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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/348472414 Evaluation of Alveolar Bone Quality: Correlation Between Histomorphometric Analysis and Lekholm and Zarb Classification Article in Journal of Craniofacial Surgery · January 2021 DOI: 10.1097/SCS.0000000000007405 CITATIONS 0 READS 42 6 authors, including: Some of the authors of this publication are also working on these related projects: My PhD course View project Comparison of histological, clinical and through imaging examinations evaluations of bone quality of maxillomandibular region for placing dental implants. View project Marina Reis Oliveira Araraquara Dental School, São Paulo State University (UNESP) 23 PUBLICATIONS 92 CITATIONS SEE PROFILE Cabrini Gabrielli São Paulo State University 142 PUBLICATIONS 953 CITATIONS SEE PROFILE Cleverton Roberto de Andrade São Paulo State University 70 PUBLICATIONS 745 CITATIONS SEE PROFILE Eduardo Hochuli-Vieira São Paulo State University 185 PUBLICATIONS 1,187 CITATIONS SEE PROFILE All content following this page was uploaded by Valfrido Antonio Pereira-Filho on 03 February 2021. 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Habal, MD. Unauthorized reproduction of this article is prohibited. CE: D.C.; SCS-20-01701; Total nos of Pages: 5; SCS-20-01701 Evaluation of Alveolar Bone Quality: Correlation Between Histomorphometric Analysis and Lekholm and Zarb Classification Marina Reis Oliveira, PhD,� Andréa Gonçalves, PhD,� Marisa Aparecida Cabrini Gabrielli, PhD,� Cleverton Roberto de Andrade, PhD,y Eduardo Hochuli Vieira, PhD,� and Valfrido Antonio Pereira-Filho, PhD� Objectives: This study evaluated the bone quality of the maxilla and mandible by using the classification proposed by Lekholm and Zarb (L & Z) and histomorphometry. Methods: Sixty edentulous areas were evaluated. The classification by L & Z was obtained through the evaluation of periapical and panoramic radiographs associated with the surgeon’s tactile perception during milling and implant installation. Before implant installation, bone biopsies of standardized sizes were performed for histological evaluation. Results: Type III bone quality was more frequent in the posterior (73.33%) andanterior (73.33%) maxilla, whereas type II bone quality was more frequent in the posterior (53.33%) and anterior (60.00%) mandible. Through histometry, statistical difference was observed for the amount of bone tissue of the posterior region of the maxilla in relation to the anterior and posterior regions of the mandible (P � 0.043). However, there was no difference in osteocyte counts between alveolar regions (P¼ 0.2946). In the female gender, the age showed a low positive correlation with the L & Z classification (rho¼ 0.398; P¼ 0.006) and in the male gender, a moderate negative correlation was observed (rho¼ – 0.650, P¼ 0.016). Conclusions: Both methods detected differences in the bone quality of the alveolar regions of the maxilla/mandible and that the classification by L & Z is a reliable method, since it was consistent with histomorphometry, considered the ‘‘gold standard’’ method for the evaluation of bone quality and greater bone density was observed in older men. Key Words: Bone quality, classification by Lekholm and Zarb, dental implants, histomorphometry (J Craniofac Surg 2021;00: 00–00) T here are currently several methods for evaluating bone quality.However, computed tomography (CT) is the image examination considered more adequate for such purpose, since it associates information of quantity and morphology.1–2 Despite this, it is not a resource applied in all cases of clinical practice.3 Leckholm and Zarb (L & Z) classification is still the most used method to evaluate bone quality because it has low cost and is easy to apply.4–7 In this classification, the volume and structural characteristics of the bone tissue are evaluated based on panoramic/periapical radio- graphs and surgical evaluation of the bone hardness perceived by the surgeon during the perforation to install the implant. The bone is then classified based on a scale ranging from 1 to 4 according to the amount of trabecular and cortical bone. Regarding the amount of bone available, the classification varies from A to E, where: A corresponds to most of the preserved alveolar bone and E indicates that the basal bone is already extremely reabsorbed.8 The main limitation of this classification is that it can be influenced by the surgeon’s experience, resulting in a somewhat subjective bone characterization and difficult reproducibility.1–9 However, it has been verified that tactile perception allows an acceptable classifi- cation of bone types.10 The histomorphometry, in turn, includes small bone biopsies for histological evaluation and quantification of the percentage of trabeculae in the total area of the bone fragment, and remains the gold standard method for the assessment of bone quality.7 However, it is not a viable resource in clinical practice. In this context, although there is a great diversity of methods available for preoperative assessment of bone quality, only a few are routinely used.11 In addition, many factors of bone quality and their relation to dental implants are misunderstood.12 This is because, with the exception of a few studies,6–7 most of the studies to date have evaluated the initial stability of the implant using bone histomor- phometry in cadavers, which hinders the extrapolation of results for in vivo clinical practice. Therefore, it is important to perform in vivo studies to understand the clinical situation, in which several biological factors are interfering with the primary stability of implants.13 In addition, Oliveira et al (2008)12 observed in their study that different bone qualities can be found in different regions of the maxilla and mandible. Therefore, site-specific assessment is impor- tant and careful planning for rehabilitation with implants is always necessary. In this context, studies like our study are necessary to compare the bone quality assessed by the classic classification of L & Z and histomorphometry, which is still considered the gold standard method for the evaluation of bone quality. From the �Diagnosis and Surgery Department, Araraquara Dental School, São Paulo State University (FOAr/UNESP); and yPathology and Physi- ology Department, Araraquara Dental School, São Paulo State Univer- sity (FOAr/UNESP), Araraquara, SP, Brazil. Received August 5, 2020. Accepted for publication November 18, 2020. Address correspondence and reprint requests to Marina Reis Oliveira, PhD, Rua Humaitá, 1680, Centro, Araraquara, 14903-385, SP, Brazil; E-mail: marinareis89@hotmail.com Funding was provided by the FAPESP (Foundation for Research Support of the State of São Paulo) (Process number: 2014/25253-1). The authors report no conflicts of interest. Supplemental digital contents are available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.jcraniofa- cialsurgery.com). Copyright # 2020 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000007405 CLINICAL STUDY The Journal of Craniofacial Surgery � Volume 00, Number 00, Month 2021 1 mailto:marinareis89@hotmail.com http://www.jcraniofacialsurgery.com/ http://www.jcraniofacialsurgery.com/ http://dx.doi.org/10.1097/SCS.0000000000007405 Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited. CE: D.C.; SCS-20-01701; Total nos of Pages: 5; SCS-20-01701 MATERIALS AND METHODS Patient Selection and Sample Division Thirty-six healthy patients of both genders were selected, accounting for 60 alveolar regions that met the following inclusion criteria: age between 20 and 75 years; patients with no serious diseases or decompensations that could change bone density; edentulous areas of maxilla and/or mandible, in which it was possible to install an implant with a minimum of 3.75 mm in diameter � 9 mm in length (External Hexagon - HE, Titamax TI, Neodent, Curitiba, PR, Brazil); and degree of atrophy B and C.8 Before any study procedure was initiated, the selected patients signed the informed consent form. In addition, this study was only initiated after approval by the Ethics Committee on Human Research (Process number: 917.255/2014). The 60 edentulous areas evaluated were divided into 4 groups of 15 areas each, according to the site in the maxilla: posterior maxilla, posterior mandible, anterior maxilla, and anterior mandible. Preoperative Evaluation All patients were submitted to anamnesis and were clinically assessed for residual bone quantity. Scanned panoramic and peri- apical radiographs were obtained using VistaScanCombi Plus soft- ware (Durr Dental AG, Bietigheim-Bissingen, Germany). In addition, the panoramic and periapical radiographic examinations were performed in a standardized way and always by the same person. With the information obtained, we planned the surgical procedure and determined the length of the implants. Bone Classification by L & Z This classification was performed before the surgery by a single examiner, who was also the surgeon responsible for conducting the surgeries. Thus, it was possible to determine the classification of bone quality of the edentulous areas based on the radiographic aspect and surgeon’s tactile perception to the bone resistance during the perfo- ration, as proposed in the original L & Z classification. The intraob- server calibration was performed and the Kappa index obtained was 0.87 (almost a perfect match according to Landis and Koch, 197714). Thus, after the visual evaluation of these radiographs, the evaluator classified the different areas according to L & Z as follows: bone type 1, bone type 2, bone type 3, and bone type 4. Surgical Procedure The technique to prepare the sites for the installation of the implants was employed in a standard way and taking into account the manufacturer’s recommendations. The same experienced sur- geon performed all surgeries, in order to reduce the chances of errors among operators. Surgical access was performed by a linear incision on the ridge with subsequent complete displacementof the flap to expose the bone tissue. Before starting the perforation, a bone biopsy was performed with a trephine of 2.5 mm outside diameter (Maximus, Contagem, MG, Brazil) at 30 rpm. The tre- phine was always inserted until the same height (8 mm) (Fig. 1). Shortly after its removal, the bone fragment was washed with sterile saline and fixed in 4% buffered formaldehyde. The trephine served as the initial mill for the preparation of the surgical alveolus. At the time of perforation to install the implants the surgeon was asked about the bone quality as proposed by L & Z. Histological Processing The bone fragments obtained were were submitted to routine histological processing. Serial cuts were made in the axial direction of the specimen with 6-mm thickness using a microtome (Micron, model HM 325). The sections were stained with hematoxylin and eosin and submitted to histometry and osteocyte count. Histomorphometric Analysis For the histomorphometric analysis, 3 histological slides from each biopsied area were selected by the stereometry (cervical, middle, and apical third of the bone fragment). Quantification of the bone tissue was performed by an experienced examiner, without knowledge of the alveolar region, in each group. Quantitative analysis was performed over the entire length extension of the 3 histological sections selected. The final value of bone tissue in mm and the osteocyte count resulted from the sum of the values obtained in the 3 histological sections evaluated. Optical Microscope (Dia- star – Leica Reichert Jung Products Germany) was used with 4.0/ 100X magnification lens and 5X and 10X magnification eyepieces for histometry and osteocyte count, respectively. Figures 2 and 3 show histological images of the different alveolar regions with 5- and 10-fold increase of the maxilla and mandible, respectively. The images were selected and transferred to a PC (Pentium 4 Intel) through a camera (Olimpus CAMEDIA C50/60 Wide Zoom) FIGURE 1. (A) Trephine with 2.5 mm diameter positioned for bone biopsy; (B) Bone fragment removed. FIGURE 2. Histological image of bone biopsy of the anterior region of the maxilla [(A) 5-fold increase for histometry, (B) 10-fold increase for osteocyte count]; histological image of bone biopsy of the posterior region of the maxilla [(C) 5-fold increase for histometry, (D) 10-fold increase for osteocyte count]. Oliveira et al The Journal of Craniofacial Surgery � Volume 00, Number 00, Month 2021 2 # 2021 Mutaz B. Habal, MD Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited. CE: D.C.; SCS-20-01701; Total nos of Pages: 5; SCS-20-01701 coupled to the optical microscope. With the aid of Image J Launcher software (National Institutes of Health, Bethesda, Maryland, USA (http://rsb.info.nih.gov/ij/index.htm), the total area was delimited and quantified as 100%. Subsequently, other structures, such as empty spaces, cells, and blood vessels, were subtracted from the narrowly defined bone areas. The final bone quantity of each edentulous region was obtained by calculating the sum of the bone area of the 3 quantified slides. Then, osteocyte count was carried out on the selected slides throughout their length. The count was done in duplicate for each slide and the arithmetic mean of the 2 counts was calculated. Statistical Analysis The data underwent the Shapiro–Wilk test to evaluate normality. When normality assumptions were met, analysis of variance was used, followed by Tukey post-test; when the data did not respond to normality, the Kruskal–Wallis nonparametric test was employed, followed by the Dunn post-test to test the existence of differences in the radiographic optical bone density between the alveolar regions of maxilla and mandible. In addition, a correlation analysis was performed through the Spearman correlation coefficient. The mag- nitude of the correlations obtained in the present study was based on Munro’s (2001)15 classification: low correlation (0.26 � rho � 0.49); moderate correlation (0.50 � rho � 0.69); high correlation (0.70� rho� 0.89); and very high correlation (0.90� rho� 1.00). The level of significance adopted in all statistical tests was 5% of significance. All statistical tests were calculated using SPSS soft- ware (v.21, SPSS Inc., Chicago, IL). RESULTS Classification by L & Z The final bone quality obtained by the radiological evaluation and surgeon’s tactile perception as proposed in the original L & Z classification is presented in Supplementary Digital Content, Table 1, http://links.lww.com/SCS/C276. It was observed that the most frequent bone quality in the posterior region of the maxilla was the type III (73.33%), and type II (13.33%) and IV (13.33%) bone qualities were observed in only 2 cases each. Type I bone quality was not observed in the posterior maxillary region. On the other hand, in the posterior mandibular region the most common bone quality was type II (53.33%), followed by type III (26.67%), and type I was observed in 2 cases (13.33%). Type IV bone quality was observed in only 1 case in the posterior region of the mandible (6.67%). In the anterior maxillary region, the most frequent bone quality was type III (73.33%), followed by type II bone quality (20.00%), and type IV was observed in 1 case only (6.67%). On the other hand, in the anterior area of the mandible only the type I and II bone qualities were observed, with higher frequency for type II (60.00%) when compared to type I (40.00%). Histometry and Osteocyte Count The mean values of bone tissue (mm) evaluated by histometry for each of the regions were as follows: 2243110.76 (�1450895.64) for the posterior region of the maxilla, 3992425.76 (�2018654.67) for the posterior region of the mandible, 2660685.75 (�110304.20) for the anterior region of the maxilla and 3745390.01 (�1346277.67) for the anterior region of the mandible. After submitting the data to the analysis of variance test a statistical difference was observed among the groups (P¼ 0.0062) (Supple- mentary Digital Content, Table 2, http://links.lww.com/SCS/C278). Tukey post-test showed that the mean bone tissue (mm) of the posterior maxilla is statistically different from that of the posterior (P¼ 0.013) and anterior mandible (P¼ 0.043). In contrast, no statistically significant differences were observed between the anterior and posterior maxillary area (P¼ 0.875) and the anterior and posterior mandibular area (P¼ 0.970). Similarly, no statisti- cally significant differences were observed between the anterior mandibular region and the anterior maxillary region (P¼ 0.217) (Fig. 4). In turn, the mean osteocyte count for each of the analyzed regions was as follows: 542.73 (�482.81) for the posterior region of the maxilla, 778.60 (�422.98) for the posterior region of the mandible, 616.36 (�444.12) for the anterior region of the maxilla, and 678 (�392.71) for the anterior region of the mandible. Since the osteocyte count values did not respond to normality, it was neces- sary to use nonparametric statistics. After the Kruskal–Wallis test, the data revealed no statistical difference among the groups (H(3)¼ 3.7098; P¼ 0.2946). Correlation Analysis As for the correlation analysis taking into account gender, in the female gender, the age variable showed a low positive correlation with the L & Z classification (rho¼ 0.398) with high statistical FIGURE 3. Histological image of bone biopsy of the anterior region of the mandible [(A) 5-fold increase for histometry, (B) 10-fold increase for osteocyte count], histological image of bone biopsy of the posterior region of the mandible [(C) 5-fold increase for histometry, (D) 10-fold increase for osteocyte count]. FIGURE 4. Mean and standard deviation of the variable bone tissue according to the alveolar region. Different letters indicate statistically different means according to the Tukey test (P � 0.043). The Journal of Craniofacial Surgery � Volume 00, Number 00, Month 2021 Bone Quality in the Maxillaand Mandible # 2021 Mutaz B. Habal, MD 3 http://rsb.info.nih.gov/ij/index.htm http://links.lww.com/SCS/C276 http://links.lww.com/SCS/C278 Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited. CE: D.C.; SCS-20-01701; Total nos of Pages: 5; SCS-20-01701 significance (P¼ 0.006). This means that the older the patient, the higher the L & Z classification score, and the more medullary the bone. On the other hand, regarding the histomorphometric (rho¼ – 0.254, P¼ 0.0085) and osteocytes count (rho¼ –0.278, P¼ 0.058), no statistically significant correlations were observed for the women’s age in the present study sample. In the male gender, a moderate negative correlation was observed (rho¼ –0.650, P¼ 0.016) in the analysis of the correla- tion between age and the L & Z classification, which means the older the patient, the lower the bone quality score and the more cortical the bone. However, regarding the histomorphometric (rho¼ –0.02, P¼ 0.949) and osteocytes count (rho¼ –0.308, P¼ 0.306), no statistically significant correlations were observed for the men’s age in the present study sample. DISCUSSION According to Oliveira et al (2008),12 alveolar bone quality can be extremely variable in any of the maxilla and mandible regions. Therefore, preoperative planning is extremely important in order to achieve higher success rates in the long term.16 Much has been discussed regarding the use of CT for implant planning, since this is considered the gold standard imaging exam for the evaluation of bone quality.4,5 However, because of the cost and dose of radiation received by the patient, most professionals still use conventional radiographs, especially panoramic radiography, and other subjec- tive methods for the assessment of bone quality, such as the L & Z classification.17,18 In addition, the literature lacks studies on such matter, such as our study, in which the bone quality of the different regions of the maxilla and mandible is evaluated by using the classical L & Z classification and histomorphometry, which is still considered the gold standard method for evaluation of bone quality. Besides the maxillomandibular location, others factors can interfering in the bone quality, such as: use of drugs, systemic diseases, gender, and age.5 So much so, that the results obtained show in the male gender, a moderate negative correlation was observed (rho¼ –0.650, P¼ 0.016) in the analysis of the correla- tion between age and the L & Z classification and a low positive correlation between the female gender and the L & Z classification (rho¼ 0.398; P¼ 0.006). This means that the older women, the higher the L & Z classification score and the more medullary the bone and in the men, which means the older the patient, the lower the bone quality score and the more cortical the bone. However, in the both genders there was no correlation of the age with histologi- cal analysis (P> or¼ 0.058). The most traditional method for evaluation of bone quality is the classification proposed by L & Z, in 1985,8 performed by using radiographs associated with the surgeon’s tactile perception. In a study by Lindh et al (2014),19 in which the knowledge on bone quality of Swiss and Brazilian implant specialists was evaluated, both groups attested to frequently use the aforementioned classifi- cation. Despite the wide use, this method is subjective and difficult to reproduce and therefore little investigated scientifically.1–9 Because of this, the evaluations in present study has been done by a single evaluator. Therefore, the intraobserver calibration was performed to evaluate the bone quality according to L & Z classification based on the panoramic radiographs in order to reduce the bias to the maximum. The analysis only started after calculating kappa, which was 0.87, that is, excellent.14 According to Linck et al (2016),20 the lack of scientific evidence on the use of the L & Z classification is due to the variety of ways the method is used. Although some authors classify bone tissue based on radiographic evaluation only, others associate the sur- geon’s tactile perception. However, the 2 classifications (original and modified) are strongly correlated and the surgeon’s tactile perception does not seem to have much interference with bone classification.18 Nevertheless, in this study, the original L & Z classification was used, considering the radiographic evaluation and the surgeon’s tactile perception. This is because tactile intraoper- ative perception can add important information about the charac- teristics of bone tissue.19 In addition, the original L & Z classification has been shown to be more correlated with the micro-CT than the L & Z classification based only on radiographic images.7 In addition, in 1999, Trisi and Rao10 verified that tactile perception allows an acceptable differentiation of the type of bone quality. In this study, the highest bone quality in the posterior (73.33%) and anterior (73.33%) areas of the maxilla was type III and in the posterior (53.33%) and anterior areas (60.00%) of the mandible the type II bone quality was the most observed. Linck et al (2016)20 also reported that most of the implant insertion areas were of type II or III. Another study evaluating bone quality and quantity only in the anterior maxillary region showed that type III bone quality was the most frequent in this region (69.7%).21 Similarly, Ribeiro-Rotta et al (2014)7 also found higher prevalence of type II and III bone quality (58.7%) according to the L & Z classification. However, different bone qualities can be found in the anterior and posterior regions of the maxilla and mandible, so individualized evaluation is always very important.12 A pioneering study for the validation of L & Z classification was done by Ribeiro-Rotta et al (2014),7 comparing the initial stability of the implant, L & Z classification and bone biopsies evaluated by micro-CT. However, the authors emphasized the importance of other comparative studies of this classification, since it is widely used. The comparison with bone histomorphometry is very impor- tant, because although it is not feasible in all in vivo procedures, it is still the gold standard for the evaluation of bone quality,7 since it cannot be completely replaced with micro-CT.22,23 Regarding the histomorphometric analysis, bone fragments were removed with the use of a trephine before implant installation. However, although the bone biopsies were always obtained with the same trephine, tailor made for this study, the length of bone fragments was not always the same. It is believed that this occurred due to the differences in bone microarchitecture of the different alveolar regions of the maxilla and mandible, as previously empha- sized by authors who used similar methodology.7 In order to avoid compromising the histological analysis, each specimen was evalu- ated in 3 regions (cervical, middle, and apical), so that the entire extension (cortical and medullary bone) could be evaluated. Although it is not an applicable feature in the routine clinic, histometry is considered the gold standard to assess bone qual- ity.24,25 Trisi and Rao (1999)10 found a positive correlation between the clinical and histomorphometric evaluation of bone quality after implant insertion in 56 patients, mainly in the differentiation of bone types I and IV. In the identification between intermediate bone types (II and III), nonsignificant correlation was observed. In contrast, in this study it was possible to detect statistical differences regarding the histometry between the posterior regions of the maxilla and the anterior (P¼ 0.043) and posterior (P¼ 0.013) regions of the mandible. These results suggest that it was possible to detect differences in bone quality through histometry not only in the extreme bone qualities but also in the intermediate ones. This is because, in the posterior maxillary region, the most frequent bone quality was type III (73.33%) althoughtype IV was also observed (13.33%), and in the anterior mandibular region, bone types II (60.00%) and I (40.00%) were observed. However, no significant statistical differences were observed in the histometry of the anterior and posterior regions of the maxilla and mandible. It is believed that this may have occurred because most of the bone quality of the anterior and posterior maxillary area consists of type Oliveira et al The Journal of Craniofacial Surgery � Volume 00, Number 00, Month 2021 4 # 2021 Mutaz B. Habal, MD Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited. CE: D.C.; SCS-20-01701; Total nos of Pages: 5; SCS-20-01701 III bone. On the other hand, the bone quality most observed in the anterior mandibular region was type II and it was the type III for the posterior mandibular, followed by type II. Thus, it can be suggested that in the sample studied between the posterior and anterior regions of the same maxilla there is similarity in bone quality. Regarding the osteocyte count, no statistical differences were observed between the different regions evaluated (P¼ 02946). Hernández-Cortés et al (2014)24 also used osteocyte count as an indicator to assess bone quality. However, the authors did not find statistically significant differences in the amount of osteocytes in the femoral head with osteoporosis and osteoarthritis. Thus, as in this study, the authors concluded that osteocyte count is not a good indicator to assess bone quality. Thus, the methodology used allowed to conclude that both methods allowed to detect differences in the bone quality of the alveolar regions of the maxilla/mandible and that the classification by L & Z is a reliable method to evaluate bone quality, since it was consistent with histomorphometry, considered the gold standard method for the evaluation of bone quality. ACKNOWLEDGMENTS The authors thank CAPES (Coordination for the Improvement of Higher Education Personnel) and FAPESP (Foundation for Research Support of the State of São Paulo) (Process number: 2014/25253-1). REFERENCES 1. Turkyilmaz I, Tumer C, Ozbek EN, et al. 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Comparison insight bone measurements by histomorphometry and mCT. J Bone Miner Res 2005;20:1177–1784 24. Hernández-Cortés P, Monje A, Galindo-Moreno P, et al. An ex vivo model in human femoral heads for histopathological study and resonance frequence analysis of dental implant primary stability. Biomed Res Int 2014;2014:1–8 25. Oh JS, Kim SG. Clinical study of the relationship between implant stability measurements using Periotest and Osstell mentor and bone quality assessment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2012;113:35–40 The Journal of Craniofacial Surgery � Volume 00, Number 00, Month 2021 Bone Quality in the Maxilla and Mandible # 2021 Mutaz B. Habal, MD 5 View publication statsView publication stats https://www.researchgate.net/publication/348472414
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