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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2021  |  Volume : 32  |  Issue : 2  |  Page : 455-467
Assessment of mandibular osseous changes using radiomorphometric indices by cone beam computed tomography in patients with End-stage renal failure versus normal population (Observational Study)


1 Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Cairo University, Cairo, Egypt
2 Department of Internal Medicine, Faculty of Medicine, Cairo University, Cairo, Egypt
3 Department of Oral and Maxillofacial Radiology, Faculty of Dentistry; Department of Oral and Maxillofacial Radiology, Post Graduate Affairs and Scientific Research and Head of Quality Assurance Unit, Faculty of Dentistry, Cairo University, Cairo, Egypt

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Date of Web Publication11-Jan-2022
 

   Abstract 


Our study aimed to assess mandibular osseous changes using radiomorphometric indices by Cone-Beam Computed Tomography (CBCT) in patients with end-stage renal failure (ESRF) to evaluate their jaw bone quality versus a healthy sex- and age-matching population. Twenty-six patients were included in this study. They were divided equally into two groups. The first group (study group) included 13 ESRF patients and the second group (control group) included 13 patients free from any condition that could affect bone metabolism. All of the 26 participants were scanned using CBCT scanner then five indices were obtained from the reformatted panoramic images and the cross-sectional images of each mandible bilaterally mandibular cortical index (MCI), panoramic mandibular index (PMI), mental index (MI), gonial index (GI), and antegonial index (AI). There was no significant difference between MCI, MI, AI, GI and PMI of patients with ESRF and that of the control group. The assessment of intra-observer and inter-observer reliability regarding all measurements (GI, AGI, MI, and PMI) showed very strong agreement except MCI showed substantial agreement. Bone quality assessment of patients, investigated in the current study, with ESRF was not different from those of healthy sex- and age-matching dental patients using radiomorphometric indices. Quantitative radiomorphometric indices (MI, AI, GI, and PMI) are more reliable than qualitative radiomorphometric index (MCI) in the assessment of jawbones.

How to cite this article:
Mohamed EM, Abdel-Samad AM, Darwish RA, Dahaba MM. Assessment of mandibular osseous changes using radiomorphometric indices by cone beam computed tomography in patients with End-stage renal failure versus normal population (Observational Study). Saudi J Kidney Dis Transpl 2021;32:455-67

How to cite this URL:
Mohamed EM, Abdel-Samad AM, Darwish RA, Dahaba MM. Assessment of mandibular osseous changes using radiomorphometric indices by cone beam computed tomography in patients with End-stage renal failure versus normal population (Observational Study). Saudi J Kidney Dis Transpl [serial online] 2021 [cited 2022 Jul 6];32:455-67. Available from: https://www.sjkdt.org/text.asp?2021/32/2/455/335458



   Introduction Top


End-stage renal failure (ESRF) is a medical disorder that can affect a large number of populations up to 10%. There are several oral symptoms associated with renal disease, up to 90% of patients in different populations having oral symptoms.[1] ESRF is associated with changes in bone and mineral metabolism. These osseous changes result from a combination of various factors such as Vitamin D deficiency, hyperparathyroidism, malnutrition, and the use of certain drugs or hypogonadism. Osteoporosis and renal osteodystrophy are the most common bone abnormalities that result from renal insufficiency.[2],[3]

Osteoporosis is a skeletal disorder that affects strength, bone quantity, and bone quality due to deterioration of the bone microarchitecture.[4]

Renal osteodystrophy is a major clinical problem in patients on hemodialysis and predominantly affects cortical bone.[5],[6]

Radiolucent giant cell lesions (brown tumor), generalized osteoporosis, trabecular bone alterations (ground glass appearance), sub-periosteal bone resorption, metastatic soft tissue calcifications, loss of lamina dura, pulpal narrowing, and periodontal defects are the most common radiographic manifestations of renal osteodystrophy of the jaws.[2],[7]

Two-dimensional (2D) imaging modality, cone-beam computed tomography and dual-energy X-ray absorptiometry are commonly used for the assessment of bone quality.[1]

Dental panoramic radiographs play a significant role in the identification and evaluation of patients with low bone mineral density and it is useful for showing the common radiographic manifestations of renal osteodystrophy, such as cortical bone resorption at the mandibular angle, mental foramen, mandibular canal, and loss of the lamina dura of the teeth.[6],[8],[9]

There are numerous radiomorphometric indices that use measurements in panoramic radiographs, which have been suggested as possible signs of decreased value of bone mineral density including the mandibular cortical index (MCI), panoramic mandibular index (PMI), mental index (MI), antegonial index (AI) and gonial index (GI).[10] However, there are some limitations of panoramic radiograph, as it is a 2D imaging technique so it cannot illustrate the buccolingual width, suffers from the superimposition.[6],[11]

It was revealed that Cone Beam Computed Tomography (CBCT) can also be used to determine mandibular indexes in several studies. CBCT does not magnify or overlap neighboring structures, which are essential problems in panoramic radiography. CBCT images are acquired by using a low dose of radiation, shorter patient examination time, and lower costs than does CT, and it is realistic for oral and maxillofacial procedures.[3],[11],[12],[13]

That’s why this study was undertaken to assess mandibular osseous changes using radiomorphometric indices by CBCT in patients with ESRF to evaluate their jaw bone quality versus a healthy sex- and age-matching population.


   Materials and Method Top


Study design

This study is an observational cross-sectional, prospective study (data collection was planned before the index test and reference standard test were performed). Before performing any procedure, all patients received a thorough explanation concerning the clinical procedures as well as the possible risks and radiation hazards. Written informed consent was obtained and the diagnostic chart was completed detailing the patients’ names, age, sex, and duration of dialysis. The performance of this study was approved by the “Research Ethics Committee” of the Faculty of Dentistry, Cairo University.

Sample size calculation

The aim of this study is to assess bone quality in ESRF patients in comparison to normal population using radiomorphometric indices by CBCT. Based on previous studies by Dagistan et al, the mean antiGI value of the control group was 4.41 and the standard deviation was 0.72, while the mean of the dialysis patients was 3 and the standard deviation 1.05, a total sample size of 16 will be sufficient to detect a power of 80% and a significance level of 5%. The number is increased to a total sample size of 20 to allow for the use non-parametric test. To allow for 25% losses, the sample was further increased to 26 (13 participants in each group). Sample size estimation was performed by n-Query statistical package.

Sample grouping

Twenty-six patients were included in this study. They were divided equally into two groups. The first group (study group) included thirteen ESRF patients (6 females and 7 males) selected from the Out-Patient Clinic of Nephrology Department and the Artificial Kidney Unit, KasrAl Ainy Hospital, Cairo University. The second group (control group) included thirteen patients (6 females and 7 males) selected from the Prosthodontics and Surgical Departments of Faculty of Dentistry, Cairo University, recommended for CBCT imaging prior to implant placement.

Sample Selection

Chronic kidney disease patients undergoing hemodialysis (three times/week), history of dialysis (≥1 year), parathyroid hormone (PTH) (140–630) (above or below levels were excluded to avoid high and low bone turnover). Age range between (18 and 40) years not >40 to exclude postmenopausal osteoporosis to prevent the effect of the hormonal changes in the menopausal period on the bone metabolism, missing teeth in maxilla or mandible, males and females and Egyptian population were included in this study. Patients suffering from diabetes mellitus (DM), radiotherapy, alcohol consumption, corticosteroid medication, hyperthyroidism, early stages of renal failure, and completely edentulous patients in mandible or maxilla were excluded from the study. The control group was chosen with the same gender, nationality, and same age range as those of the patient group.

Laboratory investigation

For control group members, blood sampling was done by venipuncture to determine alkaline phosphatase enzyme (reference range is 50–136 IU/L), calcium (reference range is 8.6–10.2), phosphorous (reference range is 2.5–4.5), and renal function test (reference range of serum creatinine is 0.60–1.30 and blood urea from 17.0–43.0).

For the study group members, blood sampling was done by venipuncture to determine the PTH level (reference range is 15.0–65.0), calcium, phosphorous, and alkaline phosphatase enzyme. The laboratory tests were performed at the Faculty of Medicine, Cairo University.

Cone Beam Computed Tomography Assessment

Patient imaging

All of the 26 participants were scanned using the PlanmecaProMax® 3D Mid (Proface) (Asentajankatu, Helsinki, Finland) CBCT scanner at the Oral and Maxillofacial Radiology Department, Faculty of Dentistry, Cairo University using exposure parameters (90 kVp, 8 mA, 13.5 sec exposure time, 400 μm voxel size and 20 cm × 10 cm field of view). CBCT was obtained for the region of interest (ROI) for all the participants. Patient’s head was aligned using a laser beam system accurately indicating the correct anatomical positioning points and stabilized using a chin rest and lateral head supports.

Image analysis and measurements

CBCT assessment of the 26 participants was performed using the Planmeca Romexis viewer (Asentajankatu, Helsinki, Finland). Five indices were measured of each mandible bilaterally (GI, AI, MCI, MI, and PMI)

The GI was assessed on the reformatted panoramic image of each mandible bilaterally with buccolingual thickness 25 mm. For measurement of GI one line was drawn tangential to the mandibular ramus at the most convex alignment and another line tangential to the mandibular body. Finally, a third line (bisector) bisecting this angle was finally drawn. To obtain the measurement for the GI, the thickness of cortex intersected by bisector line was measured as GI[14],[15] [Figure 1].
Figure 1: Measurement of gonial index on the left side of one of the investigated mandibles on a cropped reformatted panoramic image.

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The AI was assessed on the reformatted panoramic image of each mandible bilaterally with buccolingual thickness 25 mm. It was a measurement of cortical width in the region that is anterior to the gonion, at a point that is identified by extending a line of “best fit” on the anterior border of the ascending ramus, down to the lower border of the mandible.[3],[14],[15] [Figure 2].
Figure 2: Measurement of AGI on the left side of one of the investigated mandibles on a cropped reformatted panoramic image.

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The MCI was evaluated on the reformatted panoramic images and cross-section cuts with 1 mm slice thickness and 1 mm intercut distance of each mandible bilaterally by inspection.

The morphological appearance of mandibular cortical bone distally to the mental foramen was classified into:

  • Class I, the endosteal margin of the cortex is even and sharp on both sides.
  • Class II, the endosteal margin shows semilunar defects or seems to form endosteal cortical residues on one or both sides.
  • Class III, the cortical layer forms heavy endosteal residues and is clearly porous.[16],[17]


For MI, mandibular cortical thickness was measured on the line that was perpendicular to the bottom of the mandible at the middle of the mental foramen on cross-section images.[3],[6],[18] [Figure 3].
Figure 3: Measurement of mental index of one of the investigated mandibles on cross-section image of cone-beam computed tomography.

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PMI was the ratio of the thickness of the mandibular cortex to the distance between the mental foramen and the inferior mandibular cortex. It was assessed on cross-section images[3],[18],[19] [Figure 4].
Figure 4: Cross-section cut of cone-beam computed tomography showing panoramic mandibular index (a/average of the superior and inferior border of mental foramen to inferior border of the mandible).

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Pearson’s Correlation Coefficient was applied to the linear measurements that are normally distributed, linear measurements that are not normally distributed as well as MCI; Spearman’s Correlation Coefficient was applied.

Blinding and inter and intra-observer agreement

Two observers, with experience ranging from 10–30 years in the field of oral and maxillo-facial Radiology, performed the analysis. The CBCT images were independently and separately assessed by the two radiologists in a double-blind fashion. A third radiologist, not involved in the image analysis procedures, was responsible for coding of the cases. In addition, one of the two observers performed the analysis twice. Inter-observer and intra-observer variations were statistically calculated. The means of the trials were pooled and included in further statistical analysis.

Statistical package used for this study: R statistical package, version 3.3.1 (2016-06-21). Copyright (C) 2016. The R Foundation for Statistical Computing. [Reference: *R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL: https://www.R-project.org/.]


   Result Top


Assessment of intra and inter-observer reliability for linear measurements (GI, AI, MI and PMI) showed very strong agreement range from 0.91–0.100 by using Intra-class Correlation Coefficient, statistical significance (P ≤0.05). For categorical data (MCI) Cohen’s Kappa was calculated and showed substantial agreement range from 0.61 to 0.80, statistical significance (P ≤0.05).

The descriptive analysis of age and gender distribution of participants showed that mean age of the control group participants is (33.91 years ± 7.56) which is more than that of the ESRF group participants (30.27 ± 5.61 years). The difference between both groups’ age is statistically insignificant substantial agreement. Both groups have the same gender distribution where 54% of each group’s participants are males while 46% are females.

The descriptive analysis of radio morphometric indices of control and ESRF groups showed that there was no significant difference between MCI, MI, AI, GI, and right side of PMI of patients with CRF and that of the control groupbut for the left side of PMI there was statistically significant difference between control and ESRF group [Figure 5],[Figure 6],[Figure 7],[Figure 8],[Figure 9],[Figure 10],[Figure 11],[Figure 12] and [Table 1], [Table 2].
Figure 5: Bar chart diagram representing mean gonial index in both control and renal failure group.

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Figure 6: Bar chart diagram representing mean antegonial index in both control and renal failure group.

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Figure 7: Bar chart diagram representing mean mental index in both control and renal failure group.

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Figure 8: Bar chart diagram representing mean panoramic mandibular index in both control and renal failure group.

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Figure 9: Bar chart diagram representing mandibular cortical index in both control and renal failure groups.

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Figure 10: Reformatted panoramic and cross-section images of cone-beam computed tomography showing C1 of one of the investigated mandibles; the endosteal margin of the cortex is even and sharp.

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Figure 11: Reformatted panoramic and cross-section images of cone-beam computed tomography showing C2 of one of the investigated mandibles; the endosteal margin shows semilunar defects; seems to form endosteal cortical residues.

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Figure 12: Reformatted panoramic and cross-section images of cone-beam computed tomography showing C3 of one of the investigated mandibles; the cortical layer forms heavy endosteal residues and is clearly porous.

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Table 1: Level of Ca, Ph, ALP, and PTH in end-stage renal failure patients.

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Table 2: Descriptive analysis of radiomorphometric indices (GI, AI, MI, and PMI) of control and renal failure group.

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The correlation between radiomorphometric indices and duration of dialysis in renal failure group showed that there was no significant correlation between any of the radiomorphometric indices with the duration of the renal dialysis [Table 3] except with the right side AI [Figure 13] and [Table 4].
Figure 13: Scatter diagram showing antegonial index inversely correlated with duration of dialysis.

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Table 3: Descriptive analysis of radiomorphometric index (MCI) of control and renal failure group.

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Table 4: Assessment of the correlation between all parameters and duration of dialysis.

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   Discussion Top


Secondary hyperparathyroidism is a result of renal osteodystrophy and affects up to 92% of patients undergoing hemodialysis.[6] Changes in bone metabolism in patients with ESRF are common and are caused mainly by secondary hyperparathyroidism. In the jawbones, the most commonly observed radiographic manifestations are bone demineralization, decreased trabeculation, decreased thickness of cortical bone, ground-glass appearance of bone, brown tumor, fibrocystic lesions, jaw fracture, and abnormal bone healing.[2],[6],[9]

Panoramic radiographs are beneficial for showing the effects of CRF on bones, such as resorption of mandibular cortical bone, decreased thickness of the cortical bone, and a ground-glass appearance.[6] In this respect, the panoramic-based indices, such as MCI, GI, AGI, PMI, and MI are assumed to be used to assess cortical bone status.[5],[6]

However, linear measurements on panoramic radiographs share limitations mainly related to unequal magnification and geometric distortion.[6],[20]

In contrast to panoramic radiographs, CBCT images allow 3D visualization of the dento-maxillofacial structures, without superimposition, magnification, or distortion, and provide an accurate display of the vertical as well as the buccolingual dimensions of the mandible, in actual size. Recently, it has been shown in several studies that CBCT can also be used to determine mandibular indices (panoramic-based indices).[3],[12],[13]

Consequently, this study was designed to assess early mandibular osseous changes using radiomorphometric indices by CBCT in patients with ESRF with PTH (140–600 pg/ mL) to evaluate their jaw bone quality versus a healthy sex- and age-matching population.

This study is the first one conducted on this PTH range using CBCT, this range was used in other studies but using panoramic radiograph not CBCT

Regarding the criteria of patient selection in the study group, all the patients were suffering from end-stage of renal disease (stage5), were undergoing renal dialysis (hemodialysis), three times/week, and free from any other systemic disease (DM, hyperthyroidism, and cortico-steroid medication) affecting the bone quality according to Dagistan et al,[15] Henriques et al,[18] Çağlayan et al,[3] and Rangel and Caio.[21]

History of dialysis (≥1 year), PTH (140–630) not above or below to exclude high and low bone turnover as reported by Rangel and Caio,[21] and age group (18–40 years) not >40 to exclude postmenopausal osteoporosis to prevent the effect of the hormonal changes in the menopausal period on the bone metabolism (the same age range in the control group)[14] and missing teeth in mandible or maxilla recommended for implant placement in both groups.

Patients of both ESRF and the control groups had the same demographic features, including age and gender. There were no statistically significant differences between both groups in patients’ age and gender. Hence, both factors would not play any modifying role on the results of both groups.

Regarding MCI, in this study, there was no statistically significant differences between patients with ESRF and that of the controls. Our results are in contrast to the results of Secgin et al,[6] as their results revealed that cortical porosity occurs in ESRF patients four times more often than in healthy controls. This finding could be attributed to the selected age group which ranged from 18–73 years for both patient and control groups which could introduce the possibility of postmenopausal osteoporosis in female patients. This could be a factor that played a role in the difference between groups.

Also Henriques et al,[9] and Henriques et al,[18] evaluated the effects of renal osteodystrophy using panoramic radiography parameters, including MCI. In the two studies, they found that the mandibular cortex was more porous and resorption of the mandibular cortex tended to increase with increasing PTH levels in ESRF patients. This difference may be attributed to difference in patient selection as their study included patients with PTH levels of ≥500 pg/mL rendering adverse effects of the disease, such as bone resorption, could be detected more easily on panoramic radiographs.

Çağlayan et al,[3] also examined the osseous changes in the jaws of patients with CRF using CBCT, and they found statistically significant changes in MCI between ESRF patients and healthy controls. This may be due to their use of higher exposure parameters and higher resolution (110 kV and 0.16-mm voxel) as well as the different orientation of reconstructed CBCT images. Also, the subjective nature of MCI may be a reason for this variation.

For MI, although the cutoff values for detecting osteoporosis ranged from 2.69 mm to 5 mm, and even if consensus could not be reached between researchers, many studies have suggested that patients with MI ≤3 mm should be referred for further osteoporosis investigations.[10],[22]

MI measurement of the right side in the control group is 3.44 ±0.44 mm and in the ESRF group is 3.09 ± 0.97 mm. MI measurement of the left side in the control group is 3.61 ± 0.5 mm and in the ESRF group is 2.85 ± 1.07 mm which is more than normal cutoff value.

Our results for MI showed that on the right side, the difference between both groups’ was statistically insignificant. However on the left side, MI for the control group is (3.61 mm ± 0.5) which was more than that of the ESRF group (2.85 ± 1.07 mm).

The difference between both groups was statistically significant but still, the ESRF group (2.85 ± 1.07 mm) is higher than the cutoff value (2.69 mm) which rendered this difference clinically insignificant. Hence, the difference between groups was not significant for MI as agreed with Henriques et al,[9] Henriques et al,[18] Çağlayan et al,[3] and Secgin et al.[6] They emphasized that the MI tended to decrease with increasing PTH levels in ESRF patients, but no significant difference was found between the groups for MI.

Considering AI, the normal cutoff value >3.2 mm.[16],[23] Mean right AI measurement in the control group is (2.3 mm ± 0.49) and the renal failure group is (1.77 mm ± 0.78). The mean left AI measurement in the control group is (2.2 mm ± 0.63), renal failure group is (1.89 mm ± 0.92) both groups are below the level of normal cut off value.

In the present study, no statistically significant difference was found between renal dialysis patients and the control group in terms of AI values which is in close proximity with the study of Padbury et al[24] and Çağlayan et al.[3]

The opposite was reported by Dagistan et al,[15] Rai et al[25] and Mohammed and Hassan.[14] This difference may be due to using CBCT instead of panoramic. As panoramic radiographs share limitations mainly related to unequal magnification and geometric distortion.[6]

For GI, Gonial cortical bone thickness <1 mm was interpreted as the radiographic indication of metabolic bone diseases.[9]

The mean GI measurement of the right side in the control group is (1.06 mm ± 0.24), for renal failure group is (1.16 ± 0.7 mm). The mean GI measurement of the left side in the control group is (1.14 mm ± 0.24), ESRF group (1.25 ± 0.97 mm); both groups are above than normal cut-off value.

The present study showed that there was no statistically significant difference between dialysis patients and the control group with mean value > 1.

On the contrary, Dagistan et al,[15] Mohammed and Hassan[14] and Gavaldá et al[8] stated in their study that the gonial cortical bone was thinner in hemodialysis patients compared to the control group. This difference could be due to their patients selection with age >40 years which introduces the possibility of postmenopausal osteoporosis in female patients. This could be responsible for the difference between groups.

For PMI, the normal cutoff value >0.3.[16],[23] Mean PMI measurement of the right side in the control group is (0.24 mm ± 0.04) and ESRF group is (0.21 ± 0.05 mm). The mean PMI measurement of the left side in the control group is (0.25 mm ± 0.04) and for the ESRF group is (0.2 ± 0.06 mm) which less than normal cut off value.

On the right side, the difference between both groups’ was statistically insignificant. However on the left side, the mean in the control group was (0.25 mm ± 0.04) which is more than that of the ESRF group (0.2 ± 0.06 mm). Although the difference between both groups was statistically significant both groups were lower than the cut off value which rendered this difference clinically insignificant.

Henriques et al[18] and Caglayan et al.[3] also did not find significant differences in PMI values of patients with ESRF similar to our results.

Concerning the correlation between all radio-morphometric indices and duration of dialysis, the results showed that there was no significant correlation between any of the measurements with the duration of the renal dialysis. These results are in line with Secgin et al.[6] except for the right side AI measurement.

The assessment of intra-rater reliability and inter-rater reliability regarding all radiomorphometric indices showed very strong agreement except for MCI which showed substantial agreement because MCI is a qualitative assessment depending on visual inspection. These results are in line with Gulsahi et al,[19] Henriques et al[18] and Secgin et al.[6]


   Conclusion Top


From the present work, the following conclusions could be reached:

  • Bone quality assessment of patients, investigated in the current study, with chronic renal failure was not different from those of healthy sex- and age- matching dental patients using radiomorphometric indices.
  • Quantitative radiomorphometric indices (MI, AI, GI, and PMI) are more reliable than qualitative radiomorphometric index (MCI) in the assessment of jawbones.


Conflict of interest: None declared.



 
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Correspondence Address:
Eman Mamdouh Mohamed
Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Cairo University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1319-2442.335458

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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    Abstract
   Introduction
   Materials and Method
   Result
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables
 

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