nonuremic
30.9

Jainkittivong et al. [5]
2007
Thailand
1520
Nonuremic
60.5
32.2

Sawair et al. [11]
2009
Jordan
618
Nonuremic
15.4
25.7

Sisman et al. [7]
2008
Turkey
2660
Nonuremic
4.1

Yoshinaka et al. [12]
2010
Japan
664
Nonuremic
17

Simunkovic et al. [13]
2011
Croatia
1679
Nonuremic
42.9
12.6

Mishra et al. [18]
2011
Malaysia
65
Nonuremic
50.8
4.6

Sisman et al. [16]
2012
Turkey
91
Uremic
41.7

Chiang et al. [17]
2014
Taiwan
2050
Nonuremic
21.1
24.2

Yoshinaka et al. [14]
2014
Japan
664
Nonuremic

29.7

Current study
2014
Taiwan
119
Uremic
23.5
6.7

Note: TP: torus palatinus; TM: torus mandibularis; *radiographic study.

The present study examined not only TP but also TM. Sisman et al. [16] only reported the prevalence of TP. Our study showed that TP occurred in 28 patients (23.5%), TM occurred in 8 patients (6.7%), and both TP and TM occurred in 4 patients (3.4%). It appears that TP is the major form of oral tori in patients undergoing hemodialysis therapy. However, Chiang et al. [17] found that the prevalence of TM (24.2%) was slightly higher than the prevalence of TP (21.1%).

The TP shapes were classified as flat, spindle, nodular, or lobular according to the criteria described by Jainkittivong et al. [5]. However, the TM shapes were not classified. In this study, we found flat tori to be the most common TP type. Numerous studies agree with this finding of flat TP being the most common shape [5, 31–33]. Studies by Reichart et al. [6], Sisman et al. [16], and Jainkittivong et al. [5], however, reported that spindle-shaped TP was the most common type. Sisman et al. [7], in 2008, surveyed a regional population in Turkey and reported that flat TP was most common there. Sisman et al. [16] speculated that the difference between these two studies in most common TP type, which were conducted in the same region, might be due to an underlying disorder, such as renal osteodystrophty, in the ESRD patients.

Nevertheless, we found in this study that patients with and without oral tori did not differ in levels of intact parathyroid hormone (). Furthermore, patients with and without oral tori also did not differ in inflammatory variables such as log high-sensitivity C-reactive protein () or nutritional variables such as albumin (). Therefore, it was very difficult to attribute tori formation in the hemodialysis patients to uremic milieu, inflammation malnutrition syndrome, or renal osteodystrophy. Sisman et al. [16] revealed that the prevalence of TP in ESRD patients undergoing peritoneal dialysis was higher (41.7%) compared to other Turkish reports and especially compared to the study by Sisman et al. [7] (4.1%) that was performed in the same region but in the general population. On the other hand, the present study demonstrated a slightly higher prevalence of TP (23.5%) in hemodialysis patients than general population (21.1%) [17].

The molar relationship could not be defined in most patients (50.4%) due to loss of first molars. In addition, there was no significant difference in molar relationship between patients with and without tori (). In 1999, Sonnier et al. [34] examined the prevalence of 3 types of exostoses in a sample of 328 modern American skulls drawn from the collection at the American Museum of Natural History. It was revealed that TP was observed in 56% of all skulls, was commonly associated with second and third molars, and was usually directly lateral to and a mean of 11.4 mm from the greater palatine foramen [34]. Mishra et al. [18] also found that TP was often located at the combined premolar to molar areas. Gorsky et al. [4] reported that the prevalence of TP in the combined molar-premolar area increased with age, whereas in the molar area it decreased, expressing a significant relation between location and age (). On the other hand, Sawair et al. [11] demonstrated that TM was mostly located at the premolar region (65.4%).

Table 6 compares the prevalence of oral tori from different studies. It was revealed that the prevalence of TP ranged from 4.1 to 60.5% [4–18] and the prevalence seemed to vary from country to country. Although the epidemiology of oral tori has been studied comprehensively in literature, there is only one group [16] reporting a high prevalence rate of TP (41.7%) in the peritoneal dialysis population. Nevertheless, the comparison of prevalence rates between patients with and without renal dialysis was not accurate without an appropriate age and gender adjusted control group.

5. Conclusion

In conclusion, neither hyperparathyroidism nor inflammation malnutrition syndrome was found to contribute to the formation of oral tori in our patients. Nevertheless, the current study is limited by a small sample size, short follow-up duration, and lack of histopathology analysis between spontaneous and hemodialysis-induced tori. Further studies are warranted.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Authors’ Contribution

Dr. Pei-Jung Chao and Dr. Huang-Yu Yang contributed equally as co-first authors, whereas Dr. Aileen I. Tsai and Dr. Tzung-Hai Yen contributed equally to cocorrespondence.

Acknowledgment

Dr. Aileen I. Tsai and Dr. Tzung-Hai Yen are supported by research grants from Chang Gung Memorial Hospital (CMRPG310191, CMRPG3C0691, CMRPG3D0071-2, CMRPG3D0681, CMRPG3D0011, and CMRPG3E0361).

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