original article

J. Stomat. Occ. Med. (2010) 3: 8994 DOI 10.1007/s12548-010-0050-8 Printed in Austria Springer-Verlag 2010

Alveolar ridge augmentation with calvaria, iliac crest and mandibular autologous bone grafts: a retrospective study on 261 implants
R. Cenzi1 , L. Arduin2 , I. Zollino2 , C. Casadio2 , A. Scarano3 , F. Carinci2
1 2

Department of Maxillofacial Surgery, Civil Hospital, Rovigo, Italy Maxillofacial Surgery, University of Ferrara, Ferrara, Italy 3 Dental Clinic, University of Pescara-Chieti, Chieti, Italy Received February 24, 2010; Accepted April 10, 2010

Purpose: In the last decade, several investigators have reported that autografts can be used to restore alveolar volume prior to implant insertion successfully. However, no report is available comparing implant inserted into calvarial, mandibular and iliac crest bone autografts. Materials and methods: A retrospective study on 261 implants inserted in 42 patients was performed. Several variables related to patients, anatomic sites, implants and grafts were investigated. Implants failure and peri-implant bone resorption were considered as predictor of clinical outcome. The KaplanMeier algorithm and Cox regression were then performed to detect those variables statistically associated with the clinical outcome. Results: A total of 261 implants were inserted: 89 (34.1%) into the mandible and 172 (65.9%) into the maxilla. Nine different implant types were used. Implant length and diameter ranged from 8 to 15 mm and from 3.5 to 6.0 mm, respectively. Implants were inserted to replace 42 incisors, 32 cuspids, 77 premolars and 110 molars. The mean post-loading follow-up was 32 months. No implant was lost (i.e. survival rate SVR 100%) and no differences were detected amongst the studied variables. On the contrary, crestal bone resorption correlates with jaws site and implant type. Conclusion: Implants can be inserted in autografted jaws successfully although a higher resorption could be expected in the molar region. In addition the type of implant can have an impact on clinical outcome. Keywords: KaplanMeier algorithm, Cox regression, autograft, implant, rehabilitation

placement of implants [1]. Bone availability is the key for successful placement of endosseus implants and the anatomical limitations of residual alveolar bone can cause less than ideal sites with an aesthetic and functional compromise [2]. Increasing the width and height of the residual alveolar bone by grafting is necessary for implant and prosthesis support. The use of osseointegrated dental implants to support prostheses appears to restore normal functional stress to the grafted bone, which protects the graft from the certain and rapid resorption observed with tissue-supported prostheses [3]. Materials previously used for grafting include autogenous bone, allogenic bone and alloplastic materials [4]. Despite the desire for an alternative to autogenous bone to simplify the surgical procedure and eliminate donor site surgery and morbidity, autogenous bone grafts remain the most predictable and successful grafting material available [5]. It can be harvested in multiple forms (particles, strips and blocks), it is available from either calvaria, iliac crest, mandible. It has no adverse antigenicity because it originates from the patient, and it is extremely reliable [3]. The donor site for the graft is based on the size of the defect to be restored. Large grafts must be harvested from the temporo-parietal cranial area or from the anterior or posterior ileum, and smaller grafts can be harvested from the symphysis [5, 6]. Due to a limited number of reports focussed on the clinical outcome of implants inserted in autogenous bone grafts [3], a retrospective study was planned to address this question. In fact there have been numerous studies of autogenous bone grafts and implants [7].

Introduction
Resorption of the edentulous maxilla results in progressive loss of volume and quality of bone available to accept the

Materials and methods

Study design/sample To address the research purpose, the investigators designed a retrospective cohort study. The study population was composed of patients grafted with autologous bone presenting to
Alveolar ridge augmentation 2/2010

Correspondence: Prof. Francesco Carinci, M.D., Chair of Maxillofacial Surgery, Arcispedale S. Anna, Corso Giovecca 203, 44100 Ferrara, Italy. E-mail: crc@unife.it

J. Stomat. Occ. Med. Springer-Verlag

89

original article

the Maxillofacial Surgery, Rovigo, Italy, for evaluation and implant treatment between January 1994 and July 2008. Subjects were screened according to the following inclusion criteria: controlled oral hygiene, the absence of any lesions in the oral cavity, previous autologous bone grafting derived from calvaria, mandible or iliac crest; in addition, the patients had to agree to participate in a post-operative checkup program. The exclusion criteria were as follows: bruxism, smoking more than 20 cigarettes/day and consumption of more than 2 glass of wine per day, localized radiation therapy of the oral cavity, antitumour chemotherapy, liver, blood and kidney diseases, immunosupressed patients, patients taking corticosteroids, pregnant women, inammatory and autoimmune diseases of the oral cavity. Graft material All patients underwent the same surgical protocol. An antimicrobial therapy was administrated with 3 g Ampicillina (Unasyn, Pzer Srl, Italy) for 6 days starting intraoperatively. Local anaesthesia was induced by inltration with Mepicain 2% with Adrenalin 1:100.00 and post-surgical analgesic treatment was performed with 30 mg Ketorolac Tromentamina (Toradol, Recordati Spa, Italy) or 10 mg Paracetamol (Perfalgan, Bristol-Myers Squibb Srl, Italy). Oral hygiene instructions were provided. The calvarial harvesting was performed by splitting the parietal diploe. Six to eight bone sticks with dimensions of approximately 30/40 mm10 mm were delimited by using a drill under abundant washing to cool the saw. The delimitation of splints was done by using an oscillating saw that cuts the calvaria at partial thickness, and then the detachment of grafts was performed by using a saw with a small blade at an angle of approximately 30 , and chisels. The occasional discovery of small areas of dura mater did not create any complications and there was never any leaking of liquor; however, bone dust with brin glue always was placed to protect areas of exposed dura. The calvarial sampling area was then protected with titanium mesh xed with micro screws. The mandible was exposed by a degloving technique through a gum-splitting incision. Symphyseal osteotomies were performed on the mandible in monocortical fashion, using a reciprocating saw with 5 mm safety margins caudal to the expected position of the mandibular dentition, anterior to the position of the mental foramen and cephalad to the inferior border of the mandible. Once the osteotomies were completed, a midline osteotomy was created for facilitated elevation of the graft. The harvest was completed by using thin chisels to elevate blocks. Bone curettes were then used to remove any remaining cancellous bone from the osteotomy site. In the donor site defect a titanium mesh was positionated xed with micro screws. In iliac crest harvesting technique, the incision started 1 cm behind the anterior superior iliac spine and continued posteriorly, following the iliac crest (for aesthetic reasons and, to avoid possible irritation of the scar from tight-tting clothes, the skin was stretched in craniomedial direction over the iliac crest before the incision was made). The incision was carried down sharply to the mid-crest, dividing the musculotendinuos aponeurosis of the tensor muscle of the fascia lata and the

Tab. 1: Cross-tabulation that matches form of graft, location and type of bone augmentation Form of graft
En-block (241)

Location
Left mandible (39) Right mandible (48) Left maxilla (86) Right maxilla (88)

Bone augmentation
None (20) Onlay (49) Inlay (175) Veener (17)

oblique abdominal muscles without transecting muscle bres. The medial cortical plate of ilium bone was exposed directly by reecting the iliac muscle subperiosteally and the donator site was exposed with a retractor. A cortico-cancellous bone block was harvested by making two horizontal and two vertical cuts using saws. The superior horizontal cut was made midcrestal. The inferior horizontal cut was made with a curve reciprocal saw. After the removal of the cortico-cancellous bone block from the inner table, additional cancellous bone was harvested. Bone was smoothed, Spongostan (Ferrosan A/S, Soeborg, Denmark) placed in the bony cavity, a suction drain placed in the operation eld and the wound closed in layers. After making a crestal incision a mucoperiostal ap was elevated. The grafts were positionated as an inlay, onlay or veneer (Table 1). Sutures were removed 10 days after surgery. After 6 month from surgery, implant insertion was provided. Implant surgery All patients underwent the same surgical protocol. An antimicrobial prophylaxis was administrated with 500 mg Amoxycillin twice a day for 5 days, starting 1 hour before surgery. Local anaesthesia was induced by inltration with Articaine/Epinephrine and post-surgical analgesic treatment was performed with 100 mg Nimesulid twice daily for 3 days. Oral hygiene instructions were provided. Implants were inserted in autogenous bone grafts after a 6-month healing period and were loaded after an additional 6 months. After a crestal incision a mucoperiosteal ap was elevated. Implants were inserted according to the procedures recommended. The implant platform was positioned at the alveolar crest level. Sutures were removed 14 days after surgery. After 24 weeks from the implant insertion, the provisional prosthesis was provided and the nal restoration was usually delivered within an additional 8 weeks. All patients were included in a strict hygiene recall. Variables Several variables are investigated: demographic (age and gender), anatomic (upper/lower jaws and tooth site), types of graft (inlay, onlay, veneer and combinations) and implant (length and diameter and type). Primary and secondary predictors of clinical outcome were used. The primary predictor is the presence/absence of the implant at the end of the observation period. It is dened as the survival rate (i.e. SVR), which is the total number of implants still in place at the end of the follow-up period.
Springer-Verlag J. Stomat. Occ. Med.

90

2/2010

Alveolar ridge augmentation

original article

The second predictor of outcome is the peri-implant bone resorption. It is dened as the implant success rate (SCR) and is evaluated according to the absence of persisting peri-implant bone resorption greater than 1.5 mm during the rst year of loading and 0.2 mm/years during the following years [8].

Data collection methods and summary of operative methods Before surgery, radiographic examinations were done with the use of orthopantomographs (Figs. 14).
Fig. 4: OPG at the end of the follow-up period

In each patient peri-implant crestal bone levels were evaluated by the calibrated examination of orthopantomograph X-rays. Measurements were recorded after surgery and at the end of the follow-up period. The measurements were carried out mesially and distally to each implant, calculating the distance between the implants platform and the most coronal point of contact between the bone and the implant.

Tab. 2: Delta IAJ medians were stratied according to the variables of interest Variable
Fig. 1: Pre-surgical ortopantomography (OPG)

Delta IAJ medians in parenthesis

None (1.3) Inlay (1.5) Onlay (1.5) Veener (1.8) None (1.5) Calvaria (1.4) Iliac crest (2.0) Mandible (1.0) Right maxilla (1.3) Left maxilla (1.4) Right mandible (1.8) Left mandible (1.5) Incisors (1.2) Cuspids (1.3) Pre-molars (1.3) Molars (1.8) L < 13 (1.5) L 13 (1.5) L > 13 (1.5) D < 3.75 (1.9) D 3.75 (1.4) D > 3.75 (1.3) Bi-Implant (1.8) P1 H (1.5) Biomax (1.5) Branemark (2.3) Hexa (0.5) Geass (1.6) Neoss (0.8) Camlog (1.6) Screwvent (0.2)

Type of graft

Type of bone

Upper/lower jaw

Implant site

Fig. 2: OPG showing grafts

Length

Diameter

Implant type

Fig. 3: OPG showing the provisional restoration

J. Stomat. Occ. Med. Springer-Verlag

Alveolar ridge augmentation

2/2010

91

original article

The bone level recorded just after the surgical insertion of the implant was the reference point for the following measurements. The measurement was rounded off to the nearest 0.1 mm. A peak Scale Loupe with a magnifying factor of seven times and a scale graduated in 0.1 mm was used. The difference between the implant-abutment junction and the bone crestal level was dened as the Implant-Abutment Junction (IAJ) and calculated at the time of operation and during the follow-up. The delta IAJ is the difference between the IAJ at the last check-up and the IAJ recorded just after the operation. Delta IAJ medians were stratied according to the variables of interest (Table 2). Peri-implant probing was not performed because controversy still exists regarding the correlation between probing depth and implant success rates [9, 10]. Data analysis Disease-specic survival curves were calculated according to the product-limit method (KaplanMeier algorithm) [11]. Time zero was dened as the date of the implant's insertion. Implants which are still in place (or have a crestal bone resorption value lower than the cut-off value) were included in the total number at risk of loss only up to the time of their last follow-up. Therefore the survival rate only changed when implant loss (or cut-off overcome) occurred. The calculated survival rate was the maximum estimate of the true survival curve. Log rank testing was used to compare survival/success curves, generated by stratications for a variable of interest. Cox regression analysis was then applied to determine the single contribution of covariates on the survival/success rate. Cox regression analysis compares survival/success data whilst taking the statistical value of independent variables into account, such as age and sex, on the whether or not, that an event (i.e. implant loss, crestal bone resorption value overcome) is likely to occur. If the associated probability was less than 5% (p < 05), the difference was considered statistically signicant. In the process of doing the regression analysis, odds ratio and 95% condence bounds were calculated. Condence bounds did not have to include the value 1 [12]. Stepwise Cox analysis allowed us to detect the variables most associated to implant survival and/or clinical success.

Switzerland), 12 Hexa (Biotec srl, Vicenza, Italy), 13 Geass (Geass srl, Udine, Italy), 18 Neoss (Neoss srl, Milan, Italy), 8 Camlog (Camlog Biotechnologies AG, Basel Switzerland), 9 Screwvent (Sweden & Martina srl, Padua, Italy). Implant length and diameter ranged from 8 to 15 mm and from 3.5 to 6.0 mm respectively. There were 93 standard length xtures (i.e. 13 mm), 140 short and 28 long implants. There were 182 standard diameter xtures (i.e. 3.75 mm), 40 narrow and 39 wide implants. Implants were inserted to replace 42 incisors, 32 cuspids, 77 premolars and 110 molars. Seventeen, 49 and 175 implants were inserted in mandibular, iliac crest and calvarial bone grafts, respectively. Twenty implants were inserted in native bone, 175 in inlay, 49 in onlay, 17 in veneer. The overall mean bone resorption around implants was 1.5 mm, whereas the mean bone resorption was 1.5, 1.4, 2.0 and 1.0 mm for native bone, calvarial, iliac crest and mandibular graft, respectively. No implant was lost in the post-operative period. Kaplan Meier algorithm demonstrates that site of graft (i.e. maxilla or mandible), type of graft, implant site (i.e. incisors, cuspid, premolar and molar) and type of implant were statistically different (Table 3). Table 4 conrmed that implant site (molars 1.8 mm) and type of xture (B-Implant 1.8 mm and Branemark 2.3 mm) correlated with a statistically signicant higher delta IAJ (i.e. deeper crestal bone loss) and thus a worst clinical outcome.

Tab. 3: Univariate analysis: type of graft is inlay, onlay, veneer and combinations; type of bone is calvaria, iliac crest and mandible; implant site is incisor, cuspid, pre and molars Variable
Type of graft Type of bone Upper/lower jaw Implant site Length

Log rank
73.78 3.81 7.13 19.09 0.61 5.67 93.75

Degree of freedom
7 3 1 3 2 2 8

Signicance
0.001 0.283 0.008 0.001 0.739 0.059 0.001

Results
Forty-two patients (30 females and 12 males) with a median age of 45.8 years had the inclusion criteria and were enrolled in the present study. Informed written consent approved by the local Ethics Committee was obtained from patients to use their data for research purposes. The mean post-loading follow-up was 32 months. Autologous grafts were previously inserted into patients jaws under general anaesthesia. Usually the mean post-grafting period was 8 months before implant surgery and the nal prosthetic restoration was delivered after additional 6 months. A total of 261 implants were inserted into 42 patients: 89 (34.1%) into the mandible and 172 (65.9%) into the maxilla. There were 52 Bi-Implant (3i implants, Biomet Inc., USA), 79 P1 H (3i implants, Biomet Inc., USA), 59 Biomax (3i implants, Biomet Inc., USA), 12 Branemark (Nobel Biocare, Zurich,

Diameter Implant type

Tab. 4: Multivariate analysis output Variable

Age Gender Type of graft Implant site Upper/lower jaw Implant type

Signicance(p-value)
0.013 0.064 0.516 0.009 0.825 0.013

92

2/2010

Alveolar ridge augmentation

Springer-Verlag J. Stomat. Occ. Med.

original article

Discussion
Autologous bone grafts are the gold standard for jaws reconstruction [3, 13, 14]. Calvaria bone graft has minimal donor site pain and its harvest can typically be incorporated into incisions made for the primary reconstruction (i.e. bicoronal incision) in case of trauma or tumour (where temporalis muscle is used). The donor sites defect can often be hidden by the hair, has a useful gradual curvature, and minimal resorption occurs. The disadvantages of calvarial grafts include the risk of epidural haematoma from damage to the sagittal or other dural sinuses, dural tears, limited shaping because of bone rigidity and limited amount of cancellous bone. The risks of intracranial complications and donor site deformity can be minimized by using split calvarial instead of full thickness bone grafts. As a donor site the skull has further advantages as skull chips or shavings as well as bone dust can be harvested to ll certain defects that do not require a formal graft, or can be used to augment a bone graft [15]. Iliac crest grafts provide an abundant supply of cancellous bone, and inner or outer cortex may provide appropriate contour. The disadvantages include limited supply of cortical bone, post-operative pain and haematoma, acetabular injury, fascia lata clicking and pain with paresthesias if injury occurs to the lateral femoral cutaneous nerve [16]. The intra oral sites used commonly for grafting are, most common, mandibular symphysis, ramous and palatine tori [17]. The mandibular symphysis is an attractive donor site, with low morbidity rate. The surgery is restricted to one intra oral site which produces an invisible scar in the labial sulcus. The main criticism for using it as a graft is the limited volume of bone available for grafting [18]. In our series no major complication occurred. No neurological problem was reported for calvarial harvesting. Iliac crest has always a local haematoma and some pain in the donor site for almost a week. No problem was reported in the case of mandibular bone sampling. Restoration of the decient alveolar ridge by autogenous bone grafting, in association with placement of osseointegrated implants, has been reported with cortico-cancellous blocks, compressed particulate marrow, and cortical grafts from the mandible and the cranium [6, 1219]. The reported individual implant success rates with maxillary and mandibular bone grafts vary from 61% in the maxilla to 98% in the mandible. In autologous maxillary sinus grafts, the implant success rate has been reported to be between 85% and 98%. [20]. In our series no implant was lost and the overall survival rate was 100% at 32 months. Peri-implant bone resorption varies in accordance with the type of bone graft, being higher in the case of iliac crest and lower in the case of mandible and calvaria. These results are not surprising being similar to those of previous reports in different series [3]. In the present study, there are two major determinants of clinical outcome: the xture site and the type of implant. In the molar region the peri-implant bone resorption is signicantly higher than on other sites (Table 2). This can be explained by the fact that in the molar area there is a prevalence of onlay grafts, whereas in the frontal region inlay grafts are preferentially used.
J. Stomat. Occ. Med. Springer-Verlag

Also the type of implants has an impact on the clinical outcome. From a general point of view it is possible to distinguish the macro-, mini-, micro- and nano-design [2124] for each implant type. The macrodesign is the shape of the implant, for example cylindrical or root form. The minidesign is the dimension of the threads or the shape of the neck (the dimension ranged from 1 to 0.1 mm); the microdesign is the shape of implants surface (for example the grooves and holes due to surface treatments like machination, acid etching and sand-blasting procedures). Finally, the nanodesign is determined by the molecular composition of the surface [2124]. Thus it is not surprising that different types of xtures have different impact on bone resorption (Table 2).

Conclusion
In conclusion implants can be successfully inserted in autografted jaws although a higher resorption should be expected in the molar region. In addition the type of implant can have an impact on clinical outcome.

Acknowledgements
This work was supported by FAR from University of Ferrara (F.C.), Ferrara, Italy, and from Regione Emilia-Romagna, Programma di Ricerca Regione-Universit, 20072009, Area 1B: Patologia osteo-articolare: ricerca pre-clinica e applicazioni cliniche della medicina rigenerativa, Unit Operativa n. 14.

Conict of interest
Authors declare that there is no conict of interest.

References
[1] Atwood DA, Bone loss of edentulous alveolar ridges. J Periodontol 1979;50:1121. [2] Breine U, Brlnemark PI. Reconstruction of alveolar jaw bone: an experimental and clinical study of immediate and preformed autologous bone grafts in combination with osseointegrated implants. Stand J Plast Reconstr Surg 1980;14:2348. [3] Carinci F, Farina A, Zanetti U, Vinci R, Negrini S, Calura G, Laino G, Piattelli A. Alveolar ridge augmentation: a comparative longitudinal study between calvaria and iliac crest bone grafts. J Oral Implantol 2005;31:3945. [4] Block MS, Kent JN. Sinus augmentation for dental implants: the use of autogenous bone. J Oral Maxillofac Surg 1997;55:12816. [5] Von Arx T, Buser D. Horizontal ridge augmentation using autogenous block grafts and the guided bone regeneration technique with collagen membranes: a clinical study with 42 patients. Clin Oral Implants Res 2006;17:35966. [6] Collins TA. Branemark-basic and beyond. In: Bell WH (ed). Modern practice in orthognathic and reconstructive surgery Vol. 2. Philadelphia, PA: Saunders; 1992. [7] Jensen SS, Terheyden H. Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone substitute materials. JOMI 2009; 24(Suppl):21836. [8] Albrektsson T, Zarb GA. Determinants of correct clinical reporting. Int J Prostodont 1998:11:51721. [9] Khan S, Cabanilla LL. Periodontal probing depth measurement: a review. Compend Contin Educ Dent 2009;30:124.

Alveolar ridge augmentation

2/2010

93

original article

[10] Karoussis IK, Mller S, Salvi GE, Heitz-Mayeld LJ, Brgger U, Lang NP. Association between periodontal and peri-implant conditions: a 10-year prospective study. Clin Oral Implants Res 2004; 15:17. [11] Dawson-Saunders B, Trapp RG. Basic and clinical biostatistics. Norwalk, CT: Appleton & Lange; 1994. [12] Jensen J, Sindet-Pedersen S. Autogenous mandibular bone grafts and osseointegrated implants for reconstruction of the severely atrophied maxilla: a preliminary report. Oral Maxillofac Surg 1991;49:127787. [13] Acocella A, Sacco R, Niardi P, Agostini T. Early implant placement in bilateral sinus oor augmentation using iliac bone block grafts in severe maxillary atrophy: a clinical, histological, and radiographic case report. J Oral Implantol 2009;35:3744. [14] Kahn A, Shlomi B, Levy Y, Better H, Chaushu G. The use of autogenous block graft for augmentation of the atrophic alveolar ridge. Refuat Hapeh Vehashinayim 2003;20:5464,102. [15] Zins JE, Whitaker LA. Membranous versus endochondral bone: implications for craniofacial reconstruction. Plast Reconstr Surg 1983;72:77884. [16] Smith JD, Abramson M. Membranous vs. endochondral bone autografts. Arch Otolaryngol 1974;99:2035. [17] Meij AW, Baart JA, Andersen BP, Kostense PJ, Sijp JR, Tuizing DB. Outcome of bone grafting in relation to cleft width in unilateral cleft lip and palate patients. Oral Surg Oral Med Oral Path Oral Radiol Endod 2003;96:1925.

[18] Booij A, Raghoebar GM, Jansma J, Kalka WW, Vissink A. Morbidity of chin bone transplants used for reconstructing alveolar defects in cleft patients. Cleft Palate Craniofac J 2005;42:5338. [19] Keller EE, Van Roekel NB, Desjardins RP, Tolman DE. Prostheticsurgical reconstruction of the severely resorbed maxilla with iliac bone grafting and tissue-integrated prostheses. Int J Oral Maxillofac Implants 1987;2:15565. [20] Donovan MG, Dickerson NC, Hanson LJ, Gustafson RB. Maxillary and mandibular reconstruction using calvarial bone grafts and Branemark implants: a preliminary report. J Oral Maxillofac Surg 1994;52:58894. [21] Palmieri A, Brunelli G, Guerzoni L, Lo Muzio L, Scarano A, Rubini C, Scapoli L, Martinelli M, Pezzetti F, Carinci F. Comparison between titanium and anatase miRNAs regulation. Nanomedicine 2007;3:13843. [22] Palmieri A, Pezzetti F, Brunelli G, Arlotti M, Lo Muzio L, Scarano A, Rubini C, Sollazzo V, Massari L, Carinci F. Anatase nanosurface regulates microRNAs. J Craniofac Surg 2008;19:32833. [23] Sollazzo V, Palmieri A, Pezzetti F, Scarano A, Martinelli M, Scapoli L, Massari L, Brunelli G, Caramelli E, Carinci F. Genetic effect of anatase on osteoblast-like cells. J Biomed Mater Res B Appl Biomater 2008;85:2936. [24] Sollazzo V, Pezzetti F, Scarano A, Piattelli A, Massari L, Brunelli G, Carinci F. Anatase coating improves implant osseointegration in vivo. J Craniofac Surg 2007; 18:80610.

94

2/2010

Alveolar ridge augmentation

Springer-Verlag J. Stomat. Occ. Med.