|Year : 2021 | Volume
| Issue : 2 | Page : 117-123
Analysis of fractal dimension and radiomorphometric indices of mandible on panoramic radiographs in end-stage renal disease at a tertiary care centre in South India
Anju Redhu1, B Suman2
1 Department of Oral Medicine and Radiology, Post graduate Institute of Dental Sciences, Rohtak, Haryana, India
2 Department of Oral Medicine and Radiology, Government Dental College and Research Institute, Bengaluru, Karnataka, India
|Date of Submission||03-Sep-2020|
|Date of Decision||04-Mar-2021|
|Date of Acceptance||31-Mar-2021|
|Date of Web Publication||23-Jun-2021|
Dr. Anju Redhu
Department of Oral Medicine and Radiology, Room No. 11, PGIDS, Rohtak - 124 001, Haryana
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background and Objectives: Chronic kidney disease (CKD), especially, end-stage renal disease (ESRD), is associated with endocrinal and metabolic alterations that negatively affect the skeletal system, and can result in renal osteodystrophy (ROD) and secondary osteoporosis. These changes can affect the mandibular density and thus can be reflected in mandible on panoramic radiographs (PR), which are frequently assessed by oral physicians. This study attempted to evaluate these mandibular skeletal alterations using radiomorphometric indices (RI) and fractal dimension (FD) analysis, in patients with ESRD, thereby aiding in their appropriate management for the dental treatment. Material and Methods: Retrospective data (including digital PRs) of 30 patients with CKD (ESRD) who were above 18 years of age were retrieved and 30 age and sex-matched healthy individuals having met the selection criteria were selected. Digital PR were used to assess the mandibular cortical index (MCI), mental index (MI), panoramic mandibular index (PMI), and FD by using ImageJ program. Results: No statistically significant difference was noted among the study groups and controls for the mean values of PMI, FD, and distribution of MCI category (P > 0.05). However, the mean value of MI was significantly reduced among the kidney patients as compared to the controls (P < 0.05). No significant correlation was noted between duration of diseases, RI (MCI, MI, PMI) and FD. Conclusion: MI values of patients with ESRD were found to be lower than those in control subjects. This finding suggests that MI analysis might be a promising, simple, and cost-effective tool for evaluating cortical bone structure in this high-risk population and any signs of osteoporosis could be withheld at the earliest stage with a prompt referral.
Keywords: End-stage renal disease, fractal dimension, panoramic radiography, radiomorphometric indices
|How to cite this article:|
Redhu A, Suman B. Analysis of fractal dimension and radiomorphometric indices of mandible on panoramic radiographs in end-stage renal disease at a tertiary care centre in South India. J Indian Acad Oral Med Radiol 2021;33:117-23
|How to cite this URL:|
Redhu A, Suman B. Analysis of fractal dimension and radiomorphometric indices of mandible on panoramic radiographs in end-stage renal disease at a tertiary care centre in South India. J Indian Acad Oral Med Radiol [serial online] 2021 [cited 2021 Nov 28];33:117-23. Available from: https://www.jiaomr.in/text.asp?2021/33/2/117/319063
| Introduction|| |
Chronic kidney disease (CKD) is defined based on the presence of kidney damage or glomerular filtration rate (GFR <60 mL/min per 1.73 m2) for >3 months. CKD is now recognized as a major medical problem worldwide. The Global Burden of Disease (GBD) study, 2015, ranked CKD as the 17th most common cause of deaths globally (age-standardized annual death rate of 19.2 deaths per 100,000 population). In many countries, CKD is now among the top five causes of death. In India, an age-adjusted incidence of end-stage renal/kidney disease (ESRD/ESKD), more commonly known as kidney failure, was reported to be 229/million population and GBD ranked CKD as the eighth leading cause of death.,
There is a paradigm shift in the perception of kidney disease, especially for nephrologists, from a life-threatening condition affecting few people who require treatment by dialysis or transplantation to a common condition that is the target for prevention, early detection, and management by other health care workers.
With advancing stage of CKD, culminating with ESRD where life sustenance is possible with a regular course of long-term dialysis or a kidney transplant, numerous systemic complications can occur as a consequence of uremic metabolites, endocrinological, and immunological imbalances.
The skeletal changes consequent to chronic renal disease can occur in the form of renal osteodystrophy (ROD) defined by quantitative histomorphometry and associated with a higher risk of fracture or CKD-MBD (chronic kidney disease-mineral and bone disorder) marked by persistent hyperphosphatemia, elevated parathyroid hormone, or FGF-23. It may manifest as increased bone demineralization, decreased thickness of cortical bone, decreased trabeculation, premature bone loss, “ground-glass” appearance, radiolucent giant cell lesions (brown tumor), due to secondary hyperparathyroidism, that can be effectively studied on the mandibular bone using digital orthopantomograms.
Digital panoramic radiographs (PRs) are widely used screening tools that facilitate the application of image processing algorithms and radiomorphometric indices (RI) which are convenient non-invasive methods of estimating bone structure.
The differential effects of CKD on the cortical and trabecular bone may be assessed radiographically utilizing RI and Fractal dimensions (FD). RI helps to delineate the alterations in mandibular cortical bone by analyzing the cortical erosion and thickness of the cortex region. On the other hand, the trabecular bone shows fractal characteristics such as self-similarity and lack of well-defined scale due to its branched structure. Therefore, fractal geometrical applications and FD can be used to define the complex structure of the trabecular bone.
Oral physician stands a fair chance of improving the quality of life for these debilitated patients by suggesting the alterations in dental treatment plan, identifying the risk of fracture and instituting prompt referral for further management. Due to the paucity of literature in this direction, this study was planned to find the relationship between mandibular FD and RI in ESRD patients using PRs.
| Materials and Methods|| |
Patients enrolled in this study were recruited from the Outpatient department of Oral Medicine and Radiology. Sample size was calculated based on the difference in the mean values of MI, that is, 0.5 of the two groups, with a standard deviation of 0.54, (which was obtained by a pilot study conducted in the department) confidence interval of 95%, at 90% power and with 5% level of significance, to be was 25 patients. However, we were able to collect data regarding 30 patients in each group. Ethical clearance was obtained from the institutional ethical committee vide letter number - GDCRI/ACM(2)/05/2017-18). Retrospective data (including digital PRS from December 2015 to November 2017) of 30 ESRD patients (posted for kidney transplant) who were above 18 years of age and had visited department of Oral Medicine and Radiology, GDCRI, Bangalore for obtaining dental clearance before undergoing renal transplant (study group) was obtained. Control group comprised of 30 age and sex-matched healthy individuals (for whom OPG were taken for diagnostic purpose from September 2017 to November 2017), and who has given the consent voluntarily to be part of the study having met the inclusion and exclusion criteria.
Good diagnostic quality radiographs of study group and control group were included.
- PRs (of study and control group)-
- With poor image quality and characteristics,
- Showing radiolucent or radiopaque pathological lesions/abnormalities/artifacts in the region of interest
- Depicting fracture of mandible/treated for the same with internal fixation in the region of interest were excluded.
For the Control group, patients with the previous history of other systemic diseases, chemotherapy, radiotherapy, taking drugs affecting bone health, having pathological lesions of the jaws, edentulous lower jaw, jaw fracture/reconstruction surgery, chronic alcoholics (using >3 units per day), pregnancy, women with surgically induced menopause or subjected to hormonal replacement therapy were excluded.
Selected PRs were taken using 9000 Digital Panoramic and Cephalometric system, (Carestream, France) at 70 kVp; 10 mA, 14.3 s and were observed at the level of the flat panel monitor with subdued lighting at a resolution of 322 dpi. Each PR was analyzed by two separate observers. Measurements were performed using MicroDicom- free DICOM viewer 0.9.1 (build 918) 32-bit software. RI were determined as follows-
- Mandibular cortical index (MCI) was determined by the visual analysis of the appearance of the lower border of the mandible near the mental foramen bilaterally on PRs and classified into specific category as proposed by Klemetti et al. as C1, with even and sharp endosteal margin of the cortex on both sides; C2, with endosteal margin depicting semilunar defects (lacunar resorption) and/or seems to form endosteal cortical residues on one or both sides; and C3, the cortical layer forms heavy endosteal cortical residues and is porous. [Figure 1]a, [Figure 1]b, [Figure 1]c.
- Mental index (MI) determined to measure the cortical width of mandible by tracing a line that passes perpendicular to the tangent to the lower border of mandible and through the center of the mental foramen [Figure 2].,
- Panoramic mandibular index (PMI) was determined based on the ratio of the cortical thickness at the base of the mandible and the distance from the center of the mental foramen to the lower border of the base of the mandible (Benson et al. 1991) [Figure 3].
|Figure 1: Evaluation of - (a) MCI- C1 Category, (b) MCI- C2 Category, (c) MCI- C3 Category|
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This was followed by fractal dimensional analysis of the PRs. FD analysis was carried out using the box-counting method in the selected region of interest using Image J program software (version 1.51 k) as follows- An area below and anterior to the mental foramen, of 90 × 90 pixel size was selected on both the sides of OPG. The selection of region of interest was done on a monitor of 17” display LED screen with a screen resolution of 1024 X 768 in 32 bits in color mode with subdued lighting.
Each image (region of interest) was duplicated and then blurred using Gaussian filter with a diameter of 35 pixels. The resulting heavily blurred image was then subtracted from the original, and 128 was added to the result at each pixel location. Afterward, the image was made binary, thresholding on a brightness value of 128. The resultant image was eroded and dilated once to reduce noise, following which, inverted and skeletonized. FD was calculated by box-counting method in Image J program [Figure 4].
|Figure 4: Stepwise methodology for the FD analysis- (a) region of interest, (b) ROI after application of Gaussian filter. (c) Image obtained after subtraction of filtered image from ROI. (d) After addition of 128 bit. (e) Conversion into binary form. (f) Skeletonised image. (g) Fractal box count in imageJ|
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To minimize intra-and inter-observer variability, two measurements at an interval of 2 weeks were taken for each parameter, by two experienced and qualified oral and maxillofacial radiologists independently who were calibrated beforehand only regarding the selection of ROI and assessment of parameters.
All the data were analyzed using the Statistical Package for the Social Sciences (SPSS) software program, version 17.0. Descriptive data statistics, cross-tabulations, and Chi-square statistics were computed. Intra and inter-observer agreement were calculated using Cronbach's alpha (α). The level of statistical significance was determined at P < 0.05. Pearson correlation was applied to find out the correlation of different parametric variables, and Spearman correlations for non-parametric variables (MCI) were applied.
| Results|| |
This study included data from 60 subjects who were equally divided into two groups: ESRD patients (study group) and controls. Each group comprised of 24 males and 6 females. The mean age of study group was 32.96 ± 11.00 years with minimum and maximum age of 19 years and 56 years, respectively. However, the mean age of control group was 36.56 ± 9.64 years with minimum and maximum age of 26 years and 57 years, respectively [Table 1].
|Table 1: Mean values of age, FD, MI and PMI in the study group and control group|
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The mean duration of kidney diseases assessed in the study group was 57.2 ± 21.53 months with minimum and maximum duration of 24 months and 108 months respectively. However, the mean duration of dialysis for the study group was 33.6 ± 14.57 months with minimum and maximum duration of 12 months and 60 months, respectively.
The mean value of the FDs for study group was 1.36 ± 0.287, with minimum and maximum values of 1.14 and 1.43 respectively. On the contrary, the value of the FDs for the control group was 1.33 ± 0.071, with minimum and maximum values of 1.14 and 1.435, respectively. However, no statistically significant difference was noted in the FD values of cases and controls (P > 0.05). The mean value of the MI for study group was 3.68 ± 0.548 mm, with minimum and maximum values of 2.6 mm and 4.79 mm, respectively. Among the control group, the mean value of the MI was 4.19 ± 0.724 mm, with minimum and maximum values of 2.32 mm and 6.23 mm respectively. The difference between the groups was found to be statistically significant (P < .05). The mean value of PMI was 0.308 ± 0.061 for study group with minimum and maximum values of 0.209 and 0.458 respectively, whereas, the mean value of PMI was 0.318 ± 0.100 for the control group with minimum and maximum values of 0.141 and 0.719, respectively. The difference was not found to be statistically significant among the groups (P > .05) [Table 1].
In the distribution of MCI, C1 category was noted in PRs of 9 patients of ESRD group, whereas, 12 patients from the control group had C1 category. C2 category was found in 18 subjects in the study group whereas, 15 subjects of the control group possessed the C2 category. Interestingly, the C3 category was demonstrated by an equal number of subjects (n = 3) for study and control group. However, the distribution among the groups was not found significantly significant (P > 0.05) [Graph 1].
The study possessed marked intra and inter-observer agreement with Cronbach's alpha value (α) > 0.89 (a single value has been provided to assess the overall agreement). Details are provided in [Table 2].
|Table 2: Intra-observer and Inter-observer Cronbach's alpha values of the two observers|
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No significant correlation was found between the FD values and the RI (MI, PMI, and MCI) among cases and control groups. However, the MI values of the study group showed a strong positive correlation (r = 0.519) with the PMI. Also, no significant correlation was obtained among FD, RI with duration of disease and duration of dialysis. [Table 3], [Table 4] and [Graph 2], [Graph 3].
|Table 3: Pearson Correlation (r) of different variables among the study group and control group|
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|Table 4: Spearman Correlation (rs) of MCI and other variables among the study group and control group|
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| Discussion|| |
With increasing life expectancy and prevalence of lifestyle diseases, United States has seen a 30% increase in prevalence of CKD in the last decade. Unfortunately, from India only limited data is available regarding the prevalence of CKD. Diabetes and hypertension today account as underlying etiological factors for almost 40–60% cases of CKD. As a matter of concern, over 50% of diabetes and hypertensive patients are not aware that they are harboring the CKD; therefore, it is necessary to screen these high-risk population specifically by health care providers, including oral physicians. Deterioration of kidney function leads to secondary hyperparathyroidism which, decidedly affects cortical and trabecular bone differentially. This study attempted to assess these differential effects by means of RI (MI, MCI and PMI) and FD among the ESRD patients.
Over the time, various researchers exhibited that mandibular cortical width has better efficacy in detecting osteoporosis on panoramic images. However, few researchers proposed that PMI and MI should not be used to assess patients' status regarding osteoporosis. Regardless of consensus between researchers, a mandibular cortical bone thickness of approximately 3 mm and a severely eroded cortex (Type III classification) were suggested as strong indicators for the investigation of osteoporosis.,, RI poses some limitations like margins of mental foramen should be distinctly visible, multiple measurements are required for precision and procedural magnification errors, thus questioning the utility of RI. However, FD addressed these limitations and assesses the trabecular bone health. Fractal analysis is a method of numerical texture analysis, which is based on a series of processes referred to as fractal mathematics to define this complex shape and structural patterns. The scope of utilizations of FD, from mathematics to biology, is very wide. In the field of dentistry, researchers had differentiated between patients with gingivitis and periodontitis and osteoporotic and non-osteoporotic patients by using dental radiographs and image analysis procedures. Many researchers stated that FD analysis was the most reliable, economical, and easily applicable method among all the methods in the evaluation of bone tissue.,
In this study, mean age of the study population belongs to the 4th decade (study group was 32.96 ± 11.00 years and control group was 36.56 ± 9.64 years) which was in-accordance with the findings of the Gumussoy et al. and Çağlayan et al. The mean duration of the diseases was found to be 57.2 ± 21.53 months and the duration of dialysis was 33.6 ± 14.57 months. Almost similar findings were noted by Çağlayan et al. with mean duration of dialysis 39 ± 29.44 months. However, Gumussoy et al. reported the average duration of dialysis of the patients was 43 ± 31 months (range 12–120 months), which is comparatively more than this study findings.
In this study, FD values of study population were found to be slightly higher than the healthy control group but the difference was not statistically significant. Previous researches have also asserted that FD get increased in some diseases, which creates osteoporotic effects on bone structure., Saeed et al. reported that demineralization and resorption, which were caused by periapical lesions could lead to increased trabecular complexity by affecting the surface porosity, and thus the FD value gets increased. The increased values in this study could be due to the anabolic effects of PTH on trabecular bone causing increased trabecular thickness and number. However, many other studies have concluded that the FD values decrease in systemic diseases.,,, as well as in chronic renal failure patients as reported by Gumussoy et al.
This study did not yield any statistically significant difference in the PMI values and MCI categories among ESRD patients and control group. These findings were partially in accordance with the findings asserted by Çağlayan et al., who also reported no statistically significant differences in the PMI values but with regard to MCI, the cortical margins of the mandible were more porous in patients with CRF than in the control group.
On the contrary, MI values in ESRD patients (3.688 mm) were comparatively lower than the control group (4.190 mm) and demonstrated a statistically significant difference. However, this finding was in contrast to the findings reported by Çağlayan et al., who conducted a similar study using CBCT and reported increased mean values of MI in patients with chronic renal failure as compared to the control group, but the difference was statistically insignificant. Secgin et al., reported a lower mean MI in patients with CRF than in healthy subjects, but the difference was not statistically significant. This finding has reinforced the fact that mandibular cortical bone thickness of approximately 3 mm is a strong indicator for the investigation of osteoporosis.,,
This study had not found any significant correlation of FD with RI (MI, PMI and MCI), age, mean duration of disease, and mean duration of dialysis, and these findings were consistent with the findings, reported by Gumussoy et al. in 2016.
Cortical bone represents nearly 80% of human bone mass and is the major determinant of bone strength. In this retrospective study, it was noted that CKD patients experienced deterioration in cortical bone over time, which was driven by hyperparathyroidism and increased bone turnover. It was established by the previous studies that chronic PTH excess is catabolic for cortical bone, causing sub-periosteal and intra-cortical erosion, and can be anabolic for trabecular bone causing increased trabecular thickness and number, thus supporting the reduced RI scores and increased FD values in ESRD patients.
Limitations and future prospects
PRs represent a two-dimensional image of a three-dimensional structure. Three-dimensional imaging performed with CBCT will certainly give more valuable information. However, CBCT was not chosen because it is not a routine diagnostic tool for a dentist. Also, the sample size of the study group was small, preventing the generalization of the results. Further, this study lacks the correlation of FD and RI with biochemical parameters (e.g., parathyroid hormone, serum calcium, phosphorus, alkaline phosphatase, and vitamin D levels) which could have highlighted some more certain facts regarding the same.
However, further research with large sample sizes in this area would help in ascertaining the role of orophysician in improving the quality of life in the CKD patients.
| Conclusion|| |
This study brings to light the effects of CKD on the mandibular cortical bone and can be manifested as decreased MI. This finding suggests that MI analysis might be a promising, simple, and cost-effective tool for evaluating cortical bone structure in this high-risk population and any signs of osteoporosis could be withheld at the earliest stage with a prompt referral.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Levey AS, De Jong PE, Coresh J, Nahas ME, Astor BC, Matsushita K, et al
. The definition, classification, and prognosis of chronic kidney disease: A KDIGO controversies conference report. Kidney Int 2011;80:17-28.
Jha V, Modi G. Uncovering the rising kidney failure deaths in India. Lancet Glob Health 2017;5:e14-5.
Varma PP. Prevalence of chronic kidney disease in India-Where are we heading? Indian J Nephrol 2015;25:133-5.
] [Full text]
Miller PD. Chronic kidney disease and osteoporosis: Evaluation and management. Bonekey Rep 2014;3:542.
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.
Nickolas TL, Stein EM, Dworakowski E, Nishiyama KK, Komandah-Kosseh M, Zhang CA, et al
. Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res 2013;28:1811-20.
Klemetti E, Kolmakov S, Kröger H. Pantomography in assessment of the osteoporosis risk group. Eur J Oral Sci 1994;102:68-72.
Ledgerton D, Horner K, Devlin H, Worthington H. Radiomorphometric indices of the mandible in a British female population. Dentomaxillofac Radiol 1999;28:173-81.
Bozdag G, Sener S. The evaluation of MCI, MI, PMI and GT on both genders with different age and dental status. Dentomaxillofac Radiol 2015;44:20140435.
White SC, Rudolph DJ. Alterations of the trabecular pattern of the jaws in patients with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;88:628-35.
Koh KJ, Kim KA. Utility of the computed tomography indices on cone beam computed tomography images in the diagnosis of osteoporosis in women. Imaging Sci Dent 2011;41:101-6.
Çağlayan F, Dağistan S, Keleş M. The osseous and dental changes of patients with chronic renal failure by CBCT. Dentomaxillofac Radiol 2015;44:20140398.
Henriques JC, Castilho JC, Jacobs R, Amorim JB, Rosa RR, Matai CV. Correlation between hand/wrist and panoramic radiographs in severe secondary hyperparathyroidism. Clin Oral Investig 2013;17:1611-7.
Henriques JC, de Melo Castilho JC, Jacobs R, Amorim JB, Rosa RR, Matai CV. Severe secondary hyperparathyroidism and panoramic radiography parameters. Clin Oral Investig 2014;18:941-8.
Shrout MK, Roberson B, Potter BJ, Mailhot JM, Hildebolt CF. A comparison of 2 patient populations using fractal analysis. J Periodontol 1998;69:9-13.
Bollen AM, Taguchi A, Hujoel PP, Hollender LG. Fractal dimension on dental radiographs. Dentomaxillofac Radiol 2001;30:270-5.
Ruttimann UE, Webber RL, Hazelrig JB. Fractal dimension fromradiographs of peridental alveolar bone. A possible diagnostic indicator of osteoporosis. Oral Surg Oral Med Oral Pathol 1992;74:98-100.
Hua Y, Nackaerts O, Duyck J, Maes F, Jacobs R. Bone quality assessment based on cone beam computed tomography imaging. Clin Oral Implants Res 2009;20:767-71.
Saeed SS, Ibraheem UM, Alnema MM. Quantitative analysis by pixel intensity and fractal dimensions for imaging diagnosis of periapical lesions. Int J Enhanced Res Sci Technol Eng 2014;3:138-44.
Demirbaş AK, Ergün S, Güneri P, Aktener BO, Boyacıoğlu H. Mandibular bone changes in sickle cell anemia: Fractal analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:e41-8.
Updike SX, Nowzari H. Fractal analysis of dental radiographs to detect periodontitis-induced trabecular changes. J Periodontal Res 2008;43:658-64.
Southard TE, Southard KA, Krizan KE, Hillis SL, Haller JW, Keller J, et al
. Mandibular bone density and fractal dimension in rabbits with induced osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:244-9.
Ergun S, Saracoglu A, Guneri P, Özpınar B. Application of fractal analysis in hyperparathyroidism. Dentomaxillofac Radiol 2009;38:281-9.
Secgin CK, Kulah CK, Gulsahi A. Analysis of mandibular changes using panoramic-based indices in patients with chronic renal failure. Int J Artif Organs 2017;0. doi: 10.5301/ijao. 5000649. Online ahead of print.
Carvalho CG, Pereira RC, Gales B, Salusky IB, Wesseling-Perry K. Cortical and trabecular bone in pediatric end-stage kidney disease. Pediatr Nephrol 2015;30:497-502.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]