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 Table of Contents  
RESEARCH ARTICLE
Year : 2022  |  Volume : 10  |  Issue : 1  |  Page : 19-28

Pre-implant evaluation of quantity and quality of mandibular bone in male diabetes mellitus patients using cone-beam computed tomography: A case–control study


1 Department of Oral Medicine and Radiology, Private Dental Practitioner, Hyderabad, Telangana, India
2 Department of Oral Medicine and Radiology, Panineeya Mahavidyalaya Institute of Dental Sciences and Research Centre, Hyderabad, Telangana, India

Date of Submission28-Mar-2022
Date of Decision05-Apr-2022
Date of Acceptance06-Apr-2022
Date of Web Publication21-Apr-2022

Correspondence Address:
Anuja Kammari
Department of Oral Medicine and Radiology, Private Dental Practitioner, H. No: 6-75, Shabad (Village and Mandal),R.R District - 509 217, Telangana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jomr.jomr_7_22

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  Abstract 


Objectives: This study was designed to evaluate and compare the quantity and quality of mandibular bone in the first molar region in male type 2 diabetes mellitus (T2DM) patients with healthy controls using cone-beam computed tomography (CBCT) imaging technique. The bone characteristics in T2DM patients were correlated with diabetes duration. Materials and Methods: The study included 25 male diabetic patients and 25 nondiabetic male patients with missing mandibular 1st molar, in the age group ranging from 35 to 60 years. HDX WILL CBCT machine utilized to obtain CBCT images. Bone density and quantitative linear measurements were performed in OnDemand software, along with glycated hemoglobin levels of diabetic patients. The obtained data were subjected to statistical analysis using the SPSS software version 20.0. Results: Type 2 diabetic patients had greater bone density as compared to controls. The height of bone is less in diabetic patients than in nondiabetics, and other quantitative linear measurements were found similar in both groups. Conclusion: This study concluded that CBCT can be used in preimplant planning and helps the clinician assess bone measurements and bone density.

Keywords: Bone density, cone-beam computed tomography, diabetes mellitus, quantitative analysis


How to cite this article:
Kammari A, Garlapati K, Ajaykartik K, Ignatius AV, Surekha B E, Saba A. Pre-implant evaluation of quantity and quality of mandibular bone in male diabetes mellitus patients using cone-beam computed tomography: A case–control study. J Oral Maxillofac Radiol 2022;10:19-28

How to cite this URL:
Kammari A, Garlapati K, Ajaykartik K, Ignatius AV, Surekha B E, Saba A. Pre-implant evaluation of quantity and quality of mandibular bone in male diabetes mellitus patients using cone-beam computed tomography: A case–control study. J Oral Maxillofac Radiol [serial online] 2022 [cited 2022 Aug 18];10:19-28. Available from: https://www.joomr.org/text.asp?2022/10/1/19/343695




  Introduction Top


Diabetes mellitus (DM) is a chronic metabolic disorder that causes hyperglycemia and leads to multiple complications caused by micro and macroangiopathy.[1] DM is also associated with some complications affecting the skeleton, decreased bone mineral density (BMD) associated with osteopenia or osteoporosis, and impaired bone regeneration potential. The decrease in BMD and osteoporosis can be considered a risk factor for reduced mandibular alveolar bone density. The mandibular bone quality and quantity can be detected using different oral and maxillofacial radiographic techniques, crucial in dental implant treatment planning.[2]

Proper presurgical dental implant planning and accurate assessment of bone structure are essential before implant placement.[3] With the advancement in dental and maxillofacial radiology, cone-beam computed tomography (CBCT) was introduced, which generates the three-dimensional (3D) information and offers the potential of improved diagnosis and treatment planning for a wide range of clinical applications in implant dentistry.[4] Hence, this study is designed to evaluate and compare the quantity and quality of mandibular bone in the 1st molar region in male DM patients with healthy controls using CBCT imaging technique for prosthetic implant placement.


  Materials and Methods Top


Study setting

The male patients attending the Department of Oral Medicine and Radiology in Panineeya Mahavidyalaya Institute of Dental Sciences and Research Center, Hyderabad, were clinically diagnosed with missing mandibular first molar (right/left/both), seeking prosthetic implant placement and indicated for CBCT imaging were selected. The Institutional Ethical Committee Review Board approved the study design and also obtained informed consent from each patient before including them in the study.

Sample selection

This cross-sectional case–control study comprises 25 male diabetic patients in the study group and 25 nondiabetic male patients in the control group with missing mandibular first molar and age ranging from 35 to 60 years. The study excluded (A) female patients, (b) patients who are on medication that interferes with bone metabolism, (c) inadequate bone for implant placement, (d) patients with metabolic disorders involving bone except for DM, (e) patients who are smokers, (f) patients who underwent radiotherapy and chemotherapy, and (g) patients with bone diseases.

Clinical examination

The patients were selected by simple random method of sampling. The selected patient was comfortably seated in the dental chair and a detailed case history was recorded. Blood samples were collected from diabetic patients by venipuncture of the antecubital vein to evaluate glycated hemoglobin (HbA1c) levels using the high performance liquid chromatography (HPLC) technology. All patients indicated for implant placement were scanned for the region of interest (ROI) using the HDX WILL CBCT scanner. 3D imaging data were acquired at 85 kV, 8 mA, exposure time of 24 seconds, FOV of 8 × 5 cm (the width andheight) and 0.3mm voxel size. CBCT images reconstructions were done and analyzed using OnDemand3D® Viewer. All the images were obtained in digital imaging and communications in medicine format (DICOM) and are viewed in OnDemand3D® Viewer.

Data collection using OnDemand3D® Viewer

In each case CBCT data was collected and panoramic images were formatted into 20 mm thick sections, with filter of 1.5x. Potential implant sites were selected and four reference lines labelled as R1 with width of 2mm were selected for that implant site [Figure 1]. The cross sectional (Trans axial) sections corresponding to those four reference lines were selected for the quantitative evaluation. On the panoramic image another reference line labelled as R2 is positioned in the mid region of crest of alveolar ridge to mandibular canal [Figure 1] and linear measurements i.e. height (H) and inferior cortex width (IC) were assessed on R1 and buccal cortex width (BC), lingual cortex width (LC), total width of bone (W1), width of cancellous bone (W2) were assessed on R2 using cross sectional (Trans axial) sections of CBCT images corresponding to those four reference lines (R1) of the potential implant site.
Figure 1: CBCT panoramic image showing reference lines R1 and R2. CBCT: Cone-beam computed tomography

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Cross sectional (Trans axial) sections were formatted into 2mm thick sections, with filter of 1.5x. The four sections corresponding with those four reference lines (R1) were selected [Figure 2] and height labelled as H was measured from crest of alveolar ridge to mandibular canal on the reference lines R1 and inferior cortex labelled as IC was measured on the same reference lines R1 [Figure 3], total bone width at the mid region between crest of alveolar ridge and mandibular canal labelled as W1 was measured from buccal cortex to lingual cortex on the reference line R2 [Figure 4] and width of the cancellous bone labelled as W2 is also measured on the same reference line R2 [Figure 5]. Width of buccal cortex labelled as BC, lingual cortex labelled as LC were also measured on the reference line R2 [Figure 6]. The average of the measurements from 4 sections were calculated and tabulated for statistical analysis.
Figure 2: Cross-sectional images (transaxial sections) corresponding with the four reference lines (R1)

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Figure 3: CBCT cross-sectional (transaxial) section depicting measurement of height of the bone measured from crest of alveolar ridge to mandibular canal (H) and inferior cortex width measured on the reference lines R1. CBCT: Cone beam computed tomography

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Figure 4: CBCT cross-sectional (transaxial) section depicting measurement of total bone width (W1) from buccal cortex to lingual cortex on the reference line R2. CBCT: Cone beam computed tomography

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Figure 5: CBCT cross-sectional (transaxial) section depicting measurement of cancellous bone width (W2) on the reference line R2. CBCT: Cone beam computed tomography

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Figure 6: CBCT cross-sectional (transaxial) section depicting measurement of buccal cortex width and lingual cortex width on the reference line R2. CBCT: Cone beam computed tomography

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A simulated implant was placed at the implant site on the panoramic image [Figure 7] and mean and standard deviation values of bone density inside the simulated implant and outside the simulated implant calculated by OnDemand software were obtained [Figure 8].
Figure 7: CBCT panoramic image showing placement of simulated implant. CBCT: Cone beam computed tomography

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Figure 8: On-demand software showing mean and SD values of bone density inside the simulated implant and outside the simulated implant. SD: Standard deviation

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Statistical analysis

The measurements from 4 transaxial sections were calculated and statistically analyzed using IBM SPSS version 20.0 software. Intergroup comparison of linear measurements and bone density was analyzed using independent sample t-tests for equality of means. Comparing HbA1c levels and bone density, a comparison between diabetes and bone density duration was analyzed using the ANOVA test. The correlation between HbA1c levels and bone density, the correlation between diabetes duration and bone density, and the correlation between diabetes duration and quantitative measurements were analyzed using the Pearson correlation coefficient.


  Results Top


The mean density of the bone inside the simulated implant in the study group was 1722.9 ± 488.2 HU, and in the control group, 1400.7 ± 417.2 HU with a statistically significant difference (P = 0.016) [Graph 1]. The mean density of the bone outside the simulated implant in the study group was 1890.4 ± 474.3 HU, and in the control group, 1533.8 ± 455.4 HU with a statistically significant difference (P = 0.009) [Graph 2].



The study group includes five groups based on HbA1c values. The mean bone density of HbA1c values <6%, 6%–7%, 7%–9%, 9%–10%, and >10% inside the simulated implant was 2038.65 ± 612.02 HU, 1826.01 ± 559.12 HU, 1845.38 ± 459.27, 934.48 ± 75.05 HU, and 1649.57 ± 405.4HU, respectively. ANOVA analysis revealed no significant difference between the groups with a P = 0.125 [Graph 3]. The mean bone density of HbA1c values <6%, 6%–7%, 7%–9%, 9%–10%, and >10% outside the simulated implant was 2062 ± 582.25 HU, 2092.05 ± 570.92 HU, 1997.61 ± 436.30 HU, 1143.30 ± 88.89 HU, and 1824.83 ± 421.03 HU, respectively. ANOVA analysis revealed no significant difference between the groups with a P = 0.163 [Graph 4].



Correlation between HbA1c levels and mean bone density revealed a weak negative correlation between HbA1c levels and mean bone density inside the simulated implant (r = −0.203), which was nonsignificant, and the correlation between HbA1c levels and mean bone density outside the simulated implant showed a very weak negative correlation (r = −0.172) which was nonsignificant [Table 1].
Table 1: Correlation of glycated hemoglobin levels with density of bone

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Three groups of patients were divided based on the duration of diabetes. The mean bone density inside the simulated implant of diabetes duration lesser than or equal to 5 years, 6–10 years, and >10 years were 1703.22 ± 521.12 HU, 1730.17 ± 426.59HU, and 1786.32 ± 573.87HU, respectively. ANOVA analysis revealed no significant difference between the groups with a P = 0.958 [Graph 5]. The mean bone density outside the simulated implant of diabetes duration lesser than or equal to 5 years, 6–10 years, and >10 years was 1879.13 ± 531.48 HU, 1921.33 ± 352.54 HU, and 1886.65 ± 521.42 HU, respectively. ANOVA analysis revealed no significant difference between the groups with a P = 0.984 [Graph 5].



Correlation between the duration of diabetes and mean bone density inside the simulated implant revealed a nonsignificant, very weak positive correlation (r = 0.131), and even duration of diabetes and mean bone density outside the simulated implant showed a nonsignificant, very weak positive correlation (r = 0.065) [Table 2].
Table 2: Correlation of duration of diabetes with density of bone

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The mean value of bone height measured from crest of alveolar ridge to mandibular canal at the implant site in diabetic patients was 13.49 ± 2.78 mm, and in the control group, 15.55 ± 2.25 mm, which was greater in the control group and found a statistically significant difference (P = 0.006) [Graph 6].



The mean value of the mandible's width measured at the first molar region at the mid-region between the crest of alveolar ridge to the mandibular canal in diabetic patients was 10.76 ± 1.88 mm. The control group's mandibular width was 11.44 ± 2.11 mm, revealing a slightly decreased width in the diabetic group, which was nonsignificant (P = 0.231) [Graph 7].



The mean value of the width of cancellous bone in diabetic patients was 6.15 ± 1.57 mm, and in the control group, 6.74 ± 1.87 mm with no statistically significant difference (P = 0.231) between the groups [Graph 8].



The mean value of the buccal cortex's (BCs) width in diabetic patients was 2.32 ± 0.57 mm, and in the control group, to be 2.39 ± 0.5 mm with no significant difference (P = 0.675) between the groups [Graph 9]. The mean value of the lingual cortex's (LCs) width in diabetic patients was 2.23 ± 0.61 mm, and in the control group, 2.45 ± 0.48 mm with no significant difference (P = 0.163) between the groups [Graph 10]. The mean value of the inferior cortex's (ICs) width in diabetic patients was 3.73 ± 0.67 mm, and in the control group, 3.7 ± 0.64 mm, with no significant difference (P = 0.89) between both groups [Graph 11].



Correlation between disease duration and quantitative linear measurements revealed a nonsignificant, very weak positive correlation between the height of bone (r = 0.174) [Table 3] and the width of cancellous bone (r = 0.026) [Table 4]. In contrast, a nonsignificant very weak negative correlation in the width of total bone at the mandibular 1st molar region (r = −0.007) [Table 5], BC width (r = −0.055) [Table 6], LC width (r = −0.039) [Table 7], and nonsignificant weak negative correlation was observed with IC (r = −0.378) [Table 8].
Table 3: Correlation of duration of diabetes and height of bone

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Table 4: Correlation of duration of diabetes and width of total bone

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Table 5: Correlation of duration of diabetes and width of cancellous bone

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Table 6: Correlation of duration of diabetes and width of buccal cortex

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Table 7: Correlation of duration of diabetes and width of lingual cortex

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Table 8: Correlation of duration of diabetes and width of inferior cortex

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  Discussion Top


The American Diabetes Association defined diabetes as a group of metabolic diseases characterized by hyperglycemia resulting from defects in insulin secretion, insulin action, or both.[5] According to a report published in 2013 by the International Diabetes Federation, the global prevalence of diabetes among adults (20–79 years of age) was 8.3% (382 million people), with 14 million males more than females (198 million males versus 184 million females), the majority between the ages of 40–59 years. Type 2 DM (T2DM) is present in 90%–95% of patients with the disease, and most of them are adults.[6],[7]

Men have higher bone mineral content than women. Women ≥50 have four times more osteoporosis than men and two times higher rate of osteopenia. Menopause causing a decrease in estrogen and progesterone, which are bone protectors leading to early osteoporosis in women, while 20% of older men with osteoporosis have hypogonadism.[8] To eliminate the gender bias related to bone density, the present study included only men.

Type 2 diabetes is associated with an increase in BMD but a paradoxical increased risk for skeletal fractures. However, greater BMD in T2DM is not entirely protective. The strength of the bone may be lower than predicted for BMD. The microarchitectural bone defects associated with microvascular changes of diabetes may lead to bone fragility.[9] Different studies revealed increased,[10] decreased,[11],[12],[13] or normal[14] BMD values in type 2 DM. The present study results revealed a greater mean density of bone inside and outside the simulated implant in diabetic individuals than in the control group, which is in accordance with a study by Kenawy et al.[10] in which the mean maxillary trabecular bone density of the healthy group was statistically lower than that of the diabetic group. Greater BMD in type 2 diabetic patients associated with poor metabolic control may also explain by their hyperinsulinemia. Insulin in diabetic patients has an anabolic effect on the bone, where insulin binds on osteoblasts to receptors and promotes bone formation, indicating that insulin may be a physiological antagonist of bone resorption.[2]

In a study done by Jolly et al.,[14] no significant changes were seen in the bone density levels, evaluated using spiral computed tomography between the controlled diabetic and nondiabetic subjects. Another study was done by Ay et al.[13] where BMD measurements were performed on the panoramic radiographs using a five-step copper step wedge phantom, which was attached to each film cassette and by dual energy X-ray absorptiometry, no statistically significant difference was observed about BMD values between T2DM patients and healthy participants. According to these studies, there is no significant difference in BMD between controls and diabetics.

While contradictory to the present study results, Zhang et al.[12] study showed that diabetic patients had significantly lower cancellous BMD than nondiabetic subjects in the posterior mandibles using CBCT. In the study by Onoyama et al.,[11] similar results were achieved when the effect of T2DM on mandibular bone in Goto–Kakizaki diabetic rats was compared to nondiabetic Wistar reduced trabecular BMD in the mandibular molar area which was noticed in Goto–Kakizaki diabetic rats.

HbA1c analysis in the blood provides evidence of a person's average blood glucose levels during the previous 3 months, which is the estimated half-life of red blood cells. HbA1c, diabetes testing, and monitoring are a standard of care, particularly the type 2 diabetes.[15] Hence, in the present study, the diabetic status of the participants in the study group was assessed based on HbA1c levels. The five groups of HbA1c values comparing HbA1c values with bone density inside the simulated implant and outside the simulated implant were carried out. There was no significant difference between the groups. The least value of bone density was for 9%–10% HbA1c level.

There are very few studies on the comparison of mandibular bone density with HbA1c levels. Nemtoi et al.[16] studied comparing 4 groups of HbA1c values with bone quality. Seven patients (25.93%) had D1 bone quality, and 20 patients (74.07%) had D2 bone quality in ≤6% HbA1c level group while 8 patients (100%) in 6.1%–8%. Nine patients (100%) in 8.1%–10% had D3 bone quality and 6 patients (100%) in >10.1% had D4 bone quality demonstrating poor bone quality, i.e., D3 and D4 in the posterior region of the mandible in diabetes patients with poor metabolic control.

In the present study, no significant correlation was found between HbA1c levels and bone density, which is similar to the study done by Kenawy et al.[10] where no significant correlation was found between HbA1c levels and maxillary bone density measurements assessed using CBCT. While in a study by Nemtoi et al.,[16] significant inverse correlation was found between bone density in the posterior region of the mandible and HbA1c levels and also in a study done by El Saadawy et al.,[2] a statistically significant negative correlation was found between HbA1c values and BMD variables including T-score values which was evaluated using dual-energy x-ray absorptiometry (DEXA) and edentulous mandibular quad BMD evaluated using CBCT.

The present study included three groups based on the duration of diabetes. A comparison of duration of diabetes with bone density inside the simulated implant and outside the simulated implant resulted in no significant difference between the groups.

There are no studies on the comparison of duration of DM with the bone density of mandible. According to few studies, the skeleton's bone density assessment by different methods and the duration of DM comparison revealed contradictory results. In a study by Jang et al.,[17] comparing the BMDs measured at various sites between the participants with DM duration of ≤5 years and those with a disease duration of >5 years was done and found a significant association between DM duration and reduced femoral neck BMD. In another study by Asokan et al.,[18] a negative association resulted between the duration of diabetes and BMD measured in the distal end of the radius using quantitative ultrasound.

In a study by Kenawy et al.,[10] the results showed a significant correlation between diabetes duration and the qualitative density measurements of maxilla measured using CBCT. The study results conducted by Wakasugi et al.[19] revealed a significant inverse correlation between bone density measured in lumbar vertebrae using DEXA and duration of diabetes. Unlike the above studies, there is no significant correlation between DM duration and bone density in our study except for a nonsignificant, very weak positive correlation.

The mandibular bone's quantity and quality reflect the bone's physiological condition due to systemic bone degeneration disorders, such as DM.[16] In the present study, the mean height measured from crest of alveolar ridge to mandibular canal at the implant site was greater in the control group than the study group with statistically significant difference; this is in accordance to the study done by Tadiparthi and Sujatha[20] where the mean value of residual alveolar bone resorption was significantly increased among diabetics than nondiabetics, and also in a study by Al-Jabrah O,[21] the amount of mandibular residual ridge resorption among T2DM subjects was higher than nondiabetic subjects.

In the present study, the mean mandible's width measured at the 1st molar region was slightly decreased in the diabetic group, but there was no statistically significant difference between them.

In the present study, other quantitative linear measurements such as the cancellous bone width, BC width, LC width, and IC width did not reveal a significant difference between diabetic patients and healthy controls.

In our study, there was no significant correlation between duration of diabetes and quantitative linear measurements of the mandible at edentulous first molar site, which is similar to a study by Kenawy et al.[10] in which no significant correlation was found between diabetes duration and quantitative linear measurements of maxilla measured using CBCT. The limitation of the present study is that since the sample size is small, we recommend further studies in a larger sample size.


  Conclusion Top


Since the introduction of CBCT in dentistry, there has been a magnanimous contribution in treatment planning related to implant prosthesis. Bone characteristics such as bone quantity and quality play an essential role in the prognosis of implant treatment. CBCT has been a reliable diagnostic aid in preimplant planning and helps the clinician assess the bone measurements and bone density, thus preventing implant failure. Although the bone density measurements are in pseudohounsfield units, it can give an assessment of bone density. With future developments, CBCT can evolve to become an accurate assessment tool for dentists.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Shankar MS, Pal B, Rai N, Patil DP. CBCT as an emerging gold standard for presurgical planning in implant restorations. J Indian Acad Oral Med Radiol 2013;25:66-70.  Back to cited text no. 3
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Alswat KA. Gender disparities in osteoporosis. J Clin Med Res 2017;9:382-7.  Back to cited text no. 8
    
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Kenawy SM, ElBeshlawy DM, Dahaba Mushira M. Quantitative and qualitative maxillary jaw bone assessment using cone beam computed tomography of a diabetic versus a nondiabetic sample of Egyptian population. Int J Adv Res 2017;5:2113-26.  Back to cited text no. 10
    
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Ay S, Gursoy UK, Erselcan T, Marakoglu I. Assessment of mandibular bone mineral density in patients with type 2 diabetes mellitus. Dentomaxillofac Radiol 2005;34:327-31.  Back to cited text no. 13
    
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Jolly SJ, Hegde C, Shetty NS. Assessment of maxillary and mandibular bone density in controlled type II diabetes: A Computed Tomography Study. J Oral Implantol 2015;41:400-5.  Back to cited text no. 14
    
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Sherwani SI, Khan HA, Ekhzaimy A, Masood A, Sakharkar MK. Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights 2016;11:95-104.  Back to cited text no. 15
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

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