Abstract: Purpose: The aim of this retrospective pilot study was to use digital implant planning to assess radiographic outcomes of maxillary sinus augmentation bone grafting procedures (ideal, excess, or insufficient) in reference to the planned implant. Materials and Methods: After ethical approval was received, deidentified data for subjects treated for a maxillary sinus elevation procedure was extracted. Patient-specific variables (age group, gender, race, smoking, diabetes, and cardiovascular disease) and site-specific variables (type of bone graft, type of membrane, membrane perforation, and other complications) were collected, as recorded in the electronic health records. For the records that satisfied the inclusion criteria, preoperative and postoperative cone-beam computed tomography scans for lateral sinus augmentation procedures were retrieved, superimposed, and imported into the implant planning software. An ideal implant was planned digitally in a cross-sectional view by an expert in prosthodontics (KV). The implant measurements in apicocoronal (AC) and buccopalatal (BP) dimensions were kept standard for all cases and were confirmed by two previously calibrated co-investigators (GS, ID). Statistical analysis involved descriptive and bivariate analysis. Results: A total of 350 electronic health records were reviewed and 26 were included. Descriptive analysis revealed that in the AC dimension, 40.63% of procedures resulted in insufficient amount of bone graft and 37.50% of procedures resulted in excess bone graft; 21.88% of procedures had ideal amount of bone graft in the AC dimension. For the BP dimension, 81.25% of procedures resulted in ideal and 18.75% in insufficient amounts of bone graft. Conclusion: This study revealed that a limited number of maxillary sinus procedures resulted in ideal bone grafting in both the AC and BP dimensions when considering predetermined restorative guidelines for the final implant position. An excess and/or insufficient amount of bone grafting in at least one dimension resulted most of the times. With the use of technology and an interdisciplinary team of experts, future studies should aim to quantify the amount of bone graft needed for an ideal maxillary sinus elevation for upcoming implant placement.
Since the introduction of root form dental implants by Brånemark in 1971, oral rehabilitation using implants has become a common procedure for restoring partially or completely edentulous areas.1 Dental implants are considered the standard of care in cases of single-tooth replacement where adjacent teeth do not require restorations.2
In the posterior maxilla, insufficient bone is frequently encountered. Compromised alveolar bone height and width following extraction along with pneumatization of the maxillary sinus can hinder ideal implant placement.3 Also, less-dense bone quality is typically encountered in the maxillary posterior region.4-6 In cases of reduced ridge height, sinus elevation procedures using a lateral window or transcrestal approach often can enable the placement of
standard-length implants.7-10 What constitutes a “standard-length implant” has changed over the years in the literature, as different lengths have been suggested to define a “short” implant: ≤10 mm,11-13 ≤8 mm,14 or ≤6 mm.15-17
Maxillary sinus floor elevation using a lateral window is a well-documented and reliable technique to increase bone height in the posterior maxilla.8 Radiographic examination is critical for initial diagnosis of an edentulous area that is planned to be reconstructed with implant-supported restorations. Two-dimensional periapical and panoramic radiographs or 3-dimensional cone-beam computer tomography (CBCT) scans are routinely taken. After the bone grafting procedure, the presence of a “dome” on the sinus floor in a post-surgical radiograph generally means there is an adequate amount of graft material.18 A drawback of this method of judging the sufficiency of the graft is that there could actually be either an excess or inadequate amount of graft material present. If inadequate, additional surgical interventions and/or changes in the dimensions of the initially planned implant might be needed when placing the implant. Furthermore, the decision-making process with this technique is based on the operator’s clinical expertise and judgment. Past studies have explored the volumetric changes of bone graft material in sinus augmentation procedures.19,20 Others have analyzed intraoperative and postoperative complications.21
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Variability exists in the literature regarding healing time (4 to 10 months) for the bone graft after maxillary sinus elevation.22-24 Also, limited evidence is available on how to objectively ascertain the “ideal” amount of bone graft required in a lateral window sinus augmentation procedure for future implant placement. Implant survival rates for the lateral window technique approach are very high, reaching up to 98% after 3 years of functional loading.25,26 Sinus elevation procedures using a lateral approach may increase the ridge height by up to 14 mm,25 which will aid in enabling the placement of standard-length implants.8
Complications often accompany external sinus elevation procedures, including membrane perforation, sinusitis, and partial or complete graft failure,27,28 and, thus, increased costs, additional surgical time, and advanced surgical skills may be required. To avoid these issues, the use of shorter implants has been suggested in situations where there is residual ridge height of 4 mm to 9 mm.28-30 This affords the clinician and patient shorter overall treatment time, reduced cost, and fewer surgical procedures. In cases of a severely atrophic maxilla (<3 mm residual height), however, the use of short implants may be impracticable given a minimal level of evidence.31-34
The aim of this retrospective study was to use digital implant planning to assess radiographic outcomes of maxillary sinus augmentation bone grafting procedures (ideal, excess, or insufficient) via a lateral window in reference to the future implant.
Materials and Methods
The study was designed as a single-center retrospective cohort longitudinal study. It was approved by Tufts University Health Sciences Institutional Review Board (IRB No. 13145). All data was extracted from electronic health records (EHRs) of subjects treated for a maxillary sinus elevation procedure with lateral window technique at Tufts University School of Dental Medicine (TUSDM) postgraduate clinics. Inclusion criteria: subjects were treated in the TUSDM postgraduate clinical areas (between October 1, 2007, and September 30, 2018); they had a clinical (axiUm notes) and radiographic diagnosis of a severely atrophic posterior maxillary ridge (≤3 mm) that was planned for dental implant treatment; they were treated with maxillary sinus augmentation procedures with bone grafts (lateral window approach only); and pre- and postoperative (5 to 6 months after sinus augmentation) CBCTs were available in the EHR. Exclusion criteria: subjects were treated in the Faculty Practice Clinic; their records did not match the selected time window; they were treated with internal/crestal sinus elevation techniques and maxillary sinus elevation with lateral window approach and simultaneous implant placement.
Image Analysis
Upon retrieval of pre- and postoperative CBCTs, the files were imported into a digital planning software (coDiagnostiX®, Dental Wings, codiagnostix.com). Using multiplanar reconstructions, the pre- and postoperative CBCTs were oriented using the axial, sagittal, and coronal views that reflected similar orientation in each case (Figure 1).
The anatomical landmarks used for orientation of the CBCT data were as follows:
Mid-sagittal view: The mid-sagittal plane was identified using the plane where the anterior nasal spine and posterior nasal spine points (from cephalometric analysis) were aligned.
Panoramic view: The occlusal curve, or panoramic curve, was defined at the middle (buccolingually) of the maxillary alveolar ridge.
Occlusal view: Alignment of the CBCTs in the mid-sagittal and mid-axial views established that the scans were aligned in the occlusal view as well.
Digital Implant Planning and AC/BP Measurements
Once the anatomical landmarks on pre- and postoperative CBCTs were coordinated, the postoperative CT scan was superimposed on the preoperative CT scan, and a digital wax-up of the restored tooth (or teeth) was designed. All implant cases were discussed among the surgical and restorative faculty and residents prior to surgery. For calibration purposes, a 10-mm long dental implant was considered acceptable prior to lateral window sinus augmentation procedures. In compliance with this protocol, a 10-mm long by 4.1-mm diameter implant (Bone Level RC, Straumann, straumann.com) was used as a standard for planning purposes for all cases in this pilot study. With the original intent to treat established, an experienced prosthodontist used the digital planning software to perform a digital plan of a prosthetically driven implant placement in a cross-sectional view. The amount of bone graft surrounding the planned implant post–sinus augmentation procedure was quantified (in millimeters) in the apicocoronal (AC) and buccopalatal (BP) dimensions using measurement tools of the same software (Figure 1). The implant measurements were standardized for all cases and were performed by one of the co-investigators (GS) after a prior calibration and confirmed by another investigator (ID). The results were categorized into three possible scenarios, based on the height and width of the sinus augmentation performed (Figure 2):
Ideal bone graft: 2 mm to 4 mm of residual bone in the AC and BP dimensions, or membrane elevated up to the medial/palatal wall in the BP dimension.
Insufficient bone graft: less than 2 mm of residual bone in the AC or BP dimensions.
Excess bone graft: more than 4 mm of residual bone in the AC dimension.
In addition to the CBCTs, independent variables also collected from the records included patient demographics (age, gender, race/ethnicity) and medical history (current smoker/former smoker/nonsmoker; diabetes – yes/no; cardiovascular disease – yes/no). Site-specific variables included: type of bone graft (allograft, alloplast, autogenous, xenograft) and number of vials; type of membrane (resorbable, nonresorbable, or no membrane used); Schneiderian membrane perforation (yes/no); and other complications (anatomical, procedural, pathology).
Statistical Analysis
A sample size calculation was not performed because this was a pilot study. Descriptive statistics (frequencies and percentages for categorical variables; means and standard deviations for continuous variables) were calculated. The proportion of sites with insufficient, ideal, and excess bone graft in the AC dimension and insufficient and ideal bone graft in the BP dimension was assessed. Statistical significance among the bone graft categories for each independent variable was assessed using the chi-square test. The Fisher’s exact test was used if the expected cell frequency was less than 1 or if more than 20% of cells had an expected frequency less than 5. Statistical significance was set at 0.05 for overall tests and 0.017 for pairwise comparisons. SAS Version 9.4 statistical software (SAS Institute Inc.) was used for analyses.
A Bonferroni correction was used to adjust the type I error to account for multiple comparisons between groups. The Bonferroni correction set the significance cutoff for pairwise comparisons at 0.017 (ie, 0.05/3).
Results
A total of 350 electronic health records were reviewed in this study, and 26 were included. Out of the 26 records, 32 treatment sites were included in the study, as some patients received bilateral maxillary sinus lift procedures. Sites were considered independent with respect to the outcome. The age range of patients in the study was 39 to 78 years with the mean age of the study sample being 64.13 ± 9.95 (standard deviation [SD]). Nineteen subjects were male and seven were female.
Results reporting patient-specific variables, such as smoking, diabetes, and cardiovascular disease, are presented in Table 1. Site-specific variables, which included type of bone graft (allograft, xenograft, allograft mixed with xenograft, and autograft), type of membrane (resorbable, nonresorbable, or none), and presence of membrane perforation (yes/no), are reported in Table 2. From the total sites assessed, in four of them (12.5%) the bone graft augmentation was completed in a different location (ie, extremely mesial or distal) than the ideal prosthodontic planning. These sites were excluded from the study since no implant planning at the site could be performed.
Primary Outcome Measured in AC and BP Dimensions
Results from descriptive statistics of the 32 sites revealed that in the AC dimension, seven (21.88%) sites had an ideal amount of bone graft, 13 (40.63%) sites presented with an insufficient amount of bone graft, and 12 (37.50%) sites had excess bone graft. In the BP dimension, 26 (81.25%) sites resulted in an ideal amount of bone graft, and six (18.75%) sites had an insufficient amount of bone graft. The relationships between primary outcome and patient- and site-specific variables are presented in Figure 3 and Figure 4.
Patient-Specific Variables
The Fisher’s exact test showed no statistically significant association between gender (P = .7762), smoking (P = .7820), diabetes (P = .4181), and the amount of bone graft in the AC dimension. However, there was a statistically significant association between cardiovascular disease and the amount of bone graft in the AC dimension (P = .0127). Pairwise analysis further showed that this association was significant when the amount of bone graft was insufficient (16.67%) or ideal (83.33%) (P = .00072). There was no statistically significant association between any of the patient-specific variables and the amount of bone graft in the BP dimension (Figure 3).
Site-Specific Variables
Ideal results measured in AC dimensions were achieved with allograft mixed with xenograft at five (29.41%) out of 17 sites and with allograft in two (18.18%) out of 11 sites. When analyzed in the BP dimension, most cases—26 (81.25%) out of 32 sites—were ideal independent of the type of bone graft used. The use of resorbable membrane was associated with an ideal amount of bone graft at five (15.63%) sites in the AC dimension and at 24 (75%) sites in the BP dimension.
Only five Schneiderian membrane perforations (15.63%) were reported, and from those, the final bone graft result measured in the AC dimension was insufficient at three (60%) of the sites and ideal at two (40%) of the sites. Similar results were seen in the BP dimension. Results from bivariate analysis revealed that there was no statistically significant association between the type of bone graft, type of membrane, and presence of membrane perforation and the amount of bone graft in the AC and BP dimensions (Figure 4).
Discussion
This retrospective cohort pilot study demonstrated that the amount of bone grafted for the majority of maxillary sinus procedures was either insufficient or in excess when evaluated in a 3-dimensional perspective. Of the 32 sites reviewed in the current study, only seven (21.88%) had an ideal amount of bone graft in the AC dimension.
For an extensive procedure such as a maxillary lateral sinus augmentation, clinicians generally comprehend the value of bone graft material surrounding the implant body and apex to facilitate osseointegration. The radiographic outcomes (ideal, excess, or insufficient bone graft) of this study were reported by utilizing digital implant planning and 3-dimensional prosthetically driven implant placement for maxillary sinus augmentation procedures. The three categories (ideal, excess, or insufficient) were classified based on studies that have demonstrated a decrease of 10% to 15% in the height of grafted material over time and the selected implant length (10 mm).22,24 Hence, the AC dimension used a measurement range of 2 mm to 4 mm from the apex of the implant to the top of the graft to define the ideal amount of bone graft. Measurements less than 2 mm or greater than 4 mm were used to define, respectively, an insufficient or excess amount of bone graft. For the BP dimension, only insufficient or ideal (sinus membrane elevated up to the medial wall) results were documented. For some cases that were classified as having insufficient bone graft, use of a shorter implant may be an alternative to achieve the original treatment intent of avoiding additional surgical procedures. For cases that were classified as having excess bone graft, implants longer than 10 mm may be planned. For the purposes of this pilot study and to quantify the results based on initial intent to treat, 10-mm long implants were planned in all augmented sites.
The present study also included edentulous sites where all posterior teeth were missing. For those situations specifically, the use of a guide for the maxillary sinus lateral window is critical to ensure that the grafted location is aligned with the prosthetically driven implant planning location. This would reduce the instances where the bone graft is placed in an unfavorable location prosthetically, which was the case for four of the subjects in this study. For single-tooth edentulism areas, clinicians may consider using the adjacent teeth and their roots to guide the location of the lateral window. Although options exist to correct implant angulation via angulated abutments, ideal planning for screw-retained restorations should be considered. This is especially true if the interdisciplinary team collaboratively planned the therapy at the outset. This collaboration not only can facilitate the treatment planning process and surgical management, but also ensure a favorable long-term prognosis of the implant-supported restoration.35,36
Interdisciplinary collaborative care models in academic dental institutions and private practice settings are in the early stages of development.37,38 This might explain why the results from this study demonstrated that in most cases a non-optimal amount of bone graft was used. One should take into consideration that the sinus elevation procedures included in this study were from different postgraduate clinical programs (ie, prosthodontics, periodontology, implant dentistry, and oromaxillofacial surgery). Although these programs are all part of the same institution, protocols for maxillary sinus elevation using the lateral window may vary between disciplines.
As dentistry moves toward interdisciplinary and interprofessional care models, it is relevant to further discuss the patient-specific variables included in this retrospective study. Current data reports statistically significant association between the presence of cardiovascular disease and the amount of bone graft in the AC dimension (P = .0127).39 Smoking has been associated with poor wound healing, however the present study’s findings demonstrated that current smokers had an ideal or excessive amount of bone graft in the AC dimension (Figure 3).
The significance of this study is that the results support collaboration between the disciplines treating the patient and the use of technological advancements, specifically CBCT and digital implant planning, to facilitate an ideal maxillary sinus elevation procedure, which can reduce cost, chairtime, and the risk of complications. For academic institutions, it is key to educate the next generation of students and residents using the latest technologies in an interdisciplinary and interprofessional collaborative healthcare model, focusing on a patient-centered approach.39-41 In addition, the data from this study allows for an appropriate sample size calculation for a future study with a higher level of evidence, such as a randomized controlled clinical trial.
Conclusion
This study revealed that external sinus lift procedures may result in ideal bone grafting when considering the final position of the implant while respecting restorative guidelines. Usually, however, an excess or insufficient amount of bone grafting is used during a maxillary lateral sinus augmentation procedure. Future studies with a higher level of study design should consider an approach that utilizes technology in combination with an interdisciplinary team of experts to quantify the amount of bone graft needed and its position to achieve an ideal maxillary sinus elevation for future implant placement.
ACKNOWLEDGMENT
This research project (#102795-00001) was selected as the 2019 Osseointegration Foundation Applied Science Research Grant winner. The authors are grateful for the support received from the Department of Research Administration, especially Mrs. Amanda Gozzi.
ABOUT THE AUTHORS
Gayathri M. Shenoy, BDS, MS, DMD
Private Practice limited to Periodontology and Implant Dentistry, Providence, Rhode Island
Konstantinos Vazouras, DDS, MPhil, MDSc, DMD
Associate Professor and Postgraduate Program Director, Department of Prosthodontics, Tufts University School of Dental Medicine, Boston, Massachusetts
Aruna Ramesh, BDS, MS, DMD
Professor, Diagnostic Sciences – Oral and Maxillofacial Radiology, and Associate Dean of Academic Affairs, Tufts University School of Dental Medicine, Boston, Massachusetts
Shruti Jain, BDS, MPH
Assistant Professor, Public Health and Community Service, Tufts University School of Dental Medicine, Boston, Massachusetts
Nadeem Y. Karimbux, DMD, MMSc
Professor of Periodontology and Dean, Tufts University School of Dental Medicine, Boston, Massachusetts
Irina F. Dragan, DDS, DMD, MS, eMBA
Adjunct Associate Professor, Periodontology, Tufts University School of Dental Medicine, Boston, Massachusetts; Faculty Member, Harvard School of Dental Medicine, Boston, Massachusetts; Private Practice limited to Periodontology and Implant Dentistry, Boston, Massachusetts
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Figures and Images
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