Accepted Manuscript Surgical correction of horizontal bone defect utilizing the lateral maxillary wall: outcomes of a retrospective study Eduardo Anitua, DDS, MD, PhD Mohammad Hamdan Alkhraisat, DDS, PhD A. Miguel-Sánchez, PhD, DDS Gorka Orive, PhD PII:

S0278-2391(13)01433-X

DOI:

10.1016/j.joms.2013.11.022

Reference:

YJOMS 56140

To appear in:

Journal of Oral and Maxillofacial Surgery

Received Date: 9 April 2013 Revised Date:

20 November 2013

Accepted Date: 21 November 2013

Please cite this article as: Anitua E, Alkhraisat MH, Miguel-Sánchez A, Orive G, Surgical correction of horizontal bone defect utilizing the lateral maxillary wall: outcomes of a retrospective study, Journal of Oral and Maxillofacial Surgery (2014), doi: 10.1016/j.joms.2013.11.022. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Surgical correction of horizontal bone defect utilizing the lateral maxillary wall: outcomes of a retrospective study Eduardo Anitua1,2 DDS, MD, PhD, Mohammad Hamdan Alkhraisat2 , DDS, PhD,

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Miguel-Sánchez A3, PhD, DDS, Gorka Orive 1,2 PhD

Eduardo Anitua Foundation; c/ Jose Maria Cagigal 19, 01007 Vitoria, Spain

2

BTI Biotechnology Institute, c/ Jacinto Quincoces 39, 01007, Vitoria, Spain. Clínica Odontológica Universitaria, University of Murcia, Avda. Marqués de los Vélez

s/n, 30008, Murcia, Spain.

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Correspondence address: Dr. Eduardo Anitua, Eduardo Anitua Foundation; C/ Jose Maria Cagigal 19, 01007 Vitoria, Spain; Phone: +34 945160653, e-mail:

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[email protected]

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Abstract

Purpose: Report on the outcomes of a new surgical technique for the treatment of

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severe horizontal bone resorption that impedes the placement of dental implants.

Materials and methods: Eleven patients in need for bone augmentation to reconstruct a

narrow alveolar ridge were recruited for this study. Surgical correction of the alveolar

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width was carried out by harvesting an onlay bone graft from the lateral wall of the maxillary sinus and filling the intervening space with plasma rich in growth factors

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alone or mixed with autologous bone particles. Fibrin membrane was then placed to cover the surgical site before flap closure. Clinical examination and cone-beam CT scans were performed to analyze the safety and efficiency of an onlay bone graft from

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the maxilla in horizontal bone augmentation.

Results: This is the first study to describe the lateral wall of the maxillary sinus as a donor site for an onlay bone graft. The healing period was uneventful with minimal

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surgical morbidity. No flap exposure occurred and the analysis of cone-beam CT scans before and after (about 5 months) bone augmentation revealed a total gain of 5.4 mm in

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alveolar width. This permitted the placement of dental implants to support an implantborne prosthesis.

Conclusions: Onlay bone graft from the lateral wall of the maxillary sinus is a useful and safe tool for horizontal bone augmentation with minimal surgical morbidity.

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Introduction

The quantity and quality of both hard and soft tissues are critical factors in achieving

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satisfactory results with implant-borne prostheses. However, deficits in soft and /or hard tissues, due to changes due to tooth loss, is frequently encountered and requires the

performance of reconstructive surgery1 to correct the sequelae of alveolar bone resorption: 1) a posterior short and rounded alveolar process, and 2) an anterior narrow

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process.2 In the maxilla, vertical bone augmentation is achieved by the performance of

sinus floor augmentation, whereas horizontal bone augmentation is carried out via the

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performance of guided bone regeneration and/or the use of a bone block.

Bone augmentation with onlay graft requires the harvesting of a bone block from an extra- or intra-oral donor site. Extra-oral donor sites (like tibia, hip and parietal bone)

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are selected when a large amount of bone is needed to reconstruct the maxilla or mandible. Bone harvesting from such sites requires a longer surgical procedure.3,

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Furthermore, the embryonic origin is different between the harvested bone 6

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(endochondral ossification) and the alveolar bone (intramembranous ossification).5,

This is a factor that could influence the success of bone augmentation surgery as

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intramembranous bone graft seems to maintain its volume, whereas endochondral bone graft undergoes variable degrees of resorption over time.7-9

These limitations stimulated the search for and development of surgical techniques to obtain bone blocks from intra-oral donor sites.4 The reconstruction of alveolar bone for the placement of dental implants is usually localized to small area and requires smaller amounts of bone which makes feasible the selection of an intraoral donor site. The

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facile access and the possibility to obtain bone blocks without debilitating the mandible makes the symphysis a suitable donor area.5, 10, 11 Donor site morbidity, although very much lower than extra-oral sites, was reported to include pain, functional limitations,

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swelling and altered sensation in the mental and lower lip area.3 Temporary paresthesia after chin graft harvesting surgery ranged from 10 to 50%, 3, 8 and in one study impaired nerve function was considered permanent in 15 out of 22 patients who suffered altered

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sensation.3

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and the

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The ramus of the mandible is another target that allows easier surgery

possibility to obtain bone blocks of sufficient dimensions to rehabilitate vertical and horizontal alveolar bone loss.12 This donor site showed lesser postoperative complications than the symphysis area.3,

11

However, patients could suffer from

swelling, and difficulty during mouth opening and chewing. Altered sensation was

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fewer (ranged from 0 to 5%), and usually it was not persistent when compared to the symphysis.8, 3 Khoury and Khoury have developed an efficient reconstructive method based on the use of thin cortical bone block harvested from the external oblique line of 13

In this technique, the thin bone block acts as membrane and the

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the mandible.

intervening space with the residual alveolar process is filled with particulated

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autologous bone.13 This 3-D reconstructive method has the advantage to replace not only the buccal walls, but also the lingual (palatal) walls of a bone defect.13

The success of this technique has encouraged us to propose a novel use for the bone block removed from the lateral wall of the maxillary sinus during sinus floor augmentation. This novel indication consists of the use of the thin bone block as onlay bone graft to rehabilitate horizontal bone deficiency in the maxilla. Maxillary sinus

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floor augmentation is a well-documented surgical technique to resolve insufficient bone height in the posterior maxilla with minimal surgical morbidity.14,

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In the lateral

approach, a bone window in the lateral wall of the sinus is necessary to access the

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Schneiderian membrane for sinus floor elevation.16, 17

This study was conducted to evaluate the applicability of the thin bone block from the

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lateral wall of the sinus in horizontal bone augmentation and to evaluate possible surgical complications. The bone augmentation was used for in narrow alveolar ridges

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in the anterior and/or premolar region of the maxilla. Patients were followed to evaluate the occurrence of surgical complications and radiographic examination was used to measure the gain in bone width.

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Materials and methods

The patient database was reviewed to identify those who underwent lateral sinus floor augmentation. Patient's participation in this study was based on the following inclusion

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criteria: the presence of narrow alveolar ridge in the anterior and/or premolar region of the maxilla as indicated by a cone-beam CT (CBCT) scan, the use of onlay bone graft

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obtained from the lateral wall of the maxillary sinus, and the availability of CBCT scan before and after horizontal bone augmentation. Patients who failed to meet any of these criteria were excluded from the study. The principal outcomes were surgical complications, and the width of the narrow maxilla before and after the surgical intervention. The study protocol was approved by the institution's review board.

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Before surgery, patients received 1 g of amoxicillin 30 minutes before surgery and 1 g of acetaminophen 1 hour preoperatively. Plasma rich in growth factors (PRGF-Endoret) was prepared from citrated whole blood according to the instruction of the manufacturer

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(Biotechnology Institute, Vitoria, Spain). According to this protocol, plasma column was separated into fraction 2 (F2) that contains the 2 mL of the plasma richest in platelets and located just above the buffy coat (platelet richest), and into fraction 1 (F1)

that contains the rest of plasma column. Platelet activation was performed by the

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addition of 50 µL of 10% of calcium chloride per each 1 mL of plasma.18

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Lateral sinus floor augmentation: under local anesthesia, full-thickness flap was reflected to expose the alveolar crest and the lateral aspect of the posterior maxilla. A window in the lateral wall of the maxillary sinus was then created by piezoelectric surgery (BTI-ultrasonic)19 to minimize the risk of membrane perforation and postoperative complications. The removed bone block was stored in fraction 2 of

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plasma rich in growth factors (PRGF-Endoret) to increase cell survival and maintain the hydration of bone.15 This bone block was used as onlay bone graft for horizontal bone augmentation as described later.

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The sinus floor was vertically repositioned to generate a space that was filled with anorganic bovine bone mixed with PRGF-Endoret. A Valsalva maneuver was

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performed to detect any perforation of the Schneiderian membrane. A PRGF membrane prepared from fraction 1 was positioned to cover the lateral window before flap closure with monofilament 5/0 suture.

Horizontal bone augmentation: after flap elevation, the only bone graft from the lateral wall of the maxillary sinus was repositioned on the labial wall of the narrow maxilla to re-establish the horizontal dimension. Onlay graft fixation was done with a screws of 1

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and 1.2 mm in diameter, and 6 and 8 mm in length (Fig. 1 and 2). The intervening space between the onlay graft and the alveolar process was filled with autologous bone particulate mixed with fraction 2 of PRGF-Endoret (Fig. 1 and 2). The autologous bone

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particulate (3 patients) was obtained from the drilling procedure for implant insertion in another locations or by bone scraping. Otherwise, PRGF-Endoret clot prepared from fraction 2 (F2) was used as the sole filling material (8 patients).

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PRGF-membrane prepared from fraction 1 (F1) was then placed to cover the surgical site before flap closure with monofilament 5/0 suture. If tension was observed upon flap

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closure a periosteal relieving incision was practiced to achieve tension-free flap suturing.

Follow-up: visits were scheduled at 7 days, 14 days and 4-5 months after surgery. The first 2 visits were dedicated to remove sutures and to detect any surgical complications

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like graft exposure, infection, swelling, altered sensation, and hematoma. In the latter visit (4-5 months) a new cone-beam CT(CBCT) scan was realized and a second surgery

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was performed to place dental implants.

Radiographic analysis: CBCT scans obtained by GALILEOS 3D scanner were

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analyzed with BTI scan (Biotechnology Institute, Vitoria, Spain) to retrieve the width of the narrow alveolar process before and after (5 months) surgical augmentation. Measurements of the residual width of the alveolar process were performed for each bucco-lingual section that include the horizontal bone defect. At 5 months of surgery, the measurements were repeated as described earlier and the graft from the lateral maxillary wall served as reference to select the bucco-lingual section to perform the measurements.

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Statistical analysis: Data collection and analyses were performed by two independent examiners. Patients records were analyzed to derive demographic data (gender and age),

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social habits (smoking, alcohol intake), parafunctional habits (bruxism), relevant medical conditions and history of periodontal disease.

Alveolar width of the narrow maxilla and the occurrence of surgical complications were

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the principal statistical variables. The data of alveolar width of the narrow maxilla

before and after augmentation were analyzed with paired t-student test. The statistical

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significance was set at p < 0.05.

Results

For this study, 11 patients (average age 56.2 ± 7.8 years) completed the inclusion

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criteria of whom 63.6% were females. Only 1 patient reported to be smoker and one patient had type II diabetes mellitus. All patients presented an acceptable periodontal

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health according to the classification of Armitage 1999.20

The surgical access to the lateral wall of the maxillary sinus (donor site) was easy and

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the employment of ultrasonic surgery was efficient to avoid any perforation of the Schneiderian membrane during the retrieval of the bone block from the lateral wall of the sinus. This thin bone block was then used as onlay bone graft to horizontally augment the alveolar process and to create a confined space where a filling material could be retained (Fig. 1 and 2). All the cases of horizontal bone augmentation were realized in the anterior and/or premolar area of the maxilla as is indicated in Table 1.

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All patients’ recovery was uneventful. The pain and patients’ need for analgesics were not higher than conventional maxillary sinus floor augmentation. Swelling, altered sensation and infection were not observed during the study period. Moreover, incision

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dehiscence at both donor and recipient sites were absent at the time of sutures removal.

Flap reopening after 4-5 months for implant insertion showed the bone block to be

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vascularized and well-integrated to the surrounding bone. The gap was filled by newly formed bone (Fig. 1 and 2). This resulted in significant horizontal augmentation that

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permitted the insertion of dental implants without the exposure of implant threads.

The radio-graphical analysis showed an initial width of 3.57 ± 0.46 mm with a range from 1.96 to 6.05 mm (Table 1 and Fig. 3). The horizontal defect spanned a length in mesiodistal direction higher or equal to 10 mm as can be seen in Figure 1 and 2. The use

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of bone block from the lateral wall of the maxillary sinus was effective to increase the alveolar width to 8.91 ± 1.67 mm (range 6-11 mm) (Table 1 and Fig. 3). This resulted in a statistically significant gain of 5.34 ± 1.59 mm (range 2.56-8.10 mm) in the horizontal

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dimension of the reconstructed area (Table 1). The percentage of horizontal bone

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augmentation ranged from 42 to 200%, with an average of 180.6% (Table 1).

Worth to mention, transepithelial abutments (Multi-im, BTI, Biotechnology institute) were screwed into the implant after 4 months of implant insertion to deliver screwretained provisional prosthesis. The type of the prosthesis was fixed partial denture in 10 patients whereas complete fixed denture was placed in one patient.

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A longer period of follow-up is ongoing to study the stability of the augmented bone volume around dental implants as well as the success of implant-borne prostheses.

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Discussion

Successful oral rehabilitation with implant-supported prosthesis requires the presence of

adequate bone volume to provide stability to the dental implants. Herein, we treated

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patients suffering from insufficient bone width in the maxilla with a bone block from

the lateral wall of the maxillary sinus. The main objective of this study was the

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evaluation of the utilization of thin bone block from the lateral wall of maxillary sinus in horizontal bone augmentation and possible surgical complications.

The lateral and anterior wall of the maxillary sinus has been employed as a donor site of

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autologous bone but in particulated form to accomplish bone augmentation in the anterior and posterior maxilla.21 Bone shavers and curved bone collectors were employed to remove and collect autologous bone from the lateral wall of the maxillary

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sinus to access the Schneiderian membrane during sinus floor augmentation surgery.22, The harvested bone was employed to fill the space created by sinus floor elevation to

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increase the height of alveolar process for implant placement.22, 23 The novelty of the present study is in the use of the lateral wall of the maxillary sinus as a donor site for an onlay bone graft (Fig. 1 and 2). This onlay graft was efficient to increase the initial alveolar ridge width of 3.57 ± 0.46 mm by 5.54 ± 1.59 mm, achieving a new width of 8.91 ± 1.67 mm (Fig. 3 and Table 1). The thin thickness of the block would facilitate graft revascularization and the intramembranous origin would contribute to maintain the augmented volume if compared to the higher degree of

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resorption reported for endochondral bone.7, 8, 24, 9 After 5 months of surgery, the onlay graft was well integrated to the surrounding bone.

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Yates et al, in a recent study in cadavers, have showed that the graft from the symphysis had higher thickness than the graft from the ramus.25 Bone block retrieved from the symphysis could provide sufficient bone to achieve horizontal augmentation of 4-6

mm,11, 12 whereas a block from the mandibular ramus provide sufficient bone to thicken

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the alveolar ridge by 3-4 mm.12 The novel technique described herein was as efficient as

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the symphysis and as the ramus of the mandible to achieve horizontal bone augmentation but with lesser morbidity. This could improve patients recovery and avoid the risk of persistent impaired nerve function occasionally resulted after bone harvesting from the symphysis or the ramus of the mandible.

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One of the complications of bone augmentation surgery using bone onlays is gingival dehiscence and block exposure. In a recent study, the application of PRGF membrane was highly effective to prevent titanium mesh exposure26 and to promote bone

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formation. Plasma rich in growth factors employs fibrin scaffold and endogenous growth factors that orchestrate tissue healing to promote adequate tissue regeneration

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and to reduce tissue inflammation.27, 28 These growth factors promote cellular growth, proliferation and migration.27,

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Herein, PRGF membrane was placed to cover the

augmented area before flap closure and this could help in the prevention of block exposure and protect the graft from infection. The end-result was the achievement of new bone formation and ridge thickening.

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Donor site morbidity (like pain, swelling, infection) was not higher than with the conventional sinus floor augmentation procedure. The most important anatomical structure that could be affected is the Schneiderian membrane. The use of piezoelectric

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surgery with ultrasonic tips is more friendly with Schneiderian membrane than conventional surgery.19 This helped to avoid perforating the Schneiderian membrane

and minimized donor site morbidity. The bone healing at the donor site was excellent

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and patients did not report any discomfort.

The use of guided bone regeneration with resorbable/non-resobrable membrane is

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another clinical procedure for horizontal bone augmentation. In this study, the advantage of using lateral maxillary wall is that it will act as osteogenic, osteoconductive and osteoinductive membrane thanks to the properties of autologous bone. This autologous membrane with a thickness of (2-3 mm) will be integrated (no need for second surgery to remove it) and gives additional millimeters for horizontal

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bone augmentation.

After 5 months, implants were inserted in the grafted area with an adequate torque (2060 Ncm), which is indicative of achievement of bone with sufficient mechanical

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strength (Fig. 1 and 2). This study suffers from the limitation of a retrospective study design, the number of recruited patients and the absence of a control. Further studies

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are necessary to study long-term stability of the augmented bone volume as well as the functionality of the implant-supported prostheses.

Conclusions

The novel surgical technique proposed herein resulted simple and effective for horizontal bone augmentation of narrow maxilla. Donor site morbidity was minimum

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and the bone block from the lateral wall of the maxillary sinus constitutes an effective tool for the horizontal reconstruction of alveolar bone.

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Acknowledgments MHA acknowledges the support from the Program of Torres Quevedo, Ministry of Economy and Competitivity, co-founded by the European Social Fund (PTQ-11-

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04711).

Conflict of interests

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The authors EA, MHA and OG are researchers at Biotechnology Institute I+D (Vitoria, Spain). MSA has no conflict of interests.

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References

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bone. Plast Reconstr Surg 76:510, 1985 7.

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and clinical study of immediate and preformed autologous bone grafts in combination with osseointegrated implants. Scand J Plast Reconstr Surg 14:23, 1980 8.

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placement using mandibular bone grafts. Implant Dent 4:261, 1995 Raghoebar GM, Meijndert L, Kalk WW, Vissink A: Morbidity of mandibular

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bone harvesting: a comparative study. Int J Oral Maxillofac Implants 22:359, 2007 12.

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protocol for reconstruction of alveolar ridge deficiency. JIACD 2:45, 2010 13.

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Fernandez E, Cutando A, Wang HL: Evaluation of sinus floor elevation using a composite bone graft mixture. Clin Oral Implants Res 18:376, 2007 Klijn RJ, Meijer GJ, Bronkhorst EM, Jansen JA: Sinus floor augmentation

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Figure Legends

Fig. 1. A narrow alveolar ridge that span a 15.4 mm in mesiodistal direction with a width of 2.16 mm (a and b). The defect was treated with a bone block from the lateral wall of the maxillary sinus (c). The gap between the bone block and the alveolar wall

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was filled with a composite of PRGF-Endoret and autologous bone (c). Five months

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postoperatively, new bone was filling the original gap and augmented the alveolar bone width to 8.44 mm (d, e and f).

Fig. 2. Upper right canine with advanced bone loss resulting in a horizontal bone defect of 10.3 mm in mesio-distal direction (a) . After tooth extraction, the remaining alveolar wall had a width of 2.13 mm (b). This defect was bridged by an onlay bone block from the lateral wall of the maxillary sinus and the space were filled with PRGF-Endoret clot

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(c). After 5 months, the horizontal bone width was augmented to 10.1 mm (e and f). The bone block was well-integrated and new bone filled the original gap (g) which permitted

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the rehabilitation with fixed prostheses (h).

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Initial width

Final width

Gained bone width

Increased bone width

Implants (mm)

(Universal Numbering System)

(mm)

(mm)

(mm)

(%)

(diameter × length)

Case 1

6, 5

3.19 ± 0.015

8.83 ± 0.15

5.64 ± 0.16

176.8

3.75 × 10 and 3.0 × 10

Case 2

11, 12, 13

2.78 ± 0.01

8.96 ± 0.08

6.18 ± 0.08

222.3

3.75 × 10 and 3.3 × 8.5

Case 3

6, 5

5.10 ± 0.11

10.40 ± 0.23

5.30 ± 0.25

103.9

5.0 × 13

Case 4

6, 5

4.00 ± 0.15

7.50 ± 0.1

3.50 ± 0.18

87.5

3.3 × 11.5

Case 5

7, 6

1.95 ± 0.01

7.29 ± 0.07

5.34 ± 0.07

273.9

3.3 × 11 and 3.0 × 11

Case 6

5, 4

2.49 ± 0.017

9.62 ± 0.11

7.13 ± 0.11

286.4

4.0 × 10

Case 7

9, 10

3.50 ± 0.01

11.60 ± 0.02

8.10 ± 0.02

231.4

4.0 × 11.5

Case 8

12, 13

2.16 ± 0.02

8.22 ± 0.03

6.06 ± 0.03

280.6

4.25 × 10

Case 9

11, 12

6.02 ± 0.015

8.58 ± 0.04

2.56 ± 0.04

42.5

4.0 × 11.5

Case 10

9, 10, 11

6.05 ± 0.01

11.00 ± 0.03

4.95 ± 0.03

81.8

4.0 × 15

Case 11

6, 5

2.00 ± 0.1

6.00 ± 0.15

4.00 ± 0.19

200.0

5.0 × 13

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Table 1. Detailed description of clinical cases where horizontal bone augmentation was carried out to permit the placement of dental implants.

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