Clinical Outcome of the Use of Fresh Frozen Allogeneic Bone Grafts for the Reconstruction of Severely Resorbed Alveolar Ridges: Preliminary Results of a Prospective Study Matteo Chiapasco, MD1/Giacomo Colletti, MD2/Alberto Coggiola, MD, DDS3/ Giuseppe Di Martino, DDS3/Tommaso Anello, DDS3/Eugenio Romeo, MDD4 Purpose: The objectives of this study were to evaluate: (1) the clinical outcome of fresh frozen human allogeneic bone grafts (FFB) used for the reconstruction of severely atrophied edentulous ridges; (2) the survival rate of implants placed in the reconstructed areas; and (3) bone resorption. Materials and Methods: During a 2-year period, 19 patients with severely atrophied partially or totally edentulous ridges who were candidates for an implant-supported prosthesis were consecutively enrolled and reconstructed with FFB iliac blocks. Five to 7 months later, 117 implants were placed in the reconstructed areas, and prosthetic rehabilitation was started 5 to 6 months afterward. Results: The mean follow-up of patients after prosthetic loading was 27 months (range, 20 to 32 months). Prior to implant placement, graft exposure with partial or total loss of the graft occurred in four patients. After implant placement, bone graft exposures with partial loss of the grafts occurred in nine patients; in two patients, both grafts and implants were removed. The cumulative survival rate of implants was 90.2%. The mean (± standard deviation) graft resorption before implant placement was 0.98 ± 0.77 mm (range, 0 to 4 mm), while these values were 1.21 ± 1.05 mm (range, 0 to 6 mm) at loading, 1.55 ± 1.57 mm (range, 0 to 8 mm) at 12 months, and 1.93 ± 1.38 mm (range, 1 to 9 mm) at 24 months. Conclusion: Within the limits of this study (limited sample of patients and short follow-up), the reconstruction of severely atrophic edentulous ridges with FFB is associated with a relevant incidence of bone exposures and partial or total loss of the grafts, which may compromise the long-term survival of implants placed in the reconstructed areas. Int J Oral Maxillofac Implants 2015;30:450–460. doi: 10.11607/jomi.3763 Key words: allogeneic grafts, atrophy, bone graft, dental implant, fresh frozen allogeneic bone, reconstruction

N

owadays, the rehabilitation of partially or totally edentulous patients by means of oral implants and implant-supported prostheses is a routine and

1Professor

and Head, Unit of Oral Surgery, Department of Health Sciences, San Paolo Hospital, University of Milan, Milan, Italy. 2Senior Consultant, Unit of Maxillofacial Surgery, Department of Health Sciences, San Paolo Hospital, University of Milan, Milan, Italy. 3Assistant, Unit of Oral Surgery, Department of Health Sciences, San Paolo Hospital, University of Milan, Milan, Italy. 4Professor and Head, Unit of Prosthodontics, Department of Health Sciences, San Paolo Hospital, University of Milan, Milan, Italy. Correspondence to: Prof Matteo Chiapasco, Direttore Unità di Chirurgia Orale, Clinica Odontoiatrica - Dipartimento di Scienze della Salute - AO San Paolo, Università degli Studi di Milano, Via Beldiletto 1/3 - 20142 Milano, Italy. Fax: +39-02-50319040. Email: [email protected] ©2015 by Quintessence Publishing Co Inc.

well-documented treatment option.1,2 However, severe atrophy of partially or totally edentulous ridges (class V and VI according to the Cawood and Howell classification3) may lead not only to an insufficient bone volume to place osseointegrated implants, but also to unfavorable vertical, anteroposterior, and transverse maxillomandibular relationships (increased interarch distance, contraction of the transverse diameter, and/or retrusion of the maxilla) as a result of centripetal resorption of the edentulous ridges, which may compromise the definitive prosthetic restoration from a functional and esthetic viewpoint.3–7 Among the different solutions to augment bone volume at deficient sites, reconstruction with autogenous bone grafts obtained from intraoral or extraoral sites is one way to restore adequate bone volume and adequate maxillomandibular relationships to place implants in a correct, prosthetically driven position. Clinical outcomes of both reconstructive procedures and implant placement in the reconstructed sites are favorable and stable over time, with high survival rates for

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both grafts and implants.5–14 However, drawbacks of autogenous bone harvesting, including elongation of operating times, the need for general anesthesia, and hospitalization (in particular when extraoral donor sites are needed), all of which lead to increased risks of postoperative morbidity, cannot be disregarded.9,10,13,15–18 For these reasons and on the basis of the relevant experience achieved in orthopedic surgery,19–22 the use of allogeneic fresh frozen bone (FFB) grafts has been proposed as an alternative to autogenous bone for the reconstruction of atrophic arches before implant placement to reduce postoperative morbidity. However, results related to the use of FFB in oral reconstructive surgery are contradictory, as some authors reported apparently good results,23–30 whereas others reported inconsistent or questionable results.31–34 Moreover, the majority of these articles reported data related to the use of FFB for inlay grafts or onlay grafts for the correction of horizontally resorbed ridges.33–35 There is a paucity of data related to the use of FFB for the reconstruction of vertical defects, particularly if the defects involve large areas of tooth-bearing regions, including fully edentulous patients. The aim of this prospective study was to obtain more information about the behavior of this grafting material by focusing on: (1) the clinical outcome of FFB grafts used for the reconstruction of severely atrophic partially or edentulous arches, (2) the survival rates of oral implants placed in the reconstructed areas, and (3) the graft resorption.

MATERIALS AND METHODS Patient Selection

During a 2-year period (2010 to 2011), systemically healthy patients presenting with severe atrophy of partially or totally edentulous maxillae and/or mandibles (total or subtotal resorption of the alveolar ridges, corresponding to class V and VI according to Cawood and Howell3) that caused difficulty or prevented them from using a traditional removable denture and with insufficient bone to receive even short (≤ 6 mm) or reduced-diameter (< 3-mm) implants, were referred to the Unit of Oral Surgery, Department of Health Science, San Paolo Hospital, University of Milano, Italy, to determine the possibility of surgical reconstruction of their bone defects with allogeneic FFB iliac blocks to allow subsequent implant placement and implantsupported prosthetic restoration. Patients were evaluated to collect baseline data. Dental study casts and wax-ups were obtained to evaluate maxillomandibular relationships and create diagnostic and surgical templates with radiopaque markers. Radiographic examination included a panoramic

radiograph and a computed tomogram taken with the patient wearing the diagnostic templates to evaluate the relationship between the residual alveolar ridge and the ideal position of the missing dentition and, consequently, the reconstruction needed to place implants in proper, prosthetically driven positions. The enrolled patients presented with either partially or totally edentulous mandibles with less than 6 mm between the alveolar crest and the inferior alveolar canal or less than 6 mm in height in the anterior mandible or partially or totally edentulous maxillae with less than 6 mm between the alveolar crest and the nasal floor at less than 5 mm apical to the maxillary sinus (mainly as a result of relevant resorption of the alveolar ridge, not only sinus expansion). All patients presented with a relevant reduction of alveolar ridge width (less than 3 mm) with unfavorable vertical, horizontal, and/ or anteroposterior maxillomandibular relationships as a result of centripetal resorption of the edentulous ridges. All defects were of such an extent that intraoral bone grafts taken from the mental symphysis and/or from the mandibular rami were not an option because the available quantity was insufficient to properly reconstruct the deficient area. Harvesting of bone from an extraoral site was therefore necessary. Exclusion criteria included: (1) tobacco use (more than 20 cigarettes/day) or alcohol abuse; (2) congenital or acquired immunodeficiency; (3) severe renal and/or liver disease; (4) diabetes with glycosylated hemoglobin ≥ 7%; (5) history of radiotherapy in the head and neck region; (6) ongoing bisphosphonate or antiblastic chemotherapy for treatment of malignant tumors at the time of the first examination; (7) active periodontal disease involving the residual dentition (if any) at the time of the first examination (in this case, patients underwent etiologic therapy, education, and motivation in domestic oral hygiene and were reevaluated 6 months later); (8) maxillary sinus pathologies such as chronic sinusitis or relevant polyposis (when a maxillary reconstruction was needed); (9) mucosal disease, such as lichen planus, in any area to be treated; (10) poor oral hygiene; or (11) noncompliance. All patients received detailed information concerning the need for a bone grafting procedure from an extraoral site to allow the placement of oral implants in the edentulous areas affected by severe atrophy. Every patient was informed about the possibility of using iliac allogeneic FFB as an alternative to autogenous bone (AB) taken from the anterior ilium. Each patient was thoroughly informed about both the advantages and the risks related to the use of FFB and AB. For FFB, the advantages were summarized as follows: (1) no need to harvest bone from the patient’s ilium, with no associated donor site morbidity and related sequelae, including scars, temporary The International Journal of Oral & Maxillofacial Implants 451

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Chiapasco et al

ambulation disturbances, risk of fracture of the anterior iliac spine, or damage to the lateral femoral cutaneous nerve; and (2) a practically unlimited supply of reconstructive material.26,29 On the other hand, the potential disadvantages were synthesized as follows: (1) a risk of transmission of viruses such as hepatitis C (estimated 1.1 per 1 million), hepatitis B (estimated 3 per 1 million), and HIV (estimated 1.2 per 1 million); (2) immune reaction/rejection of the graft; (3) reduced or absent osteoinductive/osteogenetic potential; (4) limited patient populations and follow-ups with limited literature support (as compared to AB); (5) risk of bone resorption before and after implant placement.29,36–39 The advantages of AB can be summarized as follows: (1) absence of immune reaction; (2) known osteogenetic, osteoinductive, and osteoconductive potential; and (3) well-documented use with more than 30 years of clinical experience.5,7,9,17,40–42 Conversely, the disadvantages of AB would include: (1) longer operating time, (2) gait/ambulation disturbances for a variable time (up to 6 to 8 weeks), (3) visible scar in the skin overlying the harvesting area, (4) paresthesia in the lateral aspect of the thigh (if the lateral femoral cutaneous nerve is involved in the retraction of the flaps during the harvesting procedure), and (5) risk of bone resorption before and after implant placement. An informed consent document that included all information on the surgical procedures and the risks and complications potentially related to the reconstructive procedures with FFB and implant placement was signed by all patients before the beginning of treatment. Approval for this study was obtained from the Ethics Committee, Department of Health Sciences, San Paolo Hospital, University of Milan, Italy.

Reconstructive Procedure

All patients underwent professional oral hygiene treatment 1 to 2 weeks before the reconstructive procedure, even if no signs of periodontal disease were present. Patients were also asked to start chlorhexidine (0.2%) mouth rinses 2 days before surgery, three times per day. The reconstructive procedure was performed in all patients under general anesthesia with nasotracheal intubation and controlled blood hypotension. All patients received 2 g of ceftriaxone intravenously at the time of anesthesia induction. All reconstructive and implant placement procedures were performed by the same person (MC). A tricortical bone block and corticocancellous granules harvested from the anterior ilium of human cadavers were provided by the local tissue bank (Gaetano Pini Orthopaedics Institute). FFB is harvested aseptically from cadaveric donors and then frozen, with no additional preparation, and it becomes available for surgical purposes after at least 6 months of quarantine at –80°C.

Before use, FFB blocks were defrosted by immersion in a warm (+40°C) solution of sterile saline and rifamycin (500 mg per liter) for 45 minutes. After the blocks were defrosted, any residual portions of fat and connective tissue adherent to the surface were removed with a sharp blade. Finally, according to the extent and shape of the defect, the bone block was shaped to fit to the recipient site, with the highest possible quantity of cortical bone preserved. In some areas, a tricortical segment was used; in others, because of the excessive bulk of the bone block, one cortex was removed. The general rule was to reconstruct the deficient site using information obtained in the computed tomograms and wax-ups to recreate favorable conditions, not only for placement of implants with a minimum diameter of 3.3 mm and a minimum length of 8 mm, but also for a prosthetically driven rehabilitation. The maximum height and width of each block were measured with a caliper before fixing it to the recipient sites. To reconstruct the arches, the edentulous areas were exposed with a midcrestal incision, in association with mesial and distal vertical releasing incisions, followed by the elevation of a full-thickness mucoperiosteal flap. Any remnants of soft tissues overlying the recipient sites were carefully removed. The cortex of the residual bone in the recipient site was perforated with a 1-mm round bur to encourage bleeding and accelerate revascularization of the grafts. The atrophic area was then reconstructed with vertical and horizontal onlay FFB grafts, with care taken to leave only the cortical component of the allogeneic ilium. Careful modeling of the blocks was performed to optimize contact with the recipient site and to obtain the correct morphology of the reconstructed alveolar crest. The blocks were fixed with titanium microscrews, 1.5 mm in diameter and 8 to 16 mm in length, according to surgical needs (Synthes). Any residual space between the recipient site and the blocks, as well as among the blocks, was carefully packed with particulated allogeneic bone to prevent connective tissue ingrowth during healing, as this might compromise the integration of the grafts into the recipient bed. The grafted sites were covered with resorbable collagen membranes (Bio-Gide, Geistlich Biomaterials) to stabilize the bone chips. Before suturing, periosteal releasing incisions were performed to allow for tension-free and watertight closure of the flaps. In patients with severely atrophic edentulous maxillae, the reconstruction was associated with a bilateral sinus grafting procedure with a lateral approach, as described by Boyne and James.43 Briefly, a bony window was outlined in the lateral aspect of the maxilla, the sinus membrane was elevated, and the void created between the floor of the sinus and the elevated membrane was filled with particulated corticocancellous allogeneic bone chips.

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Chiapasco et al

Antibiotic therapy (2 g ceftriaxone per day for the following 7 days) was prescribed for all patients, and postoperative instructions included a liquid/soft diet for 2 weeks, careful oral hygiene with a toothbrush on the residual dentition, and 0.2% chlorhexidine mouthrinses until suture removal, which was performed 12 to 14 days after the reconstruction. Eight to 12 mg dexamethasone was injected intravenously at the time of general anesthesia induction and then continued for the following 2 to 3 days (8 mg the first 2 days after surgery and 4 mg the last day) to reduce postoperative swelling and consequent discomfort. Nonsteroidal analgesics (100 mg ketoprofen) were administered intravenously until patients left the hospital and continued orally in case of persistent pain. Patients were not allowed to wear any removable prostheses that contacted the reconstructed ridges for a minimum of 8 weeks after surgery. After this period, and until implants were placed, patients could wear prostheses relined with soft materials for esthetic reasons only, and they were prohibited from using them to chew hard food.

Implant Placement

Five to seven months after reconstruction, a second surgical session was scheduled to remove the microscrews and place implants in the reconstructed areas. The lengths and diameters of the implants were chosen according to the bone volume available at each implant site and to meet prosthetic needs. A surgical template based on the ideal wax-up of the missing dentition was fabricated for each patient and then used to determine the correct implant positions. The surgical procedure, performed under local or general anesthesia according to the number of implants to be placed and patient characteristics, started with the elevation of a full-thickness flap, following the same incision line used for the reconstructive surgery, to access the reconstructed areas. Any titanium microscrews that interfered with implant placement were removed. Any other remaining screws were left in place to avoid unnecessary exposure of the graft. Implant sites were prepared under the guidance of the surgical templates and implants placed according to a standard procedure. All implants were left to integrate in a submerged protocol. Patients were discharged with the same postoperative instructions they had received after reconstruction.

Prosthetic Loading

Four to 6 months after placement, implants were uncovered and healing abutments connected. One to 2 months later, the prosthetic rehabilitation was inserted. Patients were then scheduled for periodic clinical and radiographic follow-up examinations.

Follow-up Procedures

Postoperative follow-up of patients and implants included clinical and radiographic examinations. Panoramic and intraoral radiographs were taken immediately after the reconstructive procedure, at the time of implant placement, at the time of prosthetic loading, and annually thereafter. The following parameters were evaluated: (1) reconstructive procedure outcome, (2) peri-implant bone level changes (as measured on radiographs), (3) complications before and after implant placement, and (4) implant survival rate. The outcome of the reconstructive procedures was evaluated in terms of survival of the bone transplants and related complications, if present. Graft resorption before implant placement was measured with a periodontal probe mesial and distal to each microscrew used for graft fixation at the time of screw removal. The distance between the head of the screw and the first bone-to-screw contact was measured. The initial distance between the screw head and the bone graft surface was considered equal to 0 mm at the end of the reconstructive procedure, as the screw heads were always at the level of the most superficial part of the bone blocks. Values were rounded to the nearest millimeter. Peri-implant bone level changes were recorded by two independent investigators, who compared panoramic radiographs taken immediately after implant placement, at the time of prosthetic loading, and annually thereafter. Bone level changes were evaluated mesial and distal to each implant; the distance between the top of implant head shoulder and the most coronal level of direct boneto-implant contact was measured, and measurements were recorded to the nearest 0.5 mm. Dimensional distortion between the different radiographs was corrected by comparison with the actual dimensions of implants. The measurements were performed on an Apple MacBook Pro computer. For image analysis and measurements, all panoramic radiographs were acquired with a Nikon D-90 digital camera (Nikon) and analyzed with dedicated software (ImageJ, v. 1.38, U.S. National Institutes of Health). Again, the distance between the implant shoulder and the most coronal bone-to-implant contact at the time of implant placement was considered as the baseline for the following measurements. For each implant, a mathematical mean between the measurements on the mesial and distal aspects was calculated to obtain a mean resorption value. Measurements were made on panoramic radiographs, because in the majority of patients affected by severe atrophy, it was difficult to use intraoral radiographs because of the presence of a reduced lingual sulcus depth or a “flat” palate.

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Chiapasco et al

Table 1  Demographic and Clinical Data of Treated Patients Patient no.  1  2

Date of surgery Mar 2010 Apr 2010

Date of implant placement Sep 2010 Sep 2010

Type of reconstruction V+H V+H+S

Apr 2010 Apr 2010 Jun 2010

Oct 2010 Oct 2010 Dec 2010

V+H V+H+S V+H+S

Jun 2010 Jul 2010 Sep 2010

Nov 2010 Dec 2010 Mar 2011

V+H V+H+S V+H

Mand (P), 47–44, 34–37

Sep 2010

Mar 2011

V+H

M F F

Max (T) Max (P), 16–13 Max (T) Mand (P), 46–47, 35–37

Oct 2010 Oct 2010 Nov 2010

Apr 2011 Apr 2011 May 2011

V+H+S V+H+S V+H+S

74 49

F F

Nov 2010 Dec 2010

May 2011 May 2011

V+H+S V+H

15 16

69 53

F F

Dec 2010 Dec 2010

May 2011 May 2011

V+H V+H+S

17

53

F

Max (T) Max (P), 17–14 Mand (P), 34-36 Max (P), 15–25 Max (T) Mand (P), 47-45 Mand (P), 47–45, 34–37

Mar 2011

Jul 2011

V+H

18

54

M

Max (P), 16–14, 24–27

Apr 2011

Oct 2011

V+H+S

19

64

F

Mand (P), 47–45, 35–37

Apr 2011

Oct 2011

V+H

Age (y) 23 56

Sex F F

 3  4  5

63 56 48

F F F

 6  7  8

85 53 55

F F F

Site of atrophy Mand (P), 43–33 Max (T) Mand (T) Max (P), 16–22 Max (T) Max (T) Mand (T) Mand (T) Max (T) Mand (P), 47–45, 35–37

 9

72

F

10 11 12

61 56 50

13 14

Maximum vertical bone gain 6 mm 12 mm (max) 9 mm (mand) 6 mm 13 mm 11 mm (max) 10 mm (mand) 12 mm 14 mm 7 mm (right mand) 6 mm (left mand) 8 mm( right mand) 6 mm ( left mand) 12 mm 10 mm 13 mm (max) 7 mm (right mand) 9 mm (left mand) 13 mm 11 mm (max) 8 mm (mand) 10 mm 13 mm (max) 8 mm (mand) 8 mm (right mand) 8 mm (left mand) 7 mm (right max) 6 mm (left max) 7 mm (right mand) 9 mm (left mand)

H = horizontal; P = partially edentulous; S = sinus elevation; T = totally edentulous; V = vertical. FDI tooth-numbering system used.

Table 2  Incidence of Graft Complications, Treatment, and Outcome Patient no.  1  2  3  4  5  6

Prior to implant placement Time, area Management – – Exposure at 4 wk, Cur, perf buccal of 25–26 – – – – – – – –

Healed? – Yes

Between implant placement and abutment connection Time, area Management Healed? – – – – – –

– – – –

– – – –

– – –

– – –

 7













 8  9 10

– – –

– – –

– – –

– – –

– – –

– – –

14







– – Cur, perf, p. rem – – Cur, perf, p. rem Cur, t. rem

– – Yes

11 12 13

Yes

15 16

Resorption at 21 wk, 13–23 Exposure at 14 wk, buccal of 24–25 – Exposure at 20 wk, 24–27 –

Cur, p. rem Cur, perf

Yes Yes

– – Exposure at 3 wk, buccal of 12–13 – – Exposure at 11 wk, buccal of 24–26 Exposure at 6 wk, buccal of 14–17 – –

– –

– –

– t. rem –

– Yes –

Exposure at 24 wk, 36–37 – –

Cur, perf – –

Yes – –

17 18 19

– – Yes

Cur = local curettage; perf = perforations; p. rem = removal of partial bone graft; t. rem = removal of total bone graft; resorption = relevant resorption of the graft. FDI tooth numbers used.

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Chiapasco et al

Max 0 8

No. of implants Mand Lost 5 1 3 1

Date of loading Feb 2011 Feb 2011

Follow-up (mo) 32 32

4 8 8

0 0 4

0 0 1

Mar 2011 Apr 2011 Apr 2011

31 30 30

0 8 0

4 0 5

0 0 0

May 2011 Apr 2011 Jul 2011

29 29 27

0

7

0

Aug 2011

26

6 3 8

0 0 5

0 1 0

Sep 2011 Sep 2011 Oct 2011

25 25 25

6 3

0 2

3 3

Sep 2011 Oct 2011

25 24

3 7

0 2

0 0

Nov 2011 Nov 2011

23 22

0

4

0

Nov 2011

22

0

0







0

4

0

Feb 2012

20

After implant loading Time, area Management – – – – – Exposure at 60 wk, buccal of 24–26 – Exposure with resorption at 20 wk, 34–32 Exposure at 23 wk, palatal of 14–16 Exposure at 25 wk, palatal of 24–25 – Exposure at 20 wk, buccal of 34–35 Exposure at 10 wk, buccal of 14–15 Exposure at 96 wk, buccal of 12 Exposure at 24 wk, buccal of 14–16 Exposure at 13 wk, buccal of 24–25 Exposure at 52 wk, buccal of 24–26

Healed? – –

– Cur, perf – Cur

– No – Yes

Cur, perf

No

– Cur, perf Cur, perf

– No No Yes Yes Yes

– Exposure at 8 wk, buccal of 24–25

Cur, t. rem Cur, perf Cur, perf, p. rem Cur, perf, p. rem – Cur, perf

Exposure at 52 wk, buccal of 36–37 – –

Cur, p. rem – –

No – –

Exposure at 50 wk, buccal of 34–35

No – No

Clinical examinations were performed to evaluate the presence or absence of dehiscences, bone graft exposure/sequestration, and infection. Criteria for implant survival included: (1) absence of persistent pain or dysesthesia, (2) absence of periimplant infection with suppuration, (3) absence of mobility, and (4) absence of continuous peri-implant radiolucency.

RESULTS Nineteen patients (17 women and 2 men) aged between 23 and 85 years (mean age: 57 years; median age: 56 years) participated in the study (Table 1). The vertical bone gain at the end of each reconstructive procedure ranged from 6 to 14 mm (Table 1). A total of 117 implants were placed (AstraTech and XiVE implants, Dentsply; Straumann Implant System, Institut Straumann): 72 implants were placed in the maxilla and 45 in the mandible. The length of hospitalization of patients after the reconstructive procedure was 1 day for 12 patients and 2 days for 7 patients. Postoperative recovery until suture removal was uneventful in all patients. Tolerable discomfort was represented mainly by relevant swelling and visible face hematomas, which disappeared completely within 3 weeks after reconstructive surgery. However, at different times after suture removal, 14 patients experienced dehiscences (Table 2). Following local curettage and perforations, the dehiscence healed in only one patient without loss of the implants (#12), while the remaining 13 patients experienced partial or total sequestration/loss of the grafted bone, loss of one or more implants, and/or persistence of dehiscences surrounding the implants (albeit limited) in association with a variable rate of peri-implant bone resorption, although implants and related prosthetic restorations were still in function at the end of the observation period. Two patients (#1, #5) lost one implant each before loading, without any clinically detectable dehiscence or infection. However, the prosthetic rehabilitation was completed (Table 2). Only three patients (#3, #8, #19) experienced no complications during the followup period (Table 2). The mean resorption of the grafts, which appeared clinically integrated at the time of microscrew removal and implant placement, was 0.98 mm (range, 0 to 5 mm; standard deviation [SD] 0.77 mm). All data (frequency distribution, medians, and interquartile ranges) related to graft resorption are reported in Table 3. After the start of prosthetic loading, patients were followed from 20 to 32 months, with a mean of 27 months. Overall, 10 of the 117 implants were removed The International Journal of Oral & Maxillofacial Implants 455

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Chiapasco et al

Table 3  Data on Graft Resorption Before Implant Placement

Table 4  Life Table Analysis (Standard Actuarial Method) of Implants Placed

Distribution of No. (%) graft resorption of sites 0 mm 51 (25.6%) 1 mm 107 (53.8%) 2 mm 35 (17.6%) 3 mm 4 (2%) > 4 mm 2 (1%) Graft resorption (mm) Mean (SD) 0.98 (0.77) Median 1 First quartile 0 Third quartile 1 Minimum 0 Maximum 4

Observation period Placement to loading Loading to 1 y 1 y to 2 y

Surveyed 117 111 111

Dropouts 0 0 58

Removed 6 0 4

Surviving 111 111 49

Cumulative survival rate 94.87% 94.87% 90.24%

Dropouts = implants not reaching the end of the observation period.

Table 5   Data on Peri-implant Bone Resorption Distribution of peri-implant bone At loading (111 resorption implants) 0 mm 1 (0.9%) < 0.9 mm 51 (46%) 1–1.9 mm 47 (42.3%) 2–2.9 mm 3 (2.7%) 3–3.9 mm 3 (2.7%) > 4 mm 6 (5.4%) Peri-implant bone resorption (mm) Mean (SD) 1.21 (1.05) Median 1 First quartile 0.75 Third quartile 1.1 Minimum 0 Maximum 6

(6 before loading and 4 at different times after the start of loading). The cumulative survival rate for the implants was therefore 90.2% (Table 4). The mean bone resorption around the surviving implants at the time of prosthetic loading was 1.21 mm (range, 0 to 6 mm; SD 1.05 mm). One and 2 years after the start of prosthetic loading, these values were 1.55 mm (range, 0 to 8 mm; SD 1.57 mm) and 1.93 mm (range, 1 to 9 mm; SD 1.38 mm), respectively. Descriptive statistics related to peri-implant bone resorption (mean, median, frequency distribution, interquartile ranges) are reported in Table 5. Two clinical cases are presented in Figs 1 and 2.

DISCUSSION In case of severe atrophy of partially or totally edentulous patients (class V and VI according to Cawood and Howell3), in whom extremely reduced bone volume is very often associated with unfavorable vertical, anteroposterior, and transverse maxillomandibular relationships, the reconstruction of the alveolar ridge with bone grafts is a very well-documented option to allow the correction of large defects and to enable adequate implant-supported prosthetic restoration.9–11,44 Whenever AB taken from intraoral sites is insufficient, extraoral sites are needed, such as the calvarium and/or the

After 1 y (111 implants) 1 (0.9%) 23 (20.7 %) 66 (59.5%) 11 (9.9%) 1 (0.9%) 9 (8.1%)

After 2 y (49 implants) 0 0 33 (67.3%) 11 (22.5%) 2 (4.1%) 3 (6.1%)

1.55 (1.57) 1 1 1.5 0 8

1.93 (1.38) 1.5 1.25 2.25 1 9

iliac crest. If patients refuse the calvarium as a donor site, the anterior ilium represents a reliable source of bone, thanks to the relevant quantities available. Several publications with relatively long follow-up periods demonstrated that the clinical outcome of both grafting and the implants placed in the reconstructed areas are very satisfying, with survival rates of implants and the related prostheses similar to those obtained in case of implants placed in native, nonreconstructed bone.6,7,16,44–47 The authors themselves have used the anterior ilium for years and reported very good results in the treatment of severely atrophic partially or totally edentulous jaws.8–10,12,48 However, the morbidity related to the harvesting procedure is relevant. This typically comprises pain/ discomfort in ambulation (albeit transient in the vast majority of cases), which may last from a few days up to several weeks after the surgical procedure.9,10,15,16,18 The use of FFB in oral reconstructive surgery has been proposed to overcome this problem. However, outcomes reported in the literature are contradictory, as some authors claimed apparently good results,23–30 while others reported inconsistent results.31–34 This controversy may be related to several factors. There is extreme heterogenicity in site, type, and extent of the reconstruction (including small defects, sinus floor elevation with FFB blocks, inlay grafting, horizontal onlay grafts, etc). In addition, studies have used different

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Chiapasco et al

Figs 1a and 1b  Preoperative imaging showing extreme atrophy of the edentulous maxilla with expanded maxillary sinuses. Together with the severely atrophied posterior mandible, this renders implant placement impossible or inadequate from a prosthetic point of view.

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b

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Figs 1c and 1d   Preoperative clinical situation showing the extreme atrophy of the edentulous maxilla with unfavorable vertical, anteroposterior, and transverse maxillomandibular relationships.

Fig 1e   Three-dimensional reconstruction of the maxilla with vertical and horizontal onlay FFB grafts in association with bilateral sinus grafting. Fig 1f  Watertight and tension-free sutures were placed at the end of the reconstruction.

Figs 1g and 1h   Postoperative radiographic and clinical views showing an uneventful recovery and appropriate reconstruction of the maxilla and the posterior mandible.

Fig 1i  Clinical situation at the time of implant placement showing 2 mm of bone resorption around one screw and no resorption around the remaining screws. Fig 1j   Placement of eight implants in the reconstructed maxilla.

Fig 1k   Radiographic control following implant placement in both the maxilla and mandible.

Figs 1l and 1m   Clinical and radiographic views of the final result, 2 years after the start of prosthetic loading.

The International Journal of Oral & Maxillofacial Implants 457 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.

Chiapasco et al

Figs 2a and 2b  Preoperative imaging showing extreme atrophy of the edentulous maxilla with expanded maxillary sinuses. This renders implant placement impossible.

a

b Figs 2c and 2d   Postoperative radiographic and clinical views showing an uneventful recovery and appropriate reconstruction of the maxilla (in the meantime, four implants were placed in the interforaminal area of the edentulous mandible with no reconstruction).

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d Figs 2e and 2f   Clinical and radiographic views at 1 year after the start of prosthetic loading.

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f

Figs 2g and 2h   Two years after the start of prosthetic loading, a dehiscence occurred Fig 2i   Radiographic view at 2 years after around the implant in the right lateral incisor area. The prosthesis was removed, and a the start of prosthetic loading showing sequestrated, nonvital bone fragment was removed. that, despite the bone fragment removal, the initially placed implants and prosthesis are still in function, with limited periimplant bone resorption.

lengths of follow-up; study periods are often short, sometimes not even lasting to implant loading and the definitive prosthetic restoration.23,32–34 This variability makes analysis of the data difficult. Despite the relatively limited number of patients and the relatively short follow-up, the results of the present study, which includes only onlay FFB iliac grafts for the simultaneous vertical and horizontal reconstruction of complex defects, including a relevant number of edentulous arches with extreme atrophy, showed a high complication rate. Only three patients (#3, #8, #19) did not experience any complications during the follow-up period, two patients (#1, #5) lost one implant each before loading without any clinically

detectable dehiscence or infection, and 14 patients experienced complications such as dehiscences and graft sequestrations/loss. This rate of complications has not been reported in studies of the use of autogenous iliac bone blocks to restore complex three-dimensional defects with a relevant vertical component.4,6–8,12,16,46 Dehiscences were followed by healing (after local curettage and bone perforations) without loss of implants in only one patient (#12), while the remaining 13 patients experienced partial or total loss of the grafted bone, loss of one or more implants, and/or persistence of dehiscences surrounding the implants (albeit limited), in association with a variable rate of peri-implant bone resorption. Problems arose most frequently after implant

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Chiapasco et al

placement and abutment connection, raising doubts regarding the reliability of FFB for the reconstruction of severely atrophic edentulous arches. The high incidence and persistence of bone exposures around implants, as well as the removal of fragments of nonvital bone around and between implants, may increase doubts regarding the long-term survival of implants in reconstructed bone and the related prosthetic restorations. Strangely enough, these results are in contrast with a previous histologic and histomorphometric study recently published by the same group of authors.49 In that preliminary study, bone specimens were obtained with a trephine bur during implant site preparation in partially or totally edentulous patients reconstructed with iliac FFB or AB grafts. Although patients treated with FFB showed slower bone remodeling and revascularization, at the time of implant placement, the FFB grafts appeared well integrated and normal bleeding was observed from the prepared implant sites, apparently demonstrating good revascularization of the grafts. These preliminary findings encouraged the authors to consider FFB as a reliable grafting material. Yet, as already stated, a high incidence of bone exposures after abutment connection and the start of prosthetic loading was observed, together with the presence of necrotic bone on the surface of the FFB grafts. These findings are quite difficult to explain. The authors can only speculate that the grafted FFB had not yet completely revascularized (particularly in its outer part) at the time of implant placement and even at the time of implant loading, which took place 1 year after reconstruction. Because of this insufficient revascularization (both endosteal and periosteal), the grafts may have experienced a further reduction in blood supply because of the need to raise a flap and the surgical trauma during implant placement. These events may be responsible for the high incidence of spontaneous dehiscences and bone exposures after implant placement. Insufficient vascularization and dehiscences contribute to a risky condition for both grafts and implants (7 of 18 patients treated with FFB grafts and implants presented with apparently integrated implants supporting fixed prostheses, but with peri-implant soft tissue dehiscences, leading to an unpredictable prognosis). Histologic analysis of the removed FFB bone fragments showed extremely limited or absent vital cells, and the results will be presented in another paper. These findings seem to confirm the less than ideal results reported by some authors,31–34 while they are in contrast with the positive results reported in other studies.23–30 Mean peri-implant bone resorption seems to be higher in comparison with data reported for implants placed in jaws reconstructed with autogenous iliac grafts.6–10,16 These results have been also confirmed by studies comparing AB and FFB in which the

latter material demonstrated a less favorable outcome in terms of initial bone gain maintenance and incidence of complications.31–34 Furthermore, it is worth noting that an in vitro study38 demonstrated that FFB, despite the freezing process at –80°C and after at least 6 months of quarantine in a bone bank, maintains vital cells. In fact, it has been shown that osteoblast-related cells can be grown in vitro from FFB specimens. The cells derived from frozen grafts were morphologically indistinguishable from those grown out of freshly harvested trabecular bone; the authors concluded that “a frozen autograft will resemble an allograft. The detrimental effects of preservation and the immune response to the allografts contribute to failure of these grafts in vivo.50 In allograft recipients, growth of donor cells may be one aspect of a whole spectrum of immunologic reactions occurring following implantation, which may lead to a localized host/graft immune response and explain the inconsistent behavior of allografts.”38p29 Therefore, at present, FFB should be proposed and used as an alternative to autogenous bone with caution.

CONCLUSION Within the limits of this study with a small number of patients and a relatively short follow-up period, the results seem to indicate that: (1) the reconstruction of severely atrophic edentulous ridges using iliac fresh frozen bone onlay grafts is associated with a relevant incidence of soft tissue dehiscences and graft exposures, resulting in partial or total loss of the grafts (14 of 19 patients); (2) the survival rate of implants at the end of the follow-up period was 90.2%, but the persistence of dehiscences with exposure of the peri-implant grafted bone might negatively influence the long-term survival of implants; and (3) the immunologic reactions reported in the literature, which may lead to a localized host/graft immune response and rejection, seem to enforce the assertion that, at present, fresh frozen allogeneic iliac grafts should be used with caution.

ACKNOWLEDGMENTS The authors reported no conflicts of interest related to this study.

REFERENCES   1. Esposito M, Murray-Curtis L, Grusovin MG, Coulthard P, Worthington HV. Interventions for replacing missing teeth: Different types of dental implants. Cochrane Database Syst Rev 2007:CD003815.

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Chiapasco et al

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460 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.

Clinical outcome of the use of fresh frozen allogeneic bone grafts for the reconstruction of severely resorbed alveolar ridges: preliminary results of a prospective study.

The objectives of this study were to evaluate: (1) the clinical outcome of fresh frozen human allogeneic bone grafts (FFB) used for the reconstruction...
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