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British Journal of Oral and Maxillofacial Surgery 46 (2008) 665670

Review

Secondary Alveolar Bone Grafting: the Dilemma of Donor Site Selection and Morbidity
Maamon A. Rawashdeh a, , Hani Telfah b,1
a

Department Oral & Maxillofacial Surgery, Associate Professor Jordan University of Science & Technology, Consultant Oral & Maxillofacial Surgeon King Abdullah University Hospital, Coordinator of Cleft Lip & Palate Centre at King Abdullah University Hospital, Jordan b Consultant Oral & Maxillofacial Surgeon, Royal Medical Services, Jordan Armed Forces, Jordan Accepted 8 July 2008 Available online 29 August 2008

Abstract Fresh autogenous cancellous bone is ideal for secondary alveolar cleft bone grafting because it supplies living, immunocompatible bony cells that integrate fully with the maxilla and are essential for osteogenesis. Recent animal studies have shown that the dynamics of cancellous inlay bone grafts are different from those of cortical onlay bone grafts, and they refute the assumption that membranous bone grafts are superior to endochondral bone grafts because of their embryological origin. These studies prove that inlay endochondral cancellous specimens have a higher percentage increase in actual bony volume than cortical membranous and cortical endochondral inlay bone grafts. There are various donor sites for secondary alveolar cleft bone grafts. Currently the main sites for autogenous cancellous bone are iliac crest, calvarium, mandibular symphysis, and tibia. Some authors have suggested that the iliac crest donor site causes an unacceptably high degree of postoperative morbidity, but it is still the rst choice for secondary alveolar cleft bone grafts and should not be rejected solely because of such concerns. Recombinant human bone morphogenetic protein-2 (rhBMP-2) is now an attractive bony substitute that promotes the differentiation of pluripotential cells into bone-forming cells that lay down new host bone in the site of the defect. Much more research and development are necessary to nd a suitable carrier for rhBMP-2, and to study the properties of newly formed bone that it has induced before it can be a substitute for autogenous bone. 2008 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Keywords: Iliac crest; Morbidity; Secondary alveolar bone graft; Cleft lip and palate

Introduction Secondary alveolar bone grafting is a well-established technique in the management of patients with cleft lip and palate; any patient with a cleft should be considered for grafting.13 Many sources of bone, both autogenous and alloplastic have been studied, compared, highly proled, and abandoned, but fresh autogenous cancellous bone is ideal because it supplies

Corresponding author at: P.O. Box: 3795, Baghdad Street, Irbid, Post Code: 21110, Jordan. Tel.: +962 79 5551549; fax: +962 2 7305339. E-mail addresses: mamonrawashdeh@yahoo.com (M.A. Rawashdeh), Telfah hani@hotmail.com (H. Telfah). 1 Tel.: +962 79 5889844.

living, immunocompatible bony cells that integrate fully with the maxilla and are essential for osteogenesis.49 Historically, bone grafts have been used to treat patients with alveolar clefts since the beginning of the 20th century. Von Eiselsberg used the little nger as a pedicled graft in 1901, and Drachter used the tibia and periosteum in 1914.10 Since then the usual sites for harvesting autogenous bone have included iliac crest, cranium, chin, and rib; the greatest disadvantage being morbidity at the donor site. Today the procedure should aim at optimal physiological and psychological function with minimal impairment of growth and development in the maxillofacial complex. The question of the preferred donor site for alveolar cleft grafts has been debated for many years. Its choice is inu-

0266-4356/$ see front matter 2008 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.bjoms.2008.07.184

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enced by several factors that include the surgeons experience and preference, the volume of bone that is required and available, and the morbidity that is associated with its harvest. All sources of autogenous bone have their advantages and disadvantages. We review sources of autogenous bone for secondary alveolar cleft bone grafts.

Iliac Crest Many reports suggest that autogenous bone from the iliac crest is the gold standard by which other types of alveolar grafts should be compared.2,69,2231 It is easy to access and can supply large quantities of cancellous bone with pluripotent or osteogenic precursor cells that support osteogenesis in the early period after grafting.8,32 Because of its higher content of osteogenic cells, cancellous bone is thought to be superior to corticocancellous bone. The number of osteogenic cells/unit volume of cancellous bone can be increased further by compacting it, which is thought to increase its reliability even further.28,33 Use of cancellous bone therefore results in rapid revascularisation of the graft over 3 weeks unlike that of cortical bone, which maintains volume by creeping substitution.14 Bone from the iliac crest can be harvested by an open approach or with a trephine. Some authors have reported concern about the postoperative morbidity that is associated with traditional open harvesting, and this has been the impetus to seek alternative minimally-invasive techniques for harvesting such bone.30,34 It is difcult to ascertain from current reports how much morbidity is caused by harvesting bone from the iliac crest because many different techniques for harvesting are used, and morbidity is often not reported, or is measured inadequately. It is also difcult to compare the morbidity caused by harvesting bone from the iliac crest with other donor sites as it may be affected by harvesting techniques. The main criticism of the use of the iliac crest for secondary alveolar bone grafts is postoperative pain that limits walking and results in a prolonged stay in hospital and prolonged recovery. Several studies have shown that the severity of postoperative pain after iliac crest bone harvesting has been overstated. Most patients indicated that the pain was not severe and was readily alleviated with small quantities of analgesics.26,29,31,3537 Kalk et al.29 and Eunger and Leppnen31 reported that only 26% (n = 17) and 38% (n = 19) of their patients, respectively, found that the hip donor site was more painful than the oral wound. Several surgeons26,29,36,37 have reported that roughly 86% of their patients would be willing to have an alveolar bone graft using bone from the hip, if recommended, and many patients are satised with the residual scar.29,31,36,38 Several surgeons have reported that harvesting bone from the iliac crest did not delay mobility, and almost all patients were able to walk within the rst 24 hours after operation and could walk normally within 2 weeks.26,35,37-43 Currently, the reported length of stay in hospital after bone is harvested from the iliac crest varies widely. Bergland et al.1 discharged patients six days after operation, which is longer than the 3.63.8 days reported by Troxell et al,44 and Hall and Posnick.45 This may reect longer stays in hospital and fewer restrictions on health insurance during the early 1980s. More recently stays in hospital that have ranged between 3.6 and 6 were reduced to 2.5 days by Canady et al,26 and to two days by Kortebein et al.20 and Dawson et al.35 One day

Endochondral and membranous bone Animal studies have shown that when corticocancellous blocks are grafted to the facial skeleton in an onlay fashion, membranous bone maintained its volume better than endochondral bone.11,12 The assumption that a membranous bone graft is superior to an endochondral bone graft because of its embryological origin was used to justify the use of cranial and mandibular bone to reconstruct alveolar clefts,1316 but this ignored the fact that a full thickness bone graft, both membranous and endochondral, consists of a compact cortical layer and a cancellous layer of marrow. Membranous bone is more cortical and less cancellous than endochondral bone. Experimental work by Ozaki and Buchman,17 and Ozaki et al.18 showed that these differences in composition enable membranous bone to resorb less over time because it has more cortical bone than an endochondral bone graft, not because of embryological superiority. They found that there was no statistical difference in the rate of resorption between the two cortical onlay grafts of different embryological origin when the components were separated, and that the maintenance of volume is a result of its microarchitecture. Rosenthal and Buchman19 developed work by Ozaki and Buchman17 and Ozaki et al.18 on maintaining the volume of inlay bone grafts in the craniofacial skeleton by harvesting cortical and cancellous bone from iliac crests (endochondral origin), and cortical bone from the mandibles (membranous origin) of rabbits. Four holes were made in the cranium of each rabbit and lled with one each of endochondral cortical bone, endochondral cancellous bone, membranous cortical bone, or was left as an ungrafted control. The animals were killed at 3, 8, or 16 weeks. The crania were assessed by microcomputed tomography and histology. Unlike the data for onlay bone grafts17,18 that resorbed over time, all three types of inlay grafts in the study increased in volume over time. Interestingly, endochondral cancellous specimens increased in volume the most. They concluded that the dynamics of cancellous inlay bone grafts are different from those of cortical onlay bone. These ndings are believed to have led to a change in the way that craniofacial surgeons select a graft. In alveolar clefts, the osseous deformity is a continuity defect of the alveolar process and pyriform rim, which is reconstructed with bone that is inlayed between the osseous segments instead of onlayed on the maxilla. This may explain the superiority of cancellous iliac crest over cranial bone for secondary alveolar grafts that was shown by Sadove et al.8 in 1990, Kortebein et al.20 in 1991, and then conrmed by LaRossa et al.21 in 1995.

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in hospital has recently been advocated by Perry et al,25 and Rudman.41 Local pain control after predictable anaesthetic recovery, ability to eat and drink, and reliable, motivated carers are essential for the safety of patients who have secondary alveolar bone grafts from the iliac crest as outpatients.25

because of cultural beliefs.57 It is not possible for two teams to operate simultaneously when harvesting cranial bone, which lengthens the operation.58

Mandibular symphysis Cranial bone During the last two decades the use of the cranial bone grafts for maxillofacial procedures has been accepted. Its successful use at various craniomaxillofacial sites4649 has led to its use to treat alveolar clefts.8,14,20,50,51 Both cortical and cancellous bone can be harvested from the calvarium in young patients, and the different instruments and techniques that are available allow various consistencies to be harvested. Wolfe and Berkowitz50 used diplo from the cranium for secondary alveolar crest grafts. Denny et al14 used a curved osteotome and mallet to remove thin shavings from the outer cortex and the diplo. This random mixture was then ground manually to a granular texture to avoid thermal damage to the bone. Jackson et al.49 used the craniotome technique to harvest both outer table and diploic bone, which resulted in powdered bone that turned to slurry when mixed with blood. Several authors have claimed that the cranium, unlike the iliac crest, is a donor site with low morbidity, minimal postoperative pain, and a scar that is hidden in the hair.14,50,52,53 However, there are diverse views about the efcacy of cranial bone for secondary alveolar bone grafts. While some authors have reported poor success with alveolar bone grafts when they compared cranial bone grafts with that of the iliac crest,8,20,21,49 others reported comparable success.14,52,53 Jackson et al.49 stopped using cranial bone for secondary alveolar bone grafts after long-term evaluation of 307 cases. It has been suggested that the inferior results with cranial bone are caused by the technique used for harvesting, and when harvested with its structure intact may be more successful.8,14,20,50,51 Sadove et al.8 suggested that the efcacy of cranial bone grafting of clefts will require long-term, multiple, independent centre studies. Complications caused by harvesting cranial bone range from 0.25% (n = 27)48 to 5.5% (n = 17),49 and include haematomas or seromas (9.5%, 7 patients), infected wounds, or osteomyelitis (0.2%, n = 1),47 dural tear (0.5%4%), dural exposure (5%12%), subdural haemorrhage, leaking of cerebral spinal uid, and serious neurological problems (0.09%).4749,51,5456 None of these authors discussed how to manage visible scars and depressions of the skull in elderly balding men, or the hairless area that corresponds to the coronal aps. Some authors have expressed concern about reduced strength of the skull at a cranial donor site, and have recommended a different site for patients who might receive multiple blows to the head such as in contact sports.51 The harvesting of cranial bone is also not readily acceptable among some ethnic groups, particularly the Chinese, Bosker and van Dijk in 1980 were the rst to report the use of the mandibular symphysis bone graft for secondary alveolar clefts with good results.15 The mandibular symphysis is an attractive donor site with low morbidity and a satisfactory success rate for lling clefts. Its advantages include restriction to one intraoral site of operation, a shorter stay in hospital, minimal pain or discomfort, and an invisible scar in the lower labial sulcus.13,15,16,24,27 However, the restriction to one intraoral operating site does not allow two teams to operate simultaneously, and leads to longer operations. The main problem with symphyseal bone is the limited volume available because of permanent dentition, so it is not suitable for large or bilateral clefts.27,28,59 Disadvantages of the donor site include an increased percentage of impacted canines (31%, n = 14) in the cleft region, which was attributed to the increased cortical content of the harvested bone;15 an impacted canine is often in the middle of the palate so the patient has to have a minor operation to expose it and time-consuming orthodontic treatment. Other points to consider are the loss of unerupted permanent teeth, particularly the canines, in early mixed dentition;15,28 the possibility of necrosis of the pulp, or devitalisation of teeth; and injury to the mental nerve that could result in objective and subjective disturbances of the sensitivity of adjacent teeth and soft tissues.13,15,16,24,27

Tibia The tibia has been used extensively in orthopaedic surgery and has gained in popularity among maxillofacial surgeons for grafting to reconstruct the jaw, and orthognathic, cleft, and preprosthetic surgery.6062 However, most experience with tibial grafts has been in adults, and mainly for trauma. Drachter was the rst to use tibial bone to reconstruct facial clefts in 1914, and since then relatively few authors have reported the tibia as donor site for secondary alveolar cleft grafts. Most of these studies either compare the complication rate with that of the iliac crest, or describe variations in the technique to reduce morbidity.34,58,6366 Ilankovan et al.34 and Chen et al.66 reported that roughly 25 ml of cancellous bone could be harvested in adults without serious complications. In children, the proximal tibia is small and the epiphyseal cartilage is growing, which means that access must be minimised and located more inferiorly to avoid possible interference with the growth centre.64 Besly and Ward Booth64 modied the technique for harvesting tibial bone in adults to make it suitable for use in children, and compared

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groups who had had bone harvested from the tibia and iliac crest. The advantages of harvesting tibial cancellous bone are short operating time, minimal scarring, early mobility, and a short stay in hospital.34,58,6466 However, the amount of bone harvested can be limited, and patients must be warned about the possibility that bone may be taken from both legs.65,66 The incidence of serious complications of tibial bone harvesting is reported to range from 1.3% to 3.8%.63,66 Rates of proximal tibial fractures after grafting range from none to 2.7% (2 patients), and patients are usually advised to avoid contact sports for at least three months.65 Long-term follow-up of potential damage to the growth centre after proximal tibial grafting in patients with clefts has not been reported.34,64

sound and biologically viable union. Its use is also hoped to achieve a remodelling equilibrium that prevents loss of bone through resorption. However, it requires a suitable carrier for its clinical applications in human conditions to prevent rapid diffusion of the protein, and detailed studies of the properties of newly-formed bone that has been induced by rhBMP-2 are lacking. Much more research and development are necessary before this can be a substitute for autogenous bone.

Boneless-bone grafting Boneless-bone grafting (gingivoperiosteoplasty) was popularised by Skoog in the 1960s and modied by others. Its use is one of the most widely debated areas in the treatment of patients with cleft lip and palate; its advocates are few, but are well-respected.7679 They suggest that if healthy periosteum is closed over the alveolar defect, favourable osteogenic conditions would allow bone to bridge it.76,77 However, the degree of ossication after gingivoperiosteoplasty varies between 50% and 100%, and a third step of bone grafting may be required. Some authors also argue that all alveolar clefts will remain decient in osseous contour and bulk, which compromises the eruption and maintenance of permanent dentition, so necessitating an eventual bone graft.78,79

Autogenous bony substitutes The use of autogenous bony substitutes for secondary alveolar bone grafts may reduce morbidity because it is not necessary to harvest autogenous bone, and would reduce the cost of rehabilitating patients with clefts. There is a growing interest in the use of bony substitutes to reconstruct craniomaxillofacial defects. The search for autogenous bony substitutes began more than a century ago when HCLdemineralised bone chips from ox tibia were implanted into canine cranial defects,57,67 but substitutes have been limited in their use for late secondary alveolar cleft bone grafting in adults with minor alveolar deciencies because of their unpredictability in resorption, or in the amount of bone that is formed.33 Recently several studies have shown that bony defects can be repaired reliably with recombinant human bone morphogenetic protein (rhBMP). Many attempts have been made to purify BMP from the demineralised bone of various animals, but pure BMP has not been obtained. Advances in molecular biology have enabled the production of pure specic proteins, and nine recombinant human bone morphogenetic proteins have been cloned (designated recombinant human bone morphogenetic protein-1 - 9).68,69 Animal studies have validated the efcacy and safety of recombinant human bone morphogenetic protein-2 (rhBMP-2) and it is now an attractive bony substitute that is readily available in large quantities for widespread clinical use.7074 rhBMP-2 induces osteogenesis and many experimental studies have shown that it also induces the formation of new host bone that gives functional stability in the femur of rats and sheep, and the mandible and spine in dogs.70,71 Other studies have shown that rhBMP-2 is effective in the regeneration of alveolar bone and associated periodontal attachment apparatus.7072,74,75 Bone is induced differently with rhBMP-2 than it is with conventional bone grafts; rhBMP-2 promotes the differentiation of pluripotential cells into bone-forming cells that lay down new host bone in the site of the defect (osteoinduction).68 When used for secondary alveolar cleft bone grafts rhBMP-2 completely lls the cleft with an adequate amount of bone that integrates with the host bone to form a structurally

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