Indian Journal of Dental ResearchIndian Journal of Dental ResearchIndian Journal of Dental Research
HOME | ABOUT US | EDITORIAL BOARD | AHEAD OF PRINT | CURRENT ISSUE | ARCHIVES | INSTRUCTIONS | SUBSCRIBE | ADVERTISE | CONTACT
Indian Journal of Dental Research   Login   |  Users online: 360

Home Bookmark this page Print this page Email this page Small font sizeDefault font size Increase font size         

 


 
Table of Contents   
ORIGINAL RESEARCH  
Year : 2019  |  Volume : 30  |  Issue : 3  |  Page : 358-362
Comparison of skeletal changes related to patients with chronic kidney disease and healthy individuals in digital panoramic radiography


1 Department of Maxillofacial Radiology, School of Dentistry, Dental Implant Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
2 Isfahan Kidney Diseases Research Center, Isfahan University of Medical Science, Isfahan, Iran
3 Student Research Committee, Dental Implant Research Center, School of Dentistry, Isfahan University of Medical Sciences, Isfahan, Iran

Click here for correspondence address and email

Date of Web Publication9-Aug-2019
 

   Abstract 

Background: Chronic kidney disease (CKD) is a prevalent condition affecting bone metabolism. Bone changes in CKD patients also known as renal osteodystrophy happen due to disorders in the regulation of water and electrolytes caused by the disease. The aim of this study is to investigate the bone changes of CKD stages 3–5 patients without dialysis using digital panoramic radiography. Materials and Methods: In this cross-sectional study, panoramic radiographs were obtained from 30 patients with CKD stages 3–5 and 30 age and gender matched healthy individuals. The mean values of quantitative parameters such as mental index (MI), panoramic mandibular index (PMI), and antegonial index (AI) were measured and qualitative parameters such as mandibular cortical index (MCI) and trabecular bone pattern (TP) were recorded based on Kelemetti and Lindh calcifications, respectively. Statistical analysis was performed using t-test, Chi-square, and Mann–Whitney test (α = 0.05). Results: The mean values of MI, PMI, and AI in the two groups were not statistically significant (P > 0.05). MCI and TP were significantly different between the two groups. MCI showed more defects in mandibular cortex of CKD patients (6.7% of patients vs. 0% of control group were C3, P = 0.038), and TP showed more porosity in mandibular bone of CKD patients (10% of patients vs. 0% of control group were sparse, P = 0.001). Conclusion: The amount of MI, PMI, and AI were not related to CKD. While MCI and TP were significant parameters that showed mandibular cortical situation and trabecular bone pattern, they assess osteoporosis level in a more reliable manner in CKD stages 3–5 patients without dialysis.

Keywords: Chronic kidney disease, digital radiography, panoramic radiography, renal osteodistrophy

How to cite this article:
Abdinian M, Mortazavi M, Jandaghian Z. Comparison of skeletal changes related to patients with chronic kidney disease and healthy individuals in digital panoramic radiography. Indian J Dent Res 2019;30:358-62

How to cite this URL:
Abdinian M, Mortazavi M, Jandaghian Z. Comparison of skeletal changes related to patients with chronic kidney disease and healthy individuals in digital panoramic radiography. Indian J Dent Res [serial online] 2019 [cited 2019 Oct 16];30:358-62. Available from: http://www.ijdr.in/text.asp?2019/30/3/358/264109

   Introduction Top


Chronic kidney disease (CKD) is an important public concern with more than 10% of the world population suffering from it. High prevalence of risk factors such as hypertension and diabetes in modern life is the main reason for high incidence of this disease. About 90% of these patients show oral symptoms such as bone mineral metabolism disorder.[1],[2] Bone changes include demineralization, reduced trabeculation, ground glass appearance, loss of lamina dura, radiolucent giant cell lesions (brown tumor), and periodontal bone defect.[3],[4],[5]

Digital panoramic radiography is commonly used as a method to evaluate the amount of tooth decay and periodontal diseases. As panoramic radiographs provide a broad view of dentoalveolar structures, they can also be widely used for various purposes such as evaluation of bone status in jaws and mandibular inferior cortex as an anatomical landmark. Different indices are introduced for digital panoramic radiography in order to evaluate bone status.[6],[7]

Henrique et al.[2] have used mandibular cortical index (MCI), mental index (MI), and trabecular bone pattern (TP) in order to evaluate bone changes due to renal osteodystrophy and the relation between these three indices with severe secondary hyperparathyroidism in CKD patients. They found out that the amount of calcification and bone resorption related to CKD stage 5 patients were more than the control group and there was a significant correlation between these three indices and the blood PTH level.[2]

Çaǧlayan et al.[8] have investigated MI, antegonial index (AI), panoramic mandibular index (PMI), and MCI in CKD patients and the control group. They reported that no significant correlation exists between MI, AI, PMI, pulp chamber size, and the number of teeth with calcification in pulp in CKD patients and the control group, whereas the MCI showed more porosity of mandibular cortex margin of CKD patients than the control group. In addition, loss of lamina dura and soft tissue calcification were more common in CKD patients compared to the control group.[8]

Due to high prevalence of osteoporosis associated with CKD, studies need to be performed on the subject in order to assess alterations in bone status in CKD patients. So, the objective of this research is to compare bone changes of CKD patients and control group in Iranian population.


   Materials and Methods Top


This cross-sectional study consists of 30 CKD patients and 30 healthy controls. The patients were in stages 3–5 of the disease; their Glomerular Filtration Rates were less than 60 ml/min without dialysis and were randomly chosen by the nephrologist. The average age of patients was 38.4 years (in a range of 25–67). The age and gender matched control group was chosen from the people who came to the Radiology Department of Dentistry Faculty of Medical University of Isfahan without any systemic disease or taking any medication. The average age of the individuals in the control group was 39.2 years (in a range of 24–63 years). This study was approved by the Ethical Committee of Isfahan University of Medical Science (permit number 396276) and all participants signed a consent letter.

Patients with diseases that affect bone metabolism such as chronic liver disease, corticosteroid and anti-epilepsy medication, alcohol consumption, and a history of smoking were not included in the study. They were also excluded if they were unwilling to participate in the study or if their panoramic radiographs contained errors or lacked clarity in the desired region.

First of all, the biographic information of the patients including name, age, and gender were registered. Panoramic radiographs of the participants were taken at Department of Oral and Maxillofacial Radiology of Dentistry Faculty of Isfahan University of Medical Science (GenoRay, Jungwon-gu, Korea). The quality of all panoramic images was verified by an Oral and Maxillofacial Radiologist.

Measurements

Five indices were measured in the panoramic radiographs of all patients. The indices were MI, PMI, AI, MCI, and TP. The first three quantitative indices were measured according to Ledgerton's statement:[9]

MI: A line that is perpendicular to the bottom of the mandible at the middle of the mental foramen is drawn. The mandibular cortical thickness is measured on this line [Figure 1].
Figure 1: The measurement of mental index and panoramic mandibular index

Click here to view


PMI: The thickness of the mandibular cortex and the distance between the mental foramen and the inferior mandibular cortex is measured. The PMI is the ratio of the two previously mentioned measures [Figure 1].

AI: This index is a measurement of the mandibular cortical width measured on the extension of tangent line to the anterior border of the ascending ramus at the anterior point to the gonion.

Each of the mentioned indices was measured on both sides of the mandible and their mean value was used in this study.

MCI and TP, which are two qualitative indices, are defined as follows.

MCI: This index evaluates the appearance of the cortical border of mandible distal to the mental foramen. Based on Kelemetti classification, MCI is classified into three levels. C1: The endosteal margin of mandibular cortex is sharp and even on both sides. C2: The endosteal margin has semilunar defect (lacuna erosion) or it seems to form endosteal cortical residues on one or both sides. C3: The cortical layer forms heavy endosteal residues and is clearly porous [Figure 2].[10]
Figure 2: Classification of the trabecular bone pattern: (a) dense, (b) heterogeneous, (c) sparse, and (d) sparse with ground glass appearance

Click here to view


TP: This is an index that classifies the bilateral trabecular bone pattern in mandible as dense, heterogeneous, sparse, and sparse with ground glass appearance according to Lindh et al.[11]

Moreover, bone loss status was reported as a qualitative index in both jaws. Based on the severity of bone loss, all participants were classified as “intact” or “generalized bone loss.” Each measurement was made by the same radiologist and a trained person separately and compared with each other. 10% of data were remeasured one week later and all data were imported to IBM SPSS Statistics v. 22 (IBM Corp., Armonk, USA). t-Test, Mann–Whitney test, and Chi-square test were used for statistical analysis where level of significance was set to α = 0.05.


   Results Top


Among 30 CKD patients, 14 of them were men and 16 of them were women (ranging from 25 to 67 years with an average age of 38.4 years). The number of men and women among the control group was 13 and 17, respectively (ranging from 24 to 63 years with an average age of 39.2 years). Hence, there was not a significant difference between the two groups in age and gender. Two observers measured the parameters in all panoramic radiographs at separate times. The interobserver agreement was excellent in all quantitative parameters (MI = 0.91/PMI = 0.83/AI = 0.81).

The kappa index that was used for qualitative parameters including MCI, TP, and bone loss (BL). Kappa index indicated good interobserver agreement for MCI (0.78) and BL (0.77) and showed excellent interobserver agreement for TP (0.87) which means that this agreement was significant (α = 0.001).

Comparison of quantitative data between chronic kidney disease patients and control groups

According to t-test, the mean values of MI, PMI, and AI in CKD patients were less than the control group, but no significant difference exists in these indices between the two groups (P > 0.05) [Table 1].
Table 1: Results of the t-test for comparison between different variables in chronic kidney disease patient and control group

Click here to view


Comparison of qualitative data between chronic kidney disease patients and control groups

Mann–Whitney test revealed a significant difference in MCI between CKD patients and control groups (P = 0.038). CKD patients showed more defects in the mandibular cortex. The C3 classification was observed in CKD patients (6.7%, n = 2), but none of the healthy individuals belonged to this classification. The number of healthy people in C1 was significantly more than in C2 and C3. So, more than 80% of healthy people in control group belonged to C1 classification [Table 2].
Table 2: The frequency of mandibular cortical index in chronic kidney disease patients and control group

Click here to view


TP of CKD patients was more porous than the control group (P = 0.001). Sparse and sparse with ground glass appearances were not observed in control group while these two patterns were observed in 16.7% of CKD patients. Dense pattern was observed in the majority of healthy individuals (86.6%) in the control group [Table 3].
Table 3: The frequency of trabecular pattern in chronic kidney disease patients and control group

Click here to view


Chi-square test was used for comparison of bone loss status in the two groups. The percentage of the intact classified participants were 83.3% and 86.7% in CKD patients and control group, respectively. A significant difference between bone loss status and CKD was not observed (P = 0.999).


   Discussion Top


Osteoporosis is a systemic disease that is known for bone mass loss and an increase in bone fracture risk.[12] CKD causes different levels of osteoporosis. Bone changes caused by CKD consist of bone demineralization, reduced trabeculation, reduced bone cortex width, ground glass appearance, soft tissue metastatic calcification, radiolucent fibrolesion, radiolucent giant cell lesion, bone fracture, and unnatural bone repair.[13] Many of them are measured using quantitative and qualitative indices in panoramic radiography. TP, MI, PMI, AI, and MCI are the five main considered indices measured in this study.

Osteoporosis detection based on panoramic radiography indices has been shown in many researches. But because of low resolution of panoramic radiography that results in reduced linear measurement precision, there exists contradictory results about difference between osteoporosis and AI, MI, and PMI indices.[9],[14],[15],[16],[17],[18],[19]

Based on the result of our study, AI, PMI, and MI indices do not show a significant difference with osteoporosis caused by CKD. Consistent with these results, Secgin et al.[20] found that the mean value of MI in CKD patients was lower than that of the control group, but the difference was not statistically significant (P > 0.05). Furthermore, no significant difference was found between hemodialysis duration and mandibular indices in their research (P > 0.05). However, the usage of these indices has been shown to be beneficial and it is recommended that patients with lower values of these indices attend osteoporosis examinations.[2],[8],[9],[16],[20]

On the other hand, some researchers found that the PMI, MI, and AI indices show a significant and reliable difference with bone mineralization status, which makes them useful for osteoporosis detection. The difference between these indices and patient's age was investigated in these studies, and it is observed that aging changes the value of these indices and demonstrates a significant difference.[6],[15],[17]

TP and MCI indices showed osteoporosis status better so that the C3 classification strongly shows osteoporosis.[2],[21] Many researchers found that MCI is a strong and appropriate index in osteoporosis detection.[2],[6],[15],[17],[19]

Based on the results of our study, it is recommended to use TP and MCI indices for evaluation of bone status. These two indices are less affected by panoramic radiographic distortion and magnification, which make them more reliable indices for osteoporosis detection. Almost all of the studies that investigated MCI and TP approve the validity of these indices for osteoporosis status prediction. MCI shows mandibular cortical status and more defects in mandibular cortex are observed in CKD patients.[2],[6],[8],[11],[15],[19],[22],[23],[24],[25] In this work, C3 classification as clear sign of osteoporosis was observed only in CKD patients.

TP shows bone trabeculation quality. Lindh et al.[11] investigated this index and concluded that dental radiography is an appropriate method for osteoporosis detection by standardization of intraoral radiography conditions and the radiographic examination area (near mental foramen). According to their work, sparse and heterogeneous calcifications were considered as osteoporosis. As it was previously mentioned, CKD causes different levels of osteoporosis.[11]

In our work, it is observed that bone quality, bone trabeculation, and bone marrow space of the CKD patients are more sparse, thinner, and larger than that of the control group, respectively. A large percentage of the control group had dense calcification, while less than half of the CKD patients had this level of bone quality. Sparse calcification with ground glass appearance was only observed in CKD patients.

Messier et al.[5] investigated the amount of bone loss in CKD patients and found that the amount of alveolar bone loss in end-stage renal disease is more than early stage.[5] In a separate work, Frankenthal et al.[26] studied the correlation between PTH level in hemodialysis patients with periodontal indices and the amount of alveolar bone loss. They did not find any significant correlation between them. Considering bone loss, no significant difference was found between CKD patients and the control group in this study.[26]

Panoramic radiography is commonly prescribed by dentists. Awareness of previously mentioned indices and assessment of them in panoramic radiography of patients can be helpful for the determination of osteoporosis before visiting a doctor especially in patients prone to osteoporosis such as elderly people, menopausal women, alcohol consumers, smokers, patients who suffer from systemic disease like rheumatoid arthritis, inflammatory bowel disease, chronic disease of gastrointestinal tract, chronic obstructive pulmonary disease, cardiovascular disease, cancer, and chronic renal failure. These patients must be referred to a doctor for more examinations and validation of osteoporosis.[27],[28] Not accounting for the stage of chronic renal failure and not accounting for patients without hemodialysis are limitations of the study. It is suggested to perform this work using a larger statistical society on CKD patients with different stages of the disease, especially end-stage renal disease.


   Conclusion Top


MI, PMI, and AI indices are beneficial for the evaluation of bone status. However, no significant difference between these indices and osteoporosis caused by the CKD was found in our work. TP and MCI are both proved to be invaluable indices for bone density and mandibular cortex detection. This work can also be used to predict osteoporosis status in a reliable manner.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
   References Top

1.
de la Rosa García E, Mondragón Padilla A, Aranda Romo S, Bustamante Ramírez MA. Oral mucosa symptoms, signs and lesions, in end stage renal disease and non-end stage renal disease diabetic patients. Med Oral Patol Oral Cir Bucal 2006;11:E467-73.  Back to cited text no. 1
    
2.
Henriques JC, de Melo Castilho JC, Jacobs R, Amorim JB, Rosa RR, Matai CV, et al. Severe secondary hyperparathyroidism and panoramic radiography parameters. Clin Oral Investig 2014;18:941-8.  Back to cited text no. 2
    
3.
De Rossi SS, Glick M. Dental considerations for the patient with renal disease receiving hemodialysis. J Am Dent Assoc 1996;127:211-9.  Back to cited text no. 3
    
4.
Gumussoy I, Miloglu O, Cankaya E, Bayrakdar IS. Fractal properties of the trabecular pattern of the mandible in chronic renal failure. Dentomaxillofac Radiol 2016;45:20150389.  Back to cited text no. 4
    
5.
Messier MD, Emde K, Stern L, Radhakrishnan J, Vernocchi L, Cheng B, et al. Radiographic periodontal bone loss in chronic kidney disease. J Periodontol 2012;83:602-11.  Back to cited text no. 5
    
6.
Mansour S, AlGhamdi AS, Javed F, Marzouk H, Khan EA. Panoramic radiomorphometric indices as reliable parameters in predicting osteoporosis. Am J Med Sci 2013;346:473-8.  Back to cited text no. 6
    
7.
Soltani P, Mehdizadeh M, Azimipour M. The association between mandibular inferior cortex indices and serum levels of calcium and phosphorus. Dent Med Probl 2017;54:143-7.  Back to cited text no. 7
    
8.
Çaǧlayan F, Daǧistan 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. 8
    
9.
Ledgerton D, Horner K, Devlin H, Worthington H. Panoramic mandibular index as a radiomorphometric tool: An assessment of precision. Dentomaxillofac Radiol 1997;26:95-100.  Back to cited text no. 9
    
10.
Klemetti E, Kolmakov S, Heiskanen P, Vainio P, Lassila V. Panoramic mandibular index and bone mineral densities in postmenopausal women. Oral Surg Oral Med Oral Pathol 1993;75:774-9.  Back to cited text no. 10
    
11.
Lindh C, Horner K, Jonasson G, Olsson P, Rohlin M, Jacobs R, et al. The use of visual assessment of dental radiographs for identifying women at risk of having osteoporosis: The osteodent project. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:285-93.  Back to cited text no. 11
    
12.
Qaseem A, Forciea MA, McLean RM, Denberg TD; Clinical Guidelines Committee of the American College of Physicians. Treatment of low bone density or osteoporosis to prevent fractures in men and women: A Clinical practice guideline update from the American College of Physicians. Ann Intern Med 2017;166:818-39.  Back to cited text no. 12
    
13.
Proctor R, Kumar N, Stein A, Moles D, Porter S. Oral and dental aspects of chronic renal failure. J Dent Res 2005;84:199-208.  Back to cited text no. 13
    
14.
Ledgerton D, Horner K, Devlin H, Worthington H. Radiomorphometric indices of the mandible in a British female population. Dentomaxillofac Radiol 1999;28:173-81.  Back to cited text no. 14
    
15.
Bajoria AA, Ml A, Kamath G, Babshet M, Patil P, Sukhija P, et al. Evaluation of radiomorphometric indices in panoramic radiograph – A screening tool. Open Dent J 2015;9:303-10.  Back to cited text no. 15
    
16.
Chandak LG, Lohe VK, Bhowate RR, Gandhi KP, Vyas NV. Correlation of mandibular radiomorphometric indices with serum calcium and serum estradiol in pre – And post-menopausal women. Contemp Clin Dent 2017;8:53-8.  Back to cited text no. 16
[PUBMED]  [Full text]  
17.
Govindraju P, Chandra P. Radiomorphometric indices of the mandible – An indicator of osteoporosis. J Clin Diagn Res 2014;8:195-8.  Back to cited text no. 17
    
18.
Gulsahi A, Paksoy CS, Ozden S, Kucuk NO, Cebeci AR, Genc Y, et al. Assessment of bone mineral density in the jaws and its relationship to radiomorphometric indices. Dentomaxillofac Radiol 2010;39:284-9.  Back to cited text no. 18
    
19.
Leite AF, Figueiredo PT, Guia CM, Melo NS, de Paula AP. Correlations between seven panoramic radiomorphometric indices and bone mineral density in postmenopausal women. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:449-56.  Back to cited text no. 19
    
20.
Secgin CK, Kulah CK, Gulsahi A. Analysis of mandibular changes using panoramic-based indices in patients with chronic renal failure. Int J Artif Organs 2018;41:11-6.  Back to cited text no. 20
    
21.
Henriques JC, Castilho JC, Jacobs R, Amorim JB, Rosa RR, Matai CV, et al. Correlation between hand/wrist and panoramic radiographs in severe secondary hyperparathyroidism. Clin Oral Investig 2013;17:1611-7.  Back to cited text no. 21
    
22.
Kathirvelu D, Anburajan M. Prediction of low bone mass using a combinational approach of cortical and trabecular bone measures from dental panoramic radiographs. Proc Inst Mech Eng H 2014;228:890-8.  Back to cited text no. 22
    
23.
Kiswanjaya B, Yoshihara A, Deguchi T, Hanada N, Miyazaki H. Relationship between the mandibular inferior cortex and bone stiffness in elderly Japanese people. Osteoporos Int 2010;21:433-8.  Back to cited text no. 23
    
24.
Al-Dam A, Blake F, Atac A, Amling M, Blessmann M, Assaf A, et al. Mandibular cortical shape index in non-standardised panoramic radiographs for identifying patients with osteoporosis as defined by the German Osteology Organization. J Craniomaxillofac Surg 2013;41:e165-9.  Back to cited text no. 24
    
25.
Kwon AY, Huh KH, Yi WJ, Lee SS, Choi SC, Heo MS, et al. Is the panoramic mandibular index useful for bone quality evaluation? Imaging Sci Dent 2017;47:87-92.  Back to cited text no. 25
    
26.
Frankenthal S, Nakhoul F, Machtei EE, Green J, Ardekian L, Laufer D, et al. The effect of secondary hyperparathyroidism and hemodialysis therapy on alveolar bone and periodontium. J Clin Periodontol 2002;29:479-83.  Back to cited text no. 26
    
27.
Diab DL, Watts NB. Postmenopausal osteoporosis. Curr Opin Endocrinol Diabetes Obes 2013;20:501-9.  Back to cited text no. 27
    
28.
Montalcini T, Romeo S, Ferro Y, Migliaccio V, Gazzaruso C, Pujia A, et al. Osteoporosis in chronic inflammatory disease: The role of malnutrition. Endocrine 2013;43:59-64.  Back to cited text no. 28
    

Top
Correspondence Address:
Dr. Zahra Jandaghian
School of Dentistry, Isfahan University of Medical Sciences, Isfahan
Iran
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijdr.IJDR_175_18

Rights and Permissions


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  
 


    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed232    
    Printed7    
    Emailed0    
    PDF Downloaded30    
    Comments [Add]    

Recommend this journal