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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2019  |  Volume : 30  |  Issue : 4  |  Page : 755-763
The Relationship between carotid artery calcification and pulp stone among hemodialysis patients: A retrospective study


1 Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Akdeniz University, Antalya, Turkey
2 Department of Nephrology, Antalya Ataturk State Hospital, Antalya, Turkey
3 Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Eskisehir Osmangazi University, Eskisehir, Turkey
4 Department of Oral and MaxillofacialRadiology, Faculty of Dentistry, Ataturk University, Erzurum, Turkey

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Date of Submission19-Apr-2018
Date of Decision16-Jul-2018
Date of Acceptance17-Jul-2018
Date of Web Publication27-Aug-2019
 

   Abstract 


The aim of this study was to determine the relationship between the presence of carotid artery calcification (CAC) and pulp stone (PS). A total of 60 chronic hemodialysis (HD) patients (30 CAC positive, 30 CAC negative) participated in this study. The mean age of patients was 54.7 ± 16.4 years, and 32 (53%) of them were male. CAC was defined as the presence of heterogeneous nodular opacities in the soft tissue in C3–C4 intervertebral area. Panoramic radiographs of the patients were evaluated for CAC and PS by two oral and maxillofacial radiologists. PS was evaluated in all healthy, decayed, and restored teeth except the third molar teeth, in the coronal, sagittal, and axial planes. The Statistical Package for the Social Sciences (version 20.0; SPSS, Inc., an IBM Company, Chicago, IL, USA) was used. A probability P <0.05 was considered statistically significant. The prevalence of PS in this study was 30% (18 patients) all group. A total of 1324 teeth were analyzed and PS was detected in 237 teeth (17.9%). The occurrence of PS in teeth in CAC-positive group (10 patients, 17.2% of 654 teeth) was similar to that in CAC-negative group (8 patient, 18.3% of 670 teeth). There was no statistical correlation between CAC and PS in chronic HD patients (P = 0.08). In the subgroup analysis, the presence of diabetes (P = 0.003), parathormone level (P = 0.02), calcium × phosphorus product (P = 0.04), and C-reactive protein levels (P = 0.002) were higher, and duration of HD (P = 0.03) was significantly longer in patients with CAC-positive and PS. In chronic HD patients, the presence of PS was not a strong predictor for the presence of CAC.

How to cite this article:
Gunen Yilmaz S, Yilmaz F, Bayrakdar IS, Harorli A. The Relationship between carotid artery calcification and pulp stone among hemodialysis patients: A retrospective study. Saudi J Kidney Dis Transpl 2019;30:755-63

How to cite this URL:
Gunen Yilmaz S, Yilmaz F, Bayrakdar IS, Harorli A. The Relationship between carotid artery calcification and pulp stone among hemodialysis patients: A retrospective study. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2019 Sep 20];30:755-63. Available from: http://www.sjkdt.org/text.asp?2019/30/4/755/265449



   Introduction Top


Pulpal calcification is calcified structural masses within teeth and is seen in the form of pulp stone (PS) and diffuse calcification.[1] Diffuse calcifications are small irregular calcified masses in the apical root canal region, and are called calcific degeneration.[1],[2] PS is nodular and seen as calcified masses in the dental pulp. These stones may be seen in primary or permanent teeth in all age-groups. Their size may vary from microscopic dimensions to a size, which obliterates the pulpal cavity.[3],[4] These may be seen as a small single nodular calcified mass or several calcified opacities. PS is often observed in decayed teeth; although, it may be encountered in all teeth, including healthy and unerupted teeth.[5] PS is classified as diffuse, true, or false according to their structure.[3],[4] PS is clinically indiscernible and often insignificant unless it is not large in size. Although the incidence of PS is reported as 8%–90% in radiographic studies, it is probably underestimated because of the small stones being invisible on radiography.[6] Two major elements forming the structure of PS are calcium (32.1%) and phosphorus (14.7%), followed by fluoride, sodium, and magnesium to a lesser extent.[7]

Vascular calcifications (VC) are strong predictors of all-cause and cardiovascular mortality in patients with end-stage renal disease.[8] Cerebrovascular events (80%) often develop due to atheroma plaques in the carotid bifurcation. The finding of carotid artery calcifications (CACs) on a panoramic radiography (PR) is a powerful marker for future vascular events (cardiovascular and cerebrovascular), and it was described for the first time by Friedlander and Lande.[9]

PRs are an imaging modality which are frequently used in clinical dentistry, and they may give information about adjacent soft tissues, bones, and vascular pathologies. CAC is often seen as irregular, nodular, circular heterogeneous opacities in C3–C4 intervertebral area, close to the hyoid bone and at 1.52–2.5 cm distance from the inferioposterior mandibular angle.[2]

Numerous factors including bone-mineral metabolism disorders seen from the early stages of chronic kidney disease (CKD) (hyperphosphatemia, hyperparathyroidism, hypocalcemia), low grade chronic inflammation, use of phosphate binders-containing calcium, and Vitamin D analog, prolonged CKD and dialysis, and the presence of diabetes form a basis both for VC and PS. Calcium-phosphorus deposition in normal tissue and areas of chronic inflammation are seen in both conditions. For this reason, we believe that CAC and PS result from similar pathogenetic mechanisms.

There are a few studies evaluating the relationship between CAC and PS in hemodialysis (HD) patients.[2],[10] The aims of this study were to determine the prevalence of PS in Turkish HD patients using PRs and to evaluate the association of this condition with CAC and biochemical parameters.


   Materials and Methods Top


This observational, retrospective, single-center study examined PRs taken between 2013 and 2015 in the database of the Akdeniz University, Faculty of Dentistry and Department of Oral Maxillofacial Radiology. A total of 60 HD patients participated in this study. Patients were divided into two groups as follows: CAC-positive (n = 30) and CAC-negative (n = 30). HD was performed thrice weekly (for 4 h/day).

PRs of the patients were evaluated for CAC and PS by two oral and maxillofacial radiologists. CAC was defined in PR as heterogeneous nodular opacities in the soft tissue in the C3–C4 intervertebral area [Figure 1] and [Figure 2]. To determine the presence and location of calcification, patients with all CAC were also evaluated by color Doppler ultrasonographs. Patients without CAC on ultrasonography were excluded from the study.
Figure 1: Panoramic radiography showing carotid artery calcification (On the panoramic radiography carotid artery calcifications are observed in the area between C3 and C4 as homogeneous calcification).

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Figure 2: Pulp stone in the right molar teeth in panoramic radiograph (on panoramic radiograms pul] stone is observed in teeth number 46, 17, and 16).

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PS was evaluated in all healthy, decayed and restored teeth except the third molar teeth. All teeth were evaluated in coronal, sagittal, and axial planes. Definite radiopaque masses inside the pulp chambers and pulp canal were identified as PS [Figure 2].

Demographic and biochemical parameters in the month of PR evaluation were retrospectively recorded. Patients aged <18 years, those receiving dialysis therapy for <6 months, those with previous cerebrovascular disease and carotid endarterectomy, those with a history of orthodontic treatment, head-neck and maxillary trauma and patients noneligible for PR evaluation were excluded from the study. The study was approved by the Local Ethics Committee.

Obtaining radiographs

The PRs of all cases were obtained by the same person and were taken by giving an appropriate dose of radiation with the patients standing and with the cervical vertebrae in the vertical position as much as possible. PRs were used for the panoramic examinations according to the standard protocols. The PRs were exposed with 64–66 kVp and 8–10 mA, for 0.8–4 s depending on patient size. The images were captured with the image plate system, Fujifilm FCR. Fuji IP cassette type cc, size 15 × 30, Fuji Photofilm Co., LTD, Japan, were used. All images were interpreted using the CDR®DICOM 3.5 software, Schick, USA, in a room allowing ultimate dim light conditions.

Laboratory analyses

All patients were measured to determine the height (m), weight (kg), and blood pressure. The body mass index (BMI) was calculated as weight/height2 (kg/m2). To determine the adequacy of the HD, Kt/V (Daugirdas formula) was used. Venous blood samples were collected from all the patients after 12 h of fasting and at mid-week before an HD session. In the laboratory analyses, fasting blood glucose, blood urea nitrogen, creatinine, total protein, albumin, sodium, potassium, calcium, phosphorus, intact parathyroid hormone (PTH), ferritin, alkaline phosphatase, triglyceride, total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), C-reactive protein (CRP), and uric acid levels were measured. The LDL-C was calculated using the Friedewald method [LDL = TChol-HDL-TG/5.0 (mg/dL)].

Diabetes mellitus was defined as a patient who takes oral antidiabetics and/or insülin or a patient with blood glucose higher than 126 mg/dL. Hypertension was defined as a patient who takes antihypertensive drug or a patient with predialysis systolic blood pressure higher than 140 mm Hg and/or diastolic blood pressure higher than 90 mm Hg. Hyperlipidemia was defined as a patient who takes antihyper- lipidemic drug or a patient with TC higher than 200 mg/dL and/or LDL-C >130 mg/dL and/or triglyceride >150 mg/dL.


   Statistical Analyses Top


The data are expressed as means ± standard deviation. The Shapiro–Wilk and Kolmogorov–Smirnov tests were performed to test for the normal distribution of variables. The comparison of two groups of numeric variables was made with the Student’s t-test and Mann–Whitney U-test. Categorical data were compared using the Chi-square test. For the evaluation of reproducibility, randomly selected 18 PRs (30%) were re-evaluated by the same researchers. The Statistical Package for the Social Sciences (version 20.0; SPSS, Inc., an IBM Company, Chicago, IL, USA) was used. A value of P <0.05 was considered statistically significant.


   Results Top


The ICC value for the intra- and inter-reliability was as high as 0.997 (P <0.001) and 0.994 (P <0.001), respectively, indicating excellent reliability. The mean age of patients was 54.7 ± 16.4 years (minumum 22, maximum 78), and 32 (53%) of them were male. The mean duration on dialysis was 69.6 ± 22.1 months. Demographical, clinical data, and laboratory measurements of HD patients are shown in [Table 1].
Table 1: Demographic, clinical, and laboratory measurements of the hemodialysis patients and distribution of carotid artery calcification and pulp stone.

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There was no difference between the CAC-positive and CAC-negative groups in terms of the usage of antihypertensive drugs (P = 0.21), erythropoietin (P = 0.14), intravenous iron (P = 0.17), sevelamer (P = 0.67), parathyroidectomy (P = 0.14), and cinacalcet (P = 0.75), while the use of Vitamin D analog (calcitriol, paricalcitol) (P = 0.03) and calcium-containing phosphate-binding agent (P = 0.04) was more frequent in CAC-positive patients.

The prevalence of PS in this study was 30% (18 patients). In this study, a total of 1324 teeth were analyzed and PS was detected in 237 teeth (17.9%). The occurrence of PS in teeth in the CAC-positive group (10 patients, 17.2% of 654 teeth) was similar to that in CAC-negative group (8 patients, 18.3% of 670 teeth). No significant difference was found between CAC-positive and negative patients in terms of PS, both among patients and teeth with detected PS (P = 0.08) [Table 1]. There was no statistical correlation between CAC and the PS.

PS was found in 109 (24.1%) out of 452 teeth from the diabetic HD patient group and 128 (14.6%) out of 872 from the nondiabetic HD group (P = 0.04). PS was detected in 10 males (31.2%) and eight females (28.5%) and no significant difference was found between the two genders (P = 0.16). Out of 625 teeth evaluated in female patients, PS was detected in 112 teeth (17.9%), whereas 125 of 699 teeth in male patients had PS (17.8%). No difference between the two genders could be identified (P = 0.07). There was no difference in the occurrence of PS between the maxilla and mandible (P = 0.22).

There was no difference between the PS-positive and PS-negative groups in terms of the use of antihypertensive drugs (P = 0.15), erythropoietin (P = 0.11), sevelamer (P = 0.09), and parathyroidectomy (P = 0.09), while the use of Vitamin D analog (calcitriol, pari-calcitol) (P = 0.002), cinacalcet (P = 0.03), and calcium-containing phosphate-binding agent (P = 0.01) was more frequent in PS-positive patients.

In the subgroup analysis, in patients with presence of both CAC and PS, the prevalence of diabetes (P = 0.003), elevated PTH (P = 0.02), elevated Ca × P product (P = 0.04) and elevated CRP levels (P = 0.002) was higher and duration on HD (P = 0.03) was significantly longer. No difference between the two genders could be identified (P = 0.07) [Table 2]. There was no difference in the occurrence of PS between maxilla and mandible (P = 0.22).
Table 2: Demographic, clinical, and laboratory measurements for risk factors for pulp stone.

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On univariate and multivariate analysis, it was observed that age, diabetes, C-reactive protein, PTH, Ca × P product, and longer duration on HD were independent determinants of PS and CAC [Table 3] and [Table 4].
Table 3: Clinical-biochemical risk factors and its association with the presence of carotid artery in univariate and multivariate logistic regression analysis.

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Table 4: Clinical-biochemical risk factors and its association with the presence of pulp stone in univariate and multivariate logistic regression analysis.

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   Discussion Top


In the present study, PS was found in 30% of dialysis patients, and 17.9% of all teeth. No statistically significant difference was found between dialysis patients with positive and negative CAC in terms of the incidence of PS. In this study, both CAC and PS were more common among diabetic patients. The incidence of CAC was similar between patients with and without PS. Furthermore, both CAC and PS were correlated with diabetes, PTH, CRP, prolonged dialysis duration and high product of Ca × P. The incidence of PS increased with age in HD patients, but the incidence was similar between the genders. In the present study, we did not observe a significant difference between the maxilla and mandible in terms of PS incidence.

The etiology of PS remains largely uncertain. However, age, circulatory disorders in the pulpal tissue, interactions between the pulpal and epithelial tissues, orthodontic treatment procedures, chronic irritation, chronic inflammation, genetic and systemic diseases, and idiopathic factors predispose the occurrence of PS.[4] Among the studies conducted in Turkey, PS was found in 38% of the patients, and 4.8% of the teeth by Sener et al,[11] 5% of the teeth and 12% of the patients by Gulsahi et al,[12] 27.8% of all teeth, and 63.8% of the patients by Çolak et al,[13] and 15% of all teeth and 57.6% of the patients by Sisman et al.[3] There are a few studies in the literature evaluating PS in patients with CKD. In their study with cone-beam computed tomography (CBCT) in 15 patients, Çağlayan et al found no statistical difference between the patients with CKD and control group in terms PC (P = 0.60).[14] In a study by Kanjanabuch et al with PRs in a small number of patients (13 peritoneal dialysis patient, 17 healthy controls), no significant difference was found between the groups in terms of PC.[15] According to the results of these studies performed in different age-groups, the incidence of PS in HD patients may be increased, decreased or similar compared to the general population.

In a study by Nayak et al evaluating 150 patients for the relationship of PS with systemic diseases, PS was the most common in the cardiovascular disease (CVD) group.[16] Again, the incidence of PS was increased in patients with diabetes and autoimmune diseases.[16] In the study by Gulsahi et al, no correlation was found between PS and systemic diseases, but these diseases were not specified.[12] It has been stated that osteopontin constitutes the PS matrix and plays a key role in the occurrence of PS, by increasing in diabetic patients.[17] Talla et al showed increased incidence of PS in patients with type-2 diabetes, hypertension, and gastritis.[18] Tarim Ertas et al found no correlation between PS and kidney stones.[19]

In their study with 247 patients evaluating pulpal calcification and CAC with PRs, Horsley et al found an incidence of CAC of 32%, and the incidence of PC was 25%. In that study, the incidence of both CAC and PS was increased in elderly persons, but PS was not considered as a strong predictor of CAC.[20] The accuracy of PC in screening for CAC was 66.4%.[20]

There are few studies in the literature evaluating the relationship between PS and CAC.[2],[10] In their study evaluating 29 HD and 31 kidney transplantation patients, Kansu et al found CAC in 8 (27.5%) and PS in 5 (17.2%) HD patients.[2] In their study evaluating 112 HD patients, Patil et al found no CAC in any patient, while PS was found in five patients (4.4%).[10] A statistically significant correlation was found between CAC and PS in our study and in these two studies.[2],[10] However, the incidence of PS was higher in our study than in the two mentioned studies. In our study, we further evaluated the relationship of both CAC and PS with biochemical parameters and the traditional risk factors of atherosclerosis. Prolonged HD duration, presence of diabetes mellitus, calcium and phosphorus levels, calcium × phosphorus product, PTH, ALP, and CRP levels were higher in patients both with CAC and PS (P < 0.05) [Table 3] and [Table 4].

On the other hand, a significant correlation was found between CVD and PS in three studies, including patients with CVD.[16],[21],[22] In their study, evaluating 55 patients aged between 20 and 55 years with periapical radiograph for PS, Edds et al observed PS in 74% of patients with CVD, and 39% of patients without CVD.[21] In the same study, no significant correlation was found between PS and family history of CVD.[21] Similarly, we did not find a correlation between family history of CVD, CAC, and PS.

PS is frequently diagnosed by radiography imaging. In the histological studies, the incidence of PS is higher than in the radiological studies.[23] This is because PS with a diameter less than 200 μm cannot be visualized on radiographs.[12] Radiologically, studies have often used CBCT, PRs, and bitewing radiographs. In their study with 50 patients evaluating CAC with ultrasonography, Yeluri et al found PS in 88% and CAC in 91%, and renal calcification in 92%, and showed that CAC was more sensitive according to PR ultra-sonography.[24]

Various studies have reported increased[12],[25] or unchanged[26],[27] incidence of PS with aging. Again, there are studies reporting PS incidence as more common in female patients[11] or no difference between the genders.[3],[12]

The study has several limitations. The small number of patients and the lack of a healthy control group were the primary limitations of this study. Another limitation is that, since this study was performed among Turkish HD patients, the relationships detected between CAC and PS might not be applicable to other populations. In addition, low sensitivity of PRs in the detection of CAC and PS is another limitation.


   Conclusion Top


No significant correlation was found between PS and CAC in Turkish HD patients. Diabetes, prolonged HD duration, and high levels of parathormone, calcium × phosphorus product, and CRP were correlated both with CAC and PS.

Conflict of interest: None declared.



 
   References Top

1.
Bevelander G, Johnson PL. Histogenesis and histochemistry of pulpal calcification. J Dent Res 1956;35:714-22.  Back to cited text no. 1
    
2.
Kansu O, Ozbek M, Avcu N, Aslan U, Kansu H, Gençtoy G. Can dental pulp calcification serve as a diagnostic marker for carotid artery calcification in patients with renal diseases? Dentomaxillofac Radiol 2009;38:542-5.  Back to cited text no. 2
    
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Sisman Y, Aktan AM, Tarim-Ertas E, Ciftçi ME, Sekerci AE. The prevalence of pulp stones in a Turkish population. A radiographic survey. Med Oral Patol Oral Cir Bucal 2012;17:e212-7.  Back to cited text no. 3
    
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da Silva EJ, Prado MC, Queiroz PM, et al. Assessing pulp stones by cone-beam computed tomography. Clin Oral Investig 2017;21:2327- 33.  Back to cited text no. 4
    
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Ravanshad S, Khayat S, Freidonpour N. The prevalence of pulp stones in adult patients of shiraz dental school, a radiographic assessment. J Dent (Shiraz) 2015;16:356-61.  Back to cited text no. 5
    
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Moss-Salentijn L, Hendricks-Klyvert M. Calcified structures in human dental pulps. J Endod 1988;14:184-9.  Back to cited text no. 6
    
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Le May O, Kaqueler JC. Scanning electron microscopic study of pulp stones in human permanent teeth. Scanning Microsc 1991;5: 257-67.  Back to cited text no. 7
    
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Chen NX, Moe SM. Vascular calcification: Pathophysiology and risk factors. Curr Hypertens Rep 2012;14:228-37.  Back to cited text no. 8
    
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Friedlander AH, Lande A. Panoramic radio- graphic identification of carotid arterial plaques. Oral Surg Oral Med Oral Pathol 1981;52:102- 4.  Back to cited text no. 9
    
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Patil S, Sinha N. Pulp stone, haemodialysis, end-stage renal disease, carotid atherosclerosis. J Clin Diagn Res 2013;7:1228-31.  Back to cited text no. 10
    
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Sener S, Cobankara FK, Akgünlü F. Calcifications of the pulp chamber: Prevalence and implicated factors. Clin Oral Investig 2009;13:209-15.  Back to cited text no. 11
    
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Gulsahi A, Cebeci AI, Ozden S. A radio-graphic assessment of the prevalence of pulp stones in a group of Turkish dental patients. Int Endod J 2009;42:735-9.  Back to cited text no. 12
    
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Çolak H, Çelebi AA, Hamidi MM, Bayraktar Y, Çolak T, Uzgur R. Assessment of the prevalence of pulp stones in a sample of Turkish central Anatolian population. Scientific World Journal 2012;2012:804278.  Back to cited text no. 13
    
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Çağlayan F, Dağistan S, Keleş M. The osseous and dental changes of patients with chronic renal failure by CBCT. Dentomaxillofac Radiol 2015;44:20140398.  Back to cited text no. 14
    
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Kanjanabuch P, Sinpitaksakul P, Chinachatchawarat S, Pacharapong S, Kanjanabuch T. Oral and radiographic findings in patients undergoing continuous ambulatory peritoneal dialysis. J Med Assoc Thai 2011 ;94 Suppl 4:S106-12.  Back to cited text no. 15
    
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Nayak M, Kumar J, Prasad LK. A radiographic correlation between systemic disorders and pulp stones. Indian J Dent Res 2010;21:369- 73.  Back to cited text no. 16
[PUBMED]  [Full text]  
17.
Inagaki Y, Yoshida K, Ohba H, et al. High glucose levels increase osteopontin production and pathologic calcification in rat dental pulp tissues. J Endod 2010;36:1014-20.  Back to cited text no. 17
    
18.
Talla HV, Kommineni NK, Yalamancheli S, Avula JS, Chillakuru D. A study on pulp stones in a group of the population in Andhra Pradesh, İndia: An institutional study. J Conserv Dent 2014;17:111-4.  Back to cited text no. 18
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19.
Tarim Ertas E, Inci M, Demirtas A, et al. A radiographic correlation between renal and pulp stones. West Indian Med J 2014;63:620-5.  Back to cited text no. 19
    
20.
Horsley SH, Beckstrom B, Clark SJ, et al. Prevalence of carotid and pulp calcifications: A correlation using digital panoramic radiographs. Int J Comput Assist Radiol Surg 2009; 4:169-73.  Back to cited text no. 20
    
21.
Edds AC, Walden JE, Scheetz JP, Goldsmith LJ, Drisko CL, Eleazer PD. Pilot study of correlation of pulp stones with cardiovascular disease. J Endod 2005;31:504-6.  Back to cited text no. 21
    
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Maranhão de Moura AA, de Paiva JG. Pulpal calcifications in patients with coronary atherosclerosis. Endod Dent Traumatol 1987;3:307- 9.  Back to cited text no. 22
    
23.
Hillmann G, Geurtsen W. Light-microscopical investigation of the distribution of extracellular matrix molecules and calcifications in human dental pulps of various ages. Cell Tissue Res 1997;289:145-54.  Back to cited text no. 23
    
24.
Yeluri G, Kumar CA, Raghav N. Correlation of dental pulp stones, carotid artery and renal calcifications using digital panoramic radiography and ultrasonography. Contemp Clin Dent 2015;6:S147-51.  Back to cited text no. 24
    
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Tamse A, Kaffe I, Littner MM, Shani R. Statistical evaluation of radiologic survey of pulp stones. J Endod 1982;8:455-8.  Back to cited text no. 25
    
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Darwazeh AM, Hamasha AA, Pillai K. Prevalence of taurodontism in Jordanian dental patients. Dentomaxillofac Radiol 1998;27:163- 5.  Back to cited text no. 26
    
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al-Hadi Hamasha A, Darwazeh A. Prevalence of pulp stones in Jordanian adults. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:730-2.  Back to cited text no. 27
    

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Correspondence Address:
Sevcihan Gunen Yilmaz
Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Akdeniz University, Antalya
Turkey
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DOI: 10.4103/1319-2442.265449

PMID: 31464230

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