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Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2017.01.003, available online at http://www.sciencedirect.com
Clinical Paper Pre-Implant Surgery
Inferior alveolar neurovascular bundle repositioning: a retrospective analysis
A. Sethi, S. Banerji, T. Kaus Centre of Implant and Reconstructive Dentistry, London, UK
A. Sethi, S. Banerji, T. Kaus: Inferior alveolar neurovascular bundle repositioning: a retrospective analysis. Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx. # 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. In this study, patients with an insufficient height of bone for implant placement in the posterior mandible were treated by repositioning of the inferior alveolar neurovascular bundle (IANVB). These patients were divided into two groups: those in group A (n = 69) did not require a bone graft and implants were placed at the time of nerve repositioning; those in group B (n = 9) received bone grafts in conjunction with nerve repositioning and implants were placed upon maturation of the grafts. One hundred and twenty-one nerves were repositioned in 78 patients and 308 implants were placed. Three implants failed within the first 10 months after placement. With a certainty of 95%, an estimated overall mean survival rate better than 97.8% was observed after a mean observation period of 84.5 months. The recovery of sensation was monitored using standardized tests. The recovery of sensation varied from 24 h to 6 months. Five patients reported some residual altered sensation. The technique of repositioning the IANVB provides an effective way of treating the atrophic posterior mandible with acceptable morbidity and a high implant survival rate; however the risk of dysesthesia must be acknowledged and patients properly informed.
The amount of bone available in the posterior mandible for implant placement is limited by the position of the inferior alveolar canal. This may be further compounded by resorption of the alveolar ridge as a result of normal atrophy following tooth loss or a number of other causes. These include an increased rate of resorption due to the use of a soft tissue-supported removable prosthesis and pathologies associated with failing teeth or implants. 0901-5027/000001+06
The management of these patients is challenging in view of the difficulty in constructing removable tissue-borne partial dentures to provide masticatory function. Alternative treatments to provide fixed implant-supported restorations include the use of short implants, bone augmentation, distraction osteogenesis, and bypassing the inferior alveolar canal. Repositioning of the inferior alveolar neurovascular bundle (IANVB) is
Keywords: Inferior alveolar nerve repositioning; Dental implants; Posterior mandible; Atrophic mandible; Bone grafts. Accepted for publication 3 January 2017
reported as a method of making the entire height of the mandible available.1,2 The procedure carries an inherent risk of damage to the IANVB, which has been reported by various authors and is summarized in recent systematic reviews and reports.3–6 This must be seen in the context of the inherent risk of working in this region, where high incidences of nerve damage are reported (up to 19% at the 2-year recall).7
# 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003
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A distinction is made within the literature for repositioning of the IANVB. Nerve lateralization refers to a technique not involving the mental foramen and consists of moving the neurovascular bundle laterally and returning it to lie against the implants following their insertion. Nerve transpositioning is described as involving the mental foramen, severing the incisive branch and constructing a new foramen in a more distal position. Nerve transpositioning is reported to have a higher incidence of dysesthesia than nerve lateralization.6,8,9 The aim of this retrospective analysis was to review the recovery of sensation after nerve repositioning, including both lateralization and transpositioning, and to evaluate the survival of the implants placed. Materials and method
A retrospective analysis of clinical records of patients treated between 1988 and 2013 was performed. All treatment options and associated risks and benefits were discussed with the patient and written consent obtained prior to treatment. All patients treated with IANVB repositioning were included in the analysis. These patients fell into two groups: those who did not require a bone graft (group A) and those who required a bone graft in addition to the nerve repositioning procedure (group B). All patients who required nerve repositioning had edentulous jaws of class IV, V, or VI, as described by Cawood and Howell.10 Group A patients did not require a bone graft (Fig. 1; nerve lateralization). With regard to bone volume, patients had a bone
Patient assessment
All cases were assessed using either medical computed tomography (CT) scans or cone beam computed tomography (CBCT) scans, in order to identify the exact position of the mental foramen and to evaluate the course of the IANVB, as well as the density and volume of bone.
Fig. 2. Cross-sectional CBCT scan image of a typical class IV posterior mandible suited for a combined approach of nerve repositioning and a bone graft.
height of between 2 mm and 8 mm available above the inferior alveolar canal, and a minimum width of 6 mm was present. However the estimated total height of mandibular bone available after IANVB repositioning was in excess of 10 mm. With regard to soft tissue, the crest of the ridge was above the floor of the mouth, and attached keratinized tissue was present. Group B patients required a bone graft (Figs. 2 and 3; nerve transpositioning). With regard to bone volume, patients had a bone height of between 0 mm and 6 mm above the inferior alveolar canal and/or an insufficient width (less than 4 mm of width). The estimated effective mandibular bone height after repositioning of the IANVB was also less than 10 mm. With regard to soft tissue, the crest of the ridge was below the floor of the mouth and had little or no attached or keratinized tissue, and consequently there was a risk of long-term maintenance problems.
Surgical treatment
All operations were performed by a single surgeon. The technique used did not change over the study time period other than the introduction of a piezoelectric surgery unit 10 years ago to supplement the use of rotary instruments for bone removal. Crestal incisions were used to gain access to the mental foramen where the mental foramen was classically positioned on the labial aspect of the mandible. In severely resorbed cases, where the foramen was positioned on the superior surface, access was gained by tunnelling distally, exposing the foramen and subsequently extending the incision. In all cases, the inferior alveolar canal was identified at the mental foramen and traced distally. A ball-ended fine curved probe was inserted into the inferior alveolar canal to identify its position during exposure. Bone removal was performed using high-speed rotary instruments whilst protecting the mental nerve. In the more recent years, a piezoelectric surgery unit was used, permitting the bone to be removed with greater precision and safety than with a rapidly rotating bur. The IANVB was carefully mobilized following the exposure of the canal to prevent damage to the nerve. Stretching or compressing of the nerve was avoided.11 Group A
Fig. 1. Cross-sectional CBCT scan image of a typical class V mandible, which is ideally suited for nerve repositioning without the need for bone grafts.
Fig. 3. CT scan of a typical class VI mandible requiring a combined approach of nerve repositioning and a bone graft.
The anterior portion (incisive branch) was exposed to start with. The overlying bone was removed and the probe advanced exposing 5 mm to 10 mm of the incisive branch. The mental nerve was then deflected into the space created and the distal portion of bone overlying the inferior alveolar canal was then approached. A round tungsten carbide bur rotating at 100,000 rpm and irrigated with profuse sterile saline was used to carefully and gradually remove the bone until the probe could be seen through the remaining bone. The thin remaining layer of bone over the IANVB was removed manually, the explorer was advanced further, and the procedure was repeated.
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003
YIJOM-3577; No of Pages 6
Inferior alveolar nerve repositioning
Fig. 4. IANVB repositioned with implants in situ and both mental and incisive branches intact (nerve lateralization). The sensory supply to the remaining teeth is retained.
The IANVB was carefully retracted during implant placement. The incisive branch was usually retained (Fig. 4) and only severed if the nerve could otherwise not be manipulated for safe implant placement or if the patient was edentulous (Fig. 5). Implants were inserted simultaneously at the time of nerve repositioning. The nerve was replaced within the body of the mandible as long as there was sufficient width present. A biomaterial (betatricalcium phosphate or demineralized freeze-dried bone) was used to separate the IANVB from the implant surface and also to cover the defect.
Group B
The incisive branch was sacrificed and the nerve transpositioned buccally in group B to be able to place an onlay bone graft. A foramen (groove) was created in the external oblique ridge, in the region of the second molar (Fig. 6). This minimized the risk of injury to the buccally positioned IANVB. Implants were placed after maturation of the graft at approximately 3 months following the grafting procedure.
Fig. 6. Three-dimensional image of the postsurgical CT scan taken to plan implant placement. The graft can be seen in situ, as well as the recreated mental foramen in the region of the second molar.
Postoperative monitoring
All postoperative neurosensory assessments were performed by a single observer. Monitoring of the recovery of sensation was started 24 h after surgery to evaluate the commencement of recovery using the wisp test. Subsequently recovery was monitored at 1 week, 1 month, 3 months, and 6 months following surgery. A series of tests was performed during these monitoring sessions to evaluate the recovery of sensation and were as follows: (1) sharp test: a sharp probe was used to elicit a pain response; (2) wisp test: a wisp of cotton wool was lightly run over the affected area to monitor touch; (3) heat test: a cotton wool roll dipped in a water bath at 55 8C was used to monitor sensitivity to heat; (4) cold test: ethyl chloride sprayed on a cotton wool roll was used to elicit a response to cold; (5) discriminatory distance test: two points of a divider set 4–12 mm apart were used to establish whether the two points could be discriminated; the separation of the two points of the divider was determined by the discriminatory distance at an unaffected site. All of the tests were calibrated arbitrarily against an unaffected area, either on the upper lip or on the opposite side of the mandible.
Post-treatment monitoring
Fig. 5. Image of the IANVB repositioned with implants in situ, but the incisive nerve severed (nerve transposition). No anterior teeth are present.
Patients were reviewed on a regular basis at 6 months, 12 months, and every 2 years thereafter. Clinical examinations were performed and radiographs taken to monitor the health of the peri-implant hard and soft tissues (Fig. 7). Bone level measurements were performed by two dental nurses independently on separate occasions to allow the assessment of inter-observer variation.
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Fig. 7. Intraoral peri-apical radiograph taken 14 years postoperatively. The stability of the implants is evident, as is the outline of the inferior alveolar canal alongside the implants.
Digital radiographs were subjected to measurement using VixWin software (Gendex Dental Systems, Hatfield, PA, USA). Conventional radiographs were measured using a light table, a magnification glass (3 magnification), and a Vernier calliper. Bone levels were recorded at each implant site at the position where the greatest amount of bone loss had taken place (mesial or distal) as a worst-case scenario. Root–crown ratios were determined by measuring dental panoramic radiographs. The implant length was determined from the shoulder to the apex and the prosthetic length was measured from the implant shoulder to the highest cusp. For splinted restorations, the shortest implant length was used to determine the implant–crown ratio as a worst-case scenario. Statistical analysis
Clinical data were collected and entered into a database (Microsoft Access; Microsoft, Redmond, WA, USA). Statistical software (JMP; SAS Institute Inc., Cary, NC, USA) was used to perform an analysis of the clinical data gathered by importing the data from the clinical database. Box plots were used to depict the ages of the patients at the time of implant placement, the time under observation, and the lengths of the implants used. A Kaplan– Meier estimation was used to determine the survival of the implants. Recovery of sensation was plotted on a graph. Results
A total of 121 nerves (105 in group A and 16 in group B) were repositioned in a total of 78 patients (69 patients in group A and nine patients in group B), and a total of 308 implants were placed. Two hundred and sixty-eight implants were placed in group A and 40 implants were placed in
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003
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Fig. 8. Age distribution of the patients at the time of implant placement; histogram and box plot.
group B. Sixty-two patients were female and 16 patients were male. Fig. 8 depicts the age distribution of all patients at the time of implant placement. At implant placement, the patients ranged in age from 28.5 years to 74.4 years; the mean age of all patients at implant placement was 54.3 years. The mean time of observation since implant placement for all 308 implants placed was 84.5 months. The range of time under observation since implant placement is depicted in Fig. 9. A total of three implants failed within 10 months of placement. All three implants failed in non-grafted cases (group A). One implant failed as a result of non-integration and was not replaced. Two implants failed in a different patient as a result of infection observed 1 month postoperatively. Both implants were removed, and one was replaced on completion of healing. The Kaplan–Meier survival curve of the implants under observation since placement is depicted in Fig. 10. With a certainty of 95%, an estimated overall mean survival rate better than 97.8% was calculated after a mean observation period of 84.5 months, as well as after an observation period of 121 months (i.e., based on 100 implants under observation at 121 months, 95% confidence interval (CI) = 98.99% 1.1%). The lengths of the implants placed ranged from 10 mm to 20 mm, with a median
Fig. 10. Kaplan–Meier survival curve for implants.
Fig. 11. Distribution of implant lengths; histogram and box plot.
value of 14 mm. Fig. 11 depicts the distribution of implant lengths that were used. Table 1 summarizes the mean values of the actual lengths of all implants placed, as well as for groups A and B separately. No significant difference in implant length between groups A and B was demonstrated. All patients had total recovery of sensation based on the objective tests that were performed. However, a total of five patients continued to state that they experienced an altered sensation, even though the objective tests indicated a return to normal sensory function. When questioned, the nature of the altered sensation could not be pinpointed but appeared to be quite vague. The total recovery of sensation varied from 24 h to 6 months. The variation in neurosensory recovery was unrelated to the timing of treatment. No correlation could be obtained between earlier or later cases, or the difficulty of each case in terms of bone density or the position of the IANVB within the mandibular bone. The majority of the cases had a mental foramen on the buccal aspect. In highly resorbed cases (class VI), where the basal bone had also resorbed, the foramina were noted to be on the superior surface.
The majority of the patients had made a total recovery at 3 months post-surgery. Fig. 12 depicts the recovery of neurosensory function following the repositioning procedure. Out of 78 patients, 4 patients with bilateral repositioning of the IANVB had a different recovery time between one side and the other. The diagram has incorporated 2 different recovery times for these 4 patients, thus depicting a total of 82 different recovery times. All but three patients demonstrated complete recovery after 12 months, based on subjective feedback. Three patients (two from group A and one from group B–unilateral) claimed altered sensation of the lip and chin but found it completely acceptable. The objective tests, including the discriminatory test, considered to be the most sensitive test, demonstrated total recovery. Further analysis of the radiographic data was performed to determine the crown– implant ratio and compare groups A and B. Table 2 summarizes the crown–implant ratio and compares groups A and B. The calculations are based on measurements taken from the top of the bridge to the implant shoulder as the prosthetic length and calculated against the length of the shortest implant on panoramic radiographs for each superstructure (worst-case prosthetic ratio). Based on a comparison of the confidence intervals, no significant difference between groups A and B could be demonstrated. Crown and implant lengths showed an approximate ratio of 0.9:1. A total of 224 implants were available for ongoing monitoring and follow-up. Eighty-four implants were followed up by referring dentists and were not available for analysis. No statistically significant difference in mean observation period was found between implants in group A and in group B. The mean bone loss was calculated and compared between the groups; no significant difference was observed. Bone loss as a criterion for success was calculated according to Smith and Zarb (1.5 mm in the first year, followed by 0.2 mm annually thereafter).12 Table 3 summarizes the results of the measurements of change in bone levels. Once again, no significant difference was observed between groups A and B. Patients were seen by a hygienist on a regular basis. Whenever inflammation or suppuration was observed, this was rectified
Table 1. Mean length of the implants that were placed.
Fig. 9. Time under observation since implant placement; histogram and box plot.
Total number of implants Implant length, mm (95% CI)
All patients
Group A
Group B
308 15.1 0.2
268 15.1 0.3
40 15.0 0.5
CI, confidence interval.
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003
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Inferior alveolar nerve repositioning
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Fig. 12. Recovery of neurosensory function following the nerve repositioning procedure. 4 patients with bilateral IANVB repositioning exhibited a difference in recovery times between the right and left hand side. These were recorded as separate recovery times. Therefore 82 separate recovery times were depicted in the graph.
by conservative means. At the last appointment, no bleeding or suppuration was recorded. However, a number of patients exhibited excessive bone loss requiring intervention, as shown in Table 4. Discussion
Repositioning the IANVB is a procedure that carries a high risk of permanent damage to the inferior alveolar nerve. This may range from total anaesthesia to dysesthesia, which would be less tolerated by
the patient. The decision to undertake such a procedure must be justified by the need to provide posterior support to stabilize the dentition and provide function. It must be borne in mind that the risk of damage to the IANVB is present whenever any form of implant-related treatment is carried out in the posterior mandible. This risk is likely to increase whenever limited bone is present, which requires placing implants in close proximity to the IANVB. Sensory disturbances of up to 39% directly postoperative have been reported merely
when implants have been placed within the available bone.7 A number of alternative techniques to provide adequate bone for the insertion of implants were considered. Amongst these, the technique of distraction osteogenesis was not considered appropriate for these patients during the evaluation. This was based on the inherent risk of paresthesia during the preparation of the segment to be distracted and the risk of damage during the fixation of the distractor with the screws. Furthermore the risk of potential
Table 2. The crown length–implant length ratio for all implants.
Prosthetic ratio (worst case): crown length–implant length (95% CI)
All patients
Group A
Group B
90.0% 4.9%
88.1% 5.6%
98.2% 10.5%
CI, confidence interval. Table 3. Changes in bone level in the study groups. Number of implants under observation Observation time, months (95% CI) Mean bone loss, mm (95% CI) Success based on bone loss, %
All patients
Group A
Group B
224 98.1 7.6 0.6 0.2 92.9
184 97.3 8.8 0.6 0.2 91.8
40 101.7 13.8 0.5 0.4 97.5
CI, confidence interval. Table 4. Patients exhibiting excessive bone loss and requiring intervention. Implant sites requiring peri-implant surgery due to peri-implantitis Peri-implantitis sites resolved with non-surgical therapy
All patients
Group A
Group B
16 4
7 –
9 4
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003
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loss of the distracted segment was considered unacceptable. Numerous studies have demonstrated predictable recovery of sensation as long as damage to the inferior alveolar nerve has not occurred.8,9,13 The benefits and risks of this treatment must be evaluated carefully. The surgical risk of paresthesia must therefore be balanced against the disadvantages caused by the absence of dentition. For example, in partially dentate cases there is a risk of over-eruption of the opposing teeth if the edentulous area of the mandible is not treated. Implant-supported restorations provide an effective prosthesis to return patients to function, eliminating the risk of overeruption of the opposing dentition. Implants provide a more effective alternative to the soft tissue-supported prosthesis, which may result in accelerated resorption of the already atrophied jaw. In order to evaluate the benefits of this treatment against the risk of paresthesia, a series of sensory tests were performed. The primary purpose of the tests was to ensure that the patients did not suffer any functional compromise as a result of the procedure. No such compromise could be identified. The technique is a delicate one and must be performed without any tears to the perineurium. The IANVB must not be stretched by more than 8% and must not be compressed.14 The anterior loop of the canal near the mental foramen requires the greatest care in order to avoid damage. The patients treated in this study with this technique benefited by being provided with a stable and functional dentition supported by osseointegrated implants. No difference in neurosensory recovery was noted between nerve lateralization and nerve transpositioning. The benefits of this treatment therefore depend upon the survival and the success of the implants that provide support for the restorations. The data gathered demonstrate excellent survival of implants. The loss of bone was used as one of the criteria to establish success based on the parameters defined by Smith and Zarb.12 Acceptable levels of bone loss were found in 92.9% of the cases. Other criteria of success, such as the absence of inflammation and pain, were also observed at the last monitoring appointment and are dependent on patient compliance. The lack of paresthesia demonstrated that no anatomical structures were damaged, in this case the IANVB. This is consistent with recent systematic reviews evaluating neurosensory disturbances after inferior
alveolar nerve repositioning and transpositioning.3,4,6 One review found an incidence of 0.53% (2/378) of neurosensory disturbance at 12 months and longer.4 Survival rates, based on the 21 studies included in that review, ranged from 88% to 100% except in two case reports.4 An earlier systematic review based on 24 included studies reported a 3.4% incidence of disturbance at the end of the study when lateralization was performed, and 22.1% when transpositioning was performed.6 One of the studies reported in that systematic review showed no neurosensory disturbance at any time. A more recent case series using piezoelectric surgery reported that 11 out of 13 sites demonstrated complete recovery after 3 months, with two sites exhibiting incomplete recovery.5 However, it also reported that the patients with residual altered sensation were completely satisfied and not compromised by the outcome.5 In evaluating the continuing use of this technique, new evidence-based developments must be considered. Current short-/ medium-term data on very short implants are encouraging; this will likely lead to a reduced need for this procedure in selected cases, as long as the risk of impinging on the nerve can be avoided. Funding
None. Competing interests
None. Ethical approval
Exempt determination by Chesapeake IRB, as per letter from CIRBI– Pro00013056. Patient consent
Written patient consent was obtained to publish the clinical photographs.
4. Abayev B, Juodzbalys G. Inferior alveolar nerve lateralization and transposition for dental implant placement. Part II: a systematic review of neurosensory complications. J Oral Maxillofac Res 2015;6:e3. http:// dx.doi.org/10.5037/jomr.2014.6103. 5. de Vicente JC, Pena I, Brana P, HernandezVallejo G. The use of piezoelectric surgery to lateralize the inferior alveolar nerve with simultaneous implant placement and immediate buccal cortical bone repositioning: a prospective clinical study. Int J Oral MaxSurg 2016;45:851–7. http:// illofac dx.doi.org/10.1016/j.ijom.2016.01.017. 6. Vetromilla BM, Moura LB, Sonego CL, Torriani MA, Chagas Jr OL. Complications associated with inferior alveolar nerve repositioning for dental implant placement: a systematic review. Int J Oral Maxillofac Surg 2014;43:1360–6. http://dx.doi.org/ 10.1016/j.ijom.2014.07.010. 7. Astrand P, Borg K, Gunne J, Olsson M. Combination of natural teeth and osseointegrated implants as prosthesis abutments: a 2year longitudinal study. Int J Oral Maxillofac Implants 1991;6:305–12. 8. Fernandez Diaz JO, Naval Gias L. Rehabilitation of edentulous posterior atrophic mandible: inferior alveolar nerve lateralization by piezotome and immediate implant placement. Int J Oral Maxillofac Surg 2013;42:521–6. http://dx.doi.org/10.1016/ j.ijom.2012.10.015. 9. Hashemi HM. Neurosensory function following mandibular nerve lateralization for placement of implants. Int J Oral Maxillofac Surg 2010;39:452–6. http://dx.doi.org/ 10.1016/j.ijom.2010.02.003. 10. Cawood JI, Howell RA. A classification of the edentulous jaws. Int J Oral Maxillofac Surg 1988;17:232–6. 11. Sethi A, Kaus T. Practical implant dentistry. The science and art. Second edition. London: Quintessence Publishing Co. Ltd; 2012. 12. Smith DE, Zarb GA. Criteria for success of osseointegrated endosseous implants. J Prosthet Dent 1989;62:567–72. 13. Morrison A, Chiarot M, Kirby S. Mental nerve function after inferior alveolar nerve transposition for placement of dental implants. J Can Dent Assoc 2002;68: 46–50. 14. Lundborg G. Nerve injury and repair. Churchill Livingstone; 1988.
References 1. Sethi A. Inferior alveolar nerve repositioning in implant dentistry: clinical report. Implant Dent 1993;2:195–7. 2. Sethi A. Inferior alveolar nerve repositioning in implant dentistry: a preliminary report. Int J Periodontics Restorative Dent 1995;15:474–81. 3. Abayev B, Juodzbalys G. Inferior alveolar nerve lateralization and transposition for dental implant placement. Part I: a systematic review of surgical techniques. J Oral Maxillofac Res 2015;6:e2. http://dx.doi.org/ 10.5037/jomr.2014.6102.
Address: Ashok Sethi Centre of Implant and Reconstructive Dentistry 33 Harley Street London W1G 9QT UK Tel.: +44 2076365676 fax: +44 2074368979 E-mail:
[email protected]
Please cite this article in press as: Sethi A, et al. Inferior alveolar neurovascular bundle repositioning: a retrospective analysis, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.01.003