J Oral MexNofac 48:933-941,
Surg
1990
Bone for Secondary Alveolar Cleft 0s teoplas ty
Allogeneic
BARBARA B. MAXSON, DDS, MS,* STEVEN D. BAXTER, DDS,t KATHERINE W.L. VIG, BDS, MS, FDS, DORTH,$ AND RAYMOND J. FONSECA, DMD§ The purpose of this retrospective clinical study was to determine the efficacy of allogeneic bone for secondary alveolar cleft osteoplasty. Twentyfour patients with unilateral cleft lip and palate treated with allogeneic bone grafts were examined by a surgeon, orthodontist, and prosthodontist 20 to 47 months after surgery. Radiographic and clinical examination of the periodontal status of the teeth adjacent to the cleft and their antimeres were compared for differences with Student’s t test and the Wilcoxon test. Radiographs indicated complete bone bridging in 21 patients. Two of the remaining three patients had a l-mm radiolucent gap in the cleft site. The third patient had a 6-mm-wide radiolucency and recurrence of an oronasal fistula which was regrafted with autogenous bone. No statistically significant differences between the cleft and noncleft tooth antimeres were found for plaque, gingivitis, bleeding, sulcus depth, or level of attachment. A statistically significant difference in the amount of attached gingiva was found between the cleft and noncleft tooth antimeres. Nine patients with missing lateral incisor teeth avoided prosthetic replacement by orthodontic movement of the canine tooth into the grafted edentulous space. In those cases where the maxillary canine was unerupted at the time of the surgery, eruption into the graft occurred. Stability of the maxillary segments was sufficient to allow prosthodontic restoration with a fixed partial denture in those cases where it was indicated. cems, an influence on future maxillary growth has been reported. I-3 Although early surgical intervention may facilitate normal development of speech and address esthetic concerns, the effect on facial growth should be considered. Koberg4 reviewed the history of alveolar bone grafting in 1973. He discussed three basic schedules that had been reported for this procedure: 1) primary osteoplasty in the infant, 2) early secondary osteoplasty after the eruption of the deciduous dentition, and 3) late secondary osteoplasty after eruption of the permanent dentition. Reports of the adverse effects on maxillary growth after early surgical repair led Koberg to conclude that “. . . most severe maxillary deformities are to be expected as late results of primary bone grafting, so that late secondary osteoplasty remains the only justifiable form of bone transplantation in cleft surgery.” He also reported that attempts to use preserved bone instead of autotransplants generally resulted in failure.
The appropriate timing and technique for cleft lip and/or palate surgery has been a controversial issue among surgeons for many decades. Although early surgery to restore normal anatomic relationships may fulfill immediate functional and esthetic con-
Received from The University of Michigan, Ann Arbor. * Assistant Professor, Department of Oral Medicine, Pathology, Surgery. t Formerlv. Resident in Oral and Maxillofacial Surgery; ures- _ _ ently, in private practice, Columbus, OH. $ Associate Professor, Department of Orthodontics and Pediatric Dentistry. $ Formerly, Professor and Chairman, Department of Oral Medicine, Pathology, Surgery; presently, Dean, University of Pennsylvania School of Dentistry, Philadelphia. Address correspondence and reprint requests to Dr Maxson: Department of Oral Medicine, University of Michigan Hospitals, University Hospital Bl-B204/0018, 1500 E Medical Center Dr, Ann Arbor, MI 48109-0018. 0 1990 American geons
Association
of Oral
and Maxillofacial
Sur-
0278-2391/90/4809-0005$3.00/O
933
ALL0
934
A second review of alveolar cleft osteoplasty was made in 1985 by Witzenburg,5 who reported problems that occur when the alveolar cleft is not grafted. These include insufficient periodontal support for the teeth adjacent to the cleft, persistence of oronasal fistulae and associated sequelae, mobility of the maxillary segments with unfavorable conditions for prosthetics, relapse after orthodontic expansion of the collapsed maxillary segments, and a lack of bony support to the alar base resulting in asymmetry. He concluded that autogenous bone appeared to be the best graft material and that the majority of experiences with homologous or alloplastic materials were disappointing. Witzenburg also supported Koberg’s classification with the addition of the “secondary osteoplasty” to be performed during the mixed dentition. Since Witzenburg’s review, the efficacy of secondary osteoplasty has been reported by several authors,6-8 although primary osteoplasty may still be priferred at some institutions.“” Donor sites for harvesting the graft include iliac crest,’ rib,” mandibular symphysis,” and calvarium.‘* Rationale of Bone Grafting Although the results of early grafting procedures with allogeneic bone were disappointing, the effrcacy of allogeneic bone grafting for selected maxillofacial procedures has been evaluated in animal models. These onlay bone graft studies suggest that the vital autograft has a different biological response than the freeze-dried allograft. Allogeneic bone grafts rely on osteoinduction for new bone formation from both subperiosteal and endosteal sites. Revascularization of the graft is slower and final reorganization of the graft is delayed in comparison with the cellular response of autogenous grafts. Because the allograft acts only as a scaffold, replacement by new host bone is delayed.13 Reports from animal studies support the use of allogeneic bone grafting for maxillofacial procedures.13-16 Marx et all6 compared allogeneic maxillary cleft grafts with autogenous cleft grafts in a sample of 22 mongrel dogs. Their findings indicated that, although the allogeneic graft did induce bone formation, it was insufficient (30%) and protracted. They further stated that they would not expect such grafts to respond to passive tooth eruption, orthodontic or orthopedic forces, or growth forces in the maxilla. Several preliminary clinical studies have reported successful results with freeze-dried allogeneic bone for oral and maxillofacial procedures. Marx” used allogeneic graft material in 36 patients for cyst fill,
BONE FOR ALVEOLAR
CLEFT GRAET
osteotomy, ridge augmentation, and mandibular reconstruction. Allard et al’* reviewed 61 patients, 1 to 6 years after graft procedures for osteotomy, ridge augmentation, and secondary cleft repair. Comparison of clinical results, complications, and morbidity indicated that in selected cases, with appropriate surgical technique, frozen homologous bone was an alternative to autogenous bone in grafting procedures. A preliminary clinical report of 20 patients who received freeze-dried allogeneic bank bone for secondary repair of a unilateral alveolar cleft demonstrated bone bridging 3 to 6 months after surgery, both clinically and radiographically.” The ability of such grafts to permit orthodontic tooth movement through the graft and to allow passive tooth eruption could not be established from this short-term study. Most recently, Kraut*’ reported the results for five patients with unilateral alveolar clefts who received grafts with freeze-dried allogeneic bone. Passive eruption of the canine tooth through the graft occurred in four of the five cases. The purpose of this retrospective study was to review 24 unilateral cleft palate patients who had alveolar cleft grafts with allogeneic bone. Allogeneic bone as a grafting material was evaluated in terms of treatment outcomes using specific criteria of success and failure. Materials and Methods Forty-five patients were recalled for clinical and radiographic evaluation of secondary alveolar cleft grafts with allogeneic bone. Twenty-four of these patients were evaluated by an oral surgeon, orthodontist, and prosthodontist. All patients had bone grafts placed at The University of Michigan Hospitals at least 1 year prior to recall. Twenty-three of the patients received allogeneic cancellous bone chips and one patient received ground allogeneic bone. Preparation of the bone included reconstitution with saline and antibiotic as reported by Nique et aLI The surgical technique*’ involved full palate flaps for nasal, labial, and palatal closure. This technique is specifically designed to bring attached gingiva into the cleft defect. An acrylic resin splint was routinely wired to the teeth to protect the palate during healing. Fabrication of the splint necessitated relieving the maxillary cast with several layers of baseplate wax anteriorly and extending the acrylic resin just over the ridge crest of the surgical site. All patients were given preoperative antibiotics and steroids. They continued to receive the antibi-
MAXSONET AL
935
otic for 7 to 10 days and the steroid for 2 days postoperatively. Early ambulation, use of a bedside humidifier, and administration of a topical nasal decongestant were also part of the postoperative protocol. l9 Chart review and examination of all previous radiographs provided an historical data base for each patient. At the follow-up examination, periapical radiographs and anterior occlusal films were made of the grafted cleft area and adjacent teeth. These were evaluated by two oral surgeons for evidence of bone bridging and development of unerupted teeth. Patients were questioned about past or present problems related to the surgery, and each patient was examined and evaluated by a surgeon, an orthodontist, and a prosthodontist. Periodontal evaluation was performed by a single examiner using a University of Michigan periodontal probe. Plaque (Silness and Loe), gingivitis (Loe and Silness), exudate, calculus (Ramfjord), mobility (modified Miller), bleeding (Saxer and Muhlemann), pocket depth (Ramfjord), exposed root surface, and attached gingiva (labial only) were scored for each tooth immediately adjacent to the cleft and its antimere. Periodontal scores were averaged for each side and compared for differences with Student’s t test or a nonparametric alternative, the Wilcoxon test. Although most of the periodontal data were derived from ordinal scales, the two scores for each subject represented mean values from a number of observations which would approximate a normal distribution. Therefore, for some of the parameters where the assumption of normalcy could be made, the t test was applied. Results PREOPERATIVEFINDINGS
The average age of the patients (21 male, 3 female) at the time of surgery was 12 years 9 months (range, 9 years 0 months to 16 years 11 months). The presenting chief complaint at the time of surgery was need for alveolar cleft graft (lo), oronasal fistula (l), or both (13). Preoperative radiographs revealed no missing teeth in 12 patients, 1 missing tooth in 19 patients, and 3 patients missing 2 teeth associated with the cleft site. Canine root formation associated with the cleft was complete in 13 patients, but in 10 patients root formation was incomplete, and 1 patient was missing the succedaneous canine tooth. The average cleft width was 5.02 mm (range, 0 to 12.5 mm). One patient without a radiolucency in the cleft site
required the surgical procedure for closure of an oronasal fistula. Preoperatively, eight patients presented with retained deciduous or supernumerary teeth that required extraction at the time of the bone graft. Twelve patients received preoperative orthodontic treatment. OPERATIVE FINDINGS
Average estimated blood loss at surgery was 187 mL (range, 20 to 600 mL). Postoperative hospital stay was 1 to 2 days, with a mean of 1.46 days. Eleven patients in this sample had other surgical procedures in addition to the alveolar cleft graft in the same surgical field. These included 1 closure of a nasopalatine tistula, 1 lip revision, 1 nose revision, and extraction of retained primary or supernumerary teeth in 8 patients. POSTOPERATIVEFINDINGS
Splint removal occurred in an average of 10 days (range, 6 to 16 days). Postoperative infection developed in one patient 2 months after surgery. This patient was treated with antibiotics and proceeded to heal uneventfully. One patient experienced recurrence of the oronasal fistula and underwent a second procedure with autogenous iliac bone. The prevalence of dehiscence and sequestration is presented in Table 1. LONG-TERM FOLLOW-UP
Patients presenting for the follow-up examination were between 1 year 8 months and 3 years 11 months postsurgery (mean, 3 years 2 months). Of those interviewed, 15 patients recalled sequestration, but none recalled infection. Radiographic examination showed complete canine root formation in 21 patients. The remaining 3 patients varied in root development, 1 being threeTable 1. Prevalence of PostoPerative Dehircence and Sequestration
Natureof Finding
No. of Patients
Dehiscence
12
Sequestration
9
Occurrence 1-8 (mean,2.6) 1-7 (mean,2.3)
Time From Surgery
(mo) 1-14 l-18
936
ALL0 BONE FOR ALVEOLAR
Table 2.
CLEFT GRAFT
Periodontal Differences Between Tooth Antimeres (Parametric) t Test
Periodontal Parameter Plaque Gingivitis Sulcus depth (mm) Attached gingiva (mm)
Cleft 0.58 0.90 2.97 3.94
” 0.56 * 0.39 “_ 0.44 + 1.02
Noncleft 0.55 0.84 2.86 4.56
(O-1.75) (0.17-1.58) (2.25-3.92) (1.5-6.0)
-+ 0.40 2 0.37 f 0.34 2 1.05
(0.0-1.25) (0.0-1.50) (2.33-3.58) (3.0-6.5)
PS
P P P P
= = = =
.05 .74 .ll .23 .005
Values are given as mean i SD (range in parentheses).
quarters formed, 1 seven-eighths formed, and in 1 patient the cleft-associated canine tooth was absent preoperatively . Radiographic bony bridging was apparent in 21 patients. In the remaining 3 patients, findings were as follows: a gap of 1 mm in the graft site which appeared less radiopaque than the surrounding bone (this patient had one of the largest preoperative clefts), a l-mm radiolucent gap in a second patient, and in the third patient a 6-mm radiolucency that had been associated with a persistent fistula. This cleft was regrafted with autogenous bone 36 months later. Results from the periodontal examination are presented in Tables 2 and 3. No significant differences between cleft-associated teeth and their antimeres were found, except with regard to mobility and amount of attached gingiva. Chart review indicated that 15 patients had preoperative orthodontic treatment, while postoperative treatment had been performed for 20 patients. Of these, 5 were in active treatment and 5 had finished definitive orthodontic treatment at time of follow-up. In 21 patients, no surgical exposure of the canine tooth associated with the cleft site was necessary. In 2 other patients, development had not progressed sufficiently to determine the need for surgical exposure. In 1 patient, the tooth was absent. Orthodontic treatment to assist eruption and repositioning of the cleft-associated canine tooth was needed in 4 patients. In 18 patients, eruption of the canine tooth occurred uneventfully and in 1 patient, it was too soon to determine. From clinical and radiographic examination it was apparent that the permanent canine tooth had Table 3.
erupted into the bone graft in 9 patients (Fig 1). Movement of the adjacent teeth into the grafted cleft was demonstrated in 15 of the 24 patients in this study. Orthodontic and prosthodontic treatment, as well as orthognathic surgery, were recommended for some of the patients in this sample. The only patient in whom the allogeneic bone graft was unsuccessful had a cleft-associated tooth with loss of periodontal attachment and thus a compromised long-term prognosis. Prosthodontic examination indicated that no restorative treatment was necessary in nine patients in whom space closure was achieved orthodontitally. Eleven patients demonstrated a need for prosthodontic management. Five of these had a previous restoration that included one acrylic resin temporary fixed partial denture, one acid-etched composite resin-retained fixed partial denture, and three definitive fixed partial dentures. In four patients receiving active orthodontic treatment, prosthodontic treatment needs could not yet be determined. All patients had stable maxillary segments and, therefore, all were candidates for prosthodontic treatment with a fixed rather than removable partial denture (Fig 2). Of the 15 patients who had a residual edentulous space at the cleft site, seven demonstrated an adequate alveolar ridge for routine ridgelapped pontic placement. Four patients demonstrated deficiency in alveolar ridge which would require gingival porcelain to attain an acceptable esthetic result with fixed prosthodontics (Fig 3). In four patients it was too early to determine the need for prosthodontic treatment.
Periodontal Differences Between Tooth Antimeres (Nonparametric)
Periodontal Parameter Calculus Bleeding Exposed root (mm)* Mobility Exudate
Noncleft
Cleft 0.33 0.21 0.08 0.60
-+ 0.37 * 0.25 r 0.24 2 0.50 None
(O-1.0) (O-1.5) (o-1.0) (O-1.5)
Values are given as mean + SD (range in parentheses). * Since the distribution of these real numbers was skewed, a nonparametric
0.19 0.17 0.00 0.33
f + + 2
0.35 0.24 0.0 0.34 None
(o-1.0) (O-1.5) (.OO) (O-1.5)
test was applied to this data set.
Wiicoxon test (P s .05
P = .07 P = .56 P = .ll P=.oo4
937
MAXSON ET AL
FIGURE 1. The canine tooth will erupt through the ailogeneic bone graft if surgery is appropriately timed. A, Unerupted canine tooth asociated with the mature allogeneic bone graft. B, The canine tooth has been moved orthodontically through the graft to occupy the position of the missing lateral incisor.
Discussion The reduced morbidity from eliminating a second surgical donor site with allogeneic bone grafting is
probably most significant from the patient’s perspective. Typically, complaints concerning the iliac crest donor site relate to pain and difIiculty with ambulation. These far exceed complaints about the grafted area. Average blood loss with the single-site procedure was 187 mL as compared with 335 mL previously reported for the two-site procedure using iliac crest as donor bone.21 The surgical risks are reduced when a second surgical site is eliminated as a possible source of infection, increased blood loss, and additional anesthesia time. However, skepticism regarding the ability of allogeneic bone to produce comparable results to those using autogenous bone has been reported. 16,18*‘9 The results of this study indicate that freeze-dried allogeneic bone appears to be comparable in many respects to autogenous bone for alveolar cleft grafting. The ability of teeth to erupt through the graft and to respond to orthodontic forces makes allogeneic bone an alternative grafting option. The findings presented here are comparable to those from clinical studies that have used autogenous bone. Enemark et al’ found similar periodontal results when grafting prior to the eruption of the canine tooth and with adequate attached gingiva for teeth associated with the cleft. The need for secondary gingivoplasty, if attached gingiva is absent, is a prerequisite for an acceptable periodontal result. Our findings demonstrate that, although the height of attached gingiva was significantly less at the labial surface for the cleft-associated teeth than their antimeres, periodontal support was not compromised. In other words, significantly greater pocket depth or exposed root surface was not found as long as some attached gingiva was present. Enemark et al7 also described root resorption associated with the cleft grafts in a number of older patients which had previously been reported by Ames and Maki.23 External root resorption has also been associated with iliac crest cancellous bone used for augmentation of periodontal defects.24 Exposure of cementum or damage to the periodontal ligament is perhaps an explanation for failure rather than the type or origin of the bone graft material. Root resorption was not observed in our patients when allogeneic bone was used, provided that the timing of the graft was appropriate and the unerupted tooth not damaged during the surgery. Enemark found the optimum time for bone grafting of the unilateral cleft alveolus to be when maxillary growth was almost complete (8 to 9 years of age),’ prior to the eruption of the permanent canine tooth. Patients in this study who did not require prosthodontic treatment (37.5%) compared favorably with Enemark’s findings for unilateral clefts with autog-
FIGURE 2. Postoperative
Allogeneic bone grafting can be done in preparation for a fixed partial denture. A and B, Preoperative radiograph. D, There is satisfactory ridge form for esthetic pontic placement.
enous bone (youngest, 49%; middle, 27%; oldest, 8%). Since some of the patients in this sample were too young for final evaluation, the results are probably an underestimate. Hinrichs et a12’ reported the periodontal condition of teeth associated with unilateral cleft palate 2 to 8 years after secondary osteoplasty with autogenous iliac crestal bone. No significant difference between the cleft-associated canine tooth and the contralateral control canine tooth was found, which is in agreement with our clinica results and/or treatment outcomes. Statistically significant differences found in our study were not necessarily clinically significant. Differences in amount of attached gingiva appear to be significant for periodontal health only if there is a total absence of attached gingiva. Differences found in tooth mobility, although statistically significant, were so small that they were clinically insignificant.
findings. C,
FIGURE 3. When alveolar ridge contour after grafting is inadequate, but the alveolar segments are stabilized by the graft, gingival porcelain can be added to the pontic area of the fixed prosthesis.
MAXSON ET AL
FIGURE 4. Delayed osteogenesis of the bone graft is characteristic for the allogeneic alveolar cleft bone graft. A and B, Preoperative findings. C, Three-month postoperative radiograph. D, Seven-month postoperative radiograph. E, Ten-month postoperative radiograph. F and G, Twenty-eight-month postoperative findings.
940
Maxillary expansion is often indicated prior to the bone graft. Orthodontic tooth movement into the allogeneic bone graft site should be delayed for 3 months after surgery. The differences in biological response between autogenous and allogeneic bone can be explained by the autogenous bone graft which elicits an angioblastic proliferation from the recipient site during the first week after surgery. Survival of some of the transplanted osteoblasts allows osteogenesis to occur during the first few weeks of healing. In contrast, the allogeneic bone graft demonstrates a slower revascularization, with migration and proliferation of endothelial cells occurring 1 to 2 weeks later. The graft contributes no viable osteogenic cells, but apparently promotes osteoinduction. The angiogenic response is accompanied by new bone which is laid down at the periphery of the recipient site. As the osteoid is replaced by new bone, the nonviable graft bone is sequestered or removed as a foreign body by macrophages (Fig 4). Given these biologic differences, some cleft sites may be more responsive to autogenous bone. When the cleft is bilateral or there is an extensive alveolar defect with communicating oronasal Iistula, autogenous bone may be the preferred grafting material because of its ability to interact directly with the host tissues. A consideration associated with allogeneic bone grafts is the possibility of human immunodeficiency virus (HIV) transmission through the donor bone. The risk of transmitting HIV, as reported by Buck et al, is negligible. 26 Although safeguards against allowing infected tissue to enter the donor pool are not always infallible, estimates of the risk of receiving contaminated donor tissue can be made.27 However, it may be prudent for the surgeon to verify the safeguards used by the company producing the freeze-dried bone and be prepared to discuss the risks and benefits with the patient at the time of obtaining informed consent. With risk-benefit and cost effectiveness being important health care concerns, reduction in length of hospital stay and operating room time is a consideration when planning elective surgical procedures. As numerous social and biological issues impinge on the decision-making process in the delivery of health care, staying informed becomes increasingly more complex. Moral and ethical issues, along with economic and social pressures, will continue to influence the treatment planning process. Responsibility for selecting a treatment modality is presently shared by the clinician, the third-party carrier, and the patient. Clinicians need to evaluate the relative efftcacy of different treatment options from both risk-benefit and cost effectiveness view-
ALL0 BONE FOR ALVEOLAR
CLEFT GRAFT
points before recommending a treatment plan. logeneic bone grafts, with reduced morbidity similar outcome to autogenous bone grafts, may come a viable alternative treatment option in future.
Aland bethe
Acknowledgment The authors wish to thank Dr Charles J. Kowalski for assistance with data management.
References 1. Jolleys A, Robertson NRE: A study of the effects of early bone grafting in complete clefts of the lip and palate-Five year study. Br J Plast Sura 251229. 1972 2. F&de H, Johanson B: A foiow-up study of cleft children treated with primary bone grafting. Stand J Plast Reconstr Surg 888, 1974 3. Semb G: Effect of alveolar bone grafting on maxillary growth in unilateral cleft lip and palate patients. Cleft Palate J 25:288, 1988 4. Koberg WR: Present view on bone grafting in the cleft palate (A review of the literature). J Maxillofac Surg 1:185, 1973 5. Witzenburg B: The reconstruction of anterior residual bone defects in patients with cleft lip, alveolus, and palate. A review. J Maxillofac Surg 42:717, 1984 6. Bergland 0, Semb G, Abyholm FE: Elimination of the residual alveolar cleft by secondary bone grafting and subsequent orthodontic treatment. Cleft Palate J 23:175, 1986 7. Enemark H, Sindet-Pedersen S, Bundgaard M, et al: Combined orthodontic-surgical treatment of alveolar clefts. Ann Plast Surg 21: 127, 1988 8. Loh SA, Lee ST, Yeap CL: Evaluation of the effects of secondary bone grafting in both adults and children with cleft lip and palate. Ann Acad Med Singapore 17:4OO,1988 9. Rosenstein SW, Monroe CW, Kemahan DA, et al: The case for early bone grafting in cleft lip and palate. Plast Reconstr Surg 70:297, 1982 10. Helms JA, Speidel TM, Denis KL: Effect of timing on longterm clinical success of alveolar cleft bone grafts. Am-J Orthod Dentofac Orthoo 92:232. 1987 11. Sindet-Pedersen S, Enemark H: Mandibular bone grafts for reconstruction of alveolar clefts. J Oral Maxillofac Surg 46:533, 1988 12. Wolfe SA, Berkowitz S: The use of cranial bone grafts in the closure of alveolar and anterior palatal clefts. Plast Reconstr Surg 72:659, 1983 13. Feinberg SE, Fonseca RJ: Biological aspects of transplantation of grafts, in Fonseca RJ, Davis WH (eds): Reconstructive Preprosthetic Oral and Maxillofacial Surgery. Philadelphia, PA, Saunders, 1986 14. Narang R, Wells H, Laskin DM: Ridge augmentation with decalcified allogeneic bone matrix in dogs. J Oral Surg 30:722, 1972 15. Pike RL, Boyne PJ: Use of surface-decalcified allogeneic bone and autogenous marrow in extensive mandibular defects. J Oral Surg 32: 177, 1974 16. Marx RE, Miller RI, Ehler WJ, et al: A comparison of particulate allogeneic and particulate autogenous bone grafts into maxillary alveolar clefts in dogs. J Oral Maxillofac Surg 42~3, 1984 17. Marx RE: The use of freeze-dried allogeneic bone in oral and maxillofacial surgery. J Oral Surg 39:264, 1981 18. Allard RH, Lekkas C, Swart JG: Autologous versus homologous bone grafting in osteotomies, secondary cleft repairs and ridge augmentation: A clinical study. Oral Surg Oral Med Oral Path01 64:269, 1987 19. Nique T, Fonseca RJ, Upton LG, et al: Particulate allogeneic bone grafts into maxillary alveolar clefts in humans: A preliminary report. J Oral Maxillofac Surg 45:386, 1987
MAXSON ET AL
20. Kraut RA: The use of allogeneic bone for alveolar cleft grafting. Oral Med Oral Surg Oral Path01 64:278, 1987 21. Troxell JB, Fonseca RJ, Osbon DB: A retrospective study of alveolar cleft grafting. J Oral Maxillofac Surg 40:721, 1982 22. Ramtjord SP, Ash MM: Periodontology and Periodontics: Modem Theory and Practice. St Louis, MO, Ishiyaku EuroAmerica, Inc, 1989 23. Ames JR, Maki KA: The autogenous particulate cancellous bone marrow graft in alveolar clefts. Oral Surg 51:588, 1981 24. Dragoo RM, Sullivan HC: A clinical and histological evalu-
941
ation of autogenous iliac bone grafts in humans. Il. External tooth resorptions. J Periodontol44:615, 1973 25. Himichs JE, El-Deeb ME, Waite DE, et al: Periodontal evaluation of canines erupted through grafted alveolar cleft defects. J Oral Maxillofac Surg 42:717, 1984 26. Buck BE, Malinin TI, Brown MD: Bone transplantation and the human immunodeficiency virus, in Urist MR (ed): Clinical Orthopaedics and Related Research. Philadelphia, PA, Lippincott, 1988 27. Friedland GH, Klein RS: Transmission of the human immunodeficiency virus. N Engl J Med 317:1125, 1987
Surg
1990
Bone for Secondary Alveolar Cleft 0s teoplas ty
Allogeneic
BARBARA B. MAXSON, DDS, MS,* STEVEN D. BAXTER, DDS,t KATHERINE W.L. VIG, BDS, MS, FDS, DORTH,$ AND RAYMOND J. FONSECA, DMD§ The purpose of this retrospective clinical study was to determine the efficacy of allogeneic bone for secondary alveolar cleft osteoplasty. Twentyfour patients with unilateral cleft lip and palate treated with allogeneic bone grafts were examined by a surgeon, orthodontist, and prosthodontist 20 to 47 months after surgery. Radiographic and clinical examination of the periodontal status of the teeth adjacent to the cleft and their antimeres were compared for differences with Student’s t test and the Wilcoxon test. Radiographs indicated complete bone bridging in 21 patients. Two of the remaining three patients had a l-mm radiolucent gap in the cleft site. The third patient had a 6-mm-wide radiolucency and recurrence of an oronasal fistula which was regrafted with autogenous bone. No statistically significant differences between the cleft and noncleft tooth antimeres were found for plaque, gingivitis, bleeding, sulcus depth, or level of attachment. A statistically significant difference in the amount of attached gingiva was found between the cleft and noncleft tooth antimeres. Nine patients with missing lateral incisor teeth avoided prosthetic replacement by orthodontic movement of the canine tooth into the grafted edentulous space. In those cases where the maxillary canine was unerupted at the time of the surgery, eruption into the graft occurred. Stability of the maxillary segments was sufficient to allow prosthodontic restoration with a fixed partial denture in those cases where it was indicated. cems, an influence on future maxillary growth has been reported. I-3 Although early surgical intervention may facilitate normal development of speech and address esthetic concerns, the effect on facial growth should be considered. Koberg4 reviewed the history of alveolar bone grafting in 1973. He discussed three basic schedules that had been reported for this procedure: 1) primary osteoplasty in the infant, 2) early secondary osteoplasty after the eruption of the deciduous dentition, and 3) late secondary osteoplasty after eruption of the permanent dentition. Reports of the adverse effects on maxillary growth after early surgical repair led Koberg to conclude that “. . . most severe maxillary deformities are to be expected as late results of primary bone grafting, so that late secondary osteoplasty remains the only justifiable form of bone transplantation in cleft surgery.” He also reported that attempts to use preserved bone instead of autotransplants generally resulted in failure.
The appropriate timing and technique for cleft lip and/or palate surgery has been a controversial issue among surgeons for many decades. Although early surgery to restore normal anatomic relationships may fulfill immediate functional and esthetic con-
Received from The University of Michigan, Ann Arbor. * Assistant Professor, Department of Oral Medicine, Pathology, Surgery. t Formerlv. Resident in Oral and Maxillofacial Surgery; ures- _ _ ently, in private practice, Columbus, OH. $ Associate Professor, Department of Orthodontics and Pediatric Dentistry. $ Formerly, Professor and Chairman, Department of Oral Medicine, Pathology, Surgery; presently, Dean, University of Pennsylvania School of Dentistry, Philadelphia. Address correspondence and reprint requests to Dr Maxson: Department of Oral Medicine, University of Michigan Hospitals, University Hospital Bl-B204/0018, 1500 E Medical Center Dr, Ann Arbor, MI 48109-0018. 0 1990 American geons
Association
of Oral
and Maxillofacial
Sur-
0278-2391/90/4809-0005$3.00/O
933
ALL0
934
A second review of alveolar cleft osteoplasty was made in 1985 by Witzenburg,5 who reported problems that occur when the alveolar cleft is not grafted. These include insufficient periodontal support for the teeth adjacent to the cleft, persistence of oronasal fistulae and associated sequelae, mobility of the maxillary segments with unfavorable conditions for prosthetics, relapse after orthodontic expansion of the collapsed maxillary segments, and a lack of bony support to the alar base resulting in asymmetry. He concluded that autogenous bone appeared to be the best graft material and that the majority of experiences with homologous or alloplastic materials were disappointing. Witzenburg also supported Koberg’s classification with the addition of the “secondary osteoplasty” to be performed during the mixed dentition. Since Witzenburg’s review, the efficacy of secondary osteoplasty has been reported by several authors,6-8 although primary osteoplasty may still be priferred at some institutions.“” Donor sites for harvesting the graft include iliac crest,’ rib,” mandibular symphysis,” and calvarium.‘* Rationale of Bone Grafting Although the results of early grafting procedures with allogeneic bone were disappointing, the effrcacy of allogeneic bone grafting for selected maxillofacial procedures has been evaluated in animal models. These onlay bone graft studies suggest that the vital autograft has a different biological response than the freeze-dried allograft. Allogeneic bone grafts rely on osteoinduction for new bone formation from both subperiosteal and endosteal sites. Revascularization of the graft is slower and final reorganization of the graft is delayed in comparison with the cellular response of autogenous grafts. Because the allograft acts only as a scaffold, replacement by new host bone is delayed.13 Reports from animal studies support the use of allogeneic bone grafting for maxillofacial procedures.13-16 Marx et all6 compared allogeneic maxillary cleft grafts with autogenous cleft grafts in a sample of 22 mongrel dogs. Their findings indicated that, although the allogeneic graft did induce bone formation, it was insufficient (30%) and protracted. They further stated that they would not expect such grafts to respond to passive tooth eruption, orthodontic or orthopedic forces, or growth forces in the maxilla. Several preliminary clinical studies have reported successful results with freeze-dried allogeneic bone for oral and maxillofacial procedures. Marx” used allogeneic graft material in 36 patients for cyst fill,
BONE FOR ALVEOLAR
CLEFT GRAET
osteotomy, ridge augmentation, and mandibular reconstruction. Allard et al’* reviewed 61 patients, 1 to 6 years after graft procedures for osteotomy, ridge augmentation, and secondary cleft repair. Comparison of clinical results, complications, and morbidity indicated that in selected cases, with appropriate surgical technique, frozen homologous bone was an alternative to autogenous bone in grafting procedures. A preliminary clinical report of 20 patients who received freeze-dried allogeneic bank bone for secondary repair of a unilateral alveolar cleft demonstrated bone bridging 3 to 6 months after surgery, both clinically and radiographically.” The ability of such grafts to permit orthodontic tooth movement through the graft and to allow passive tooth eruption could not be established from this short-term study. Most recently, Kraut*’ reported the results for five patients with unilateral alveolar clefts who received grafts with freeze-dried allogeneic bone. Passive eruption of the canine tooth through the graft occurred in four of the five cases. The purpose of this retrospective study was to review 24 unilateral cleft palate patients who had alveolar cleft grafts with allogeneic bone. Allogeneic bone as a grafting material was evaluated in terms of treatment outcomes using specific criteria of success and failure. Materials and Methods Forty-five patients were recalled for clinical and radiographic evaluation of secondary alveolar cleft grafts with allogeneic bone. Twenty-four of these patients were evaluated by an oral surgeon, orthodontist, and prosthodontist. All patients had bone grafts placed at The University of Michigan Hospitals at least 1 year prior to recall. Twenty-three of the patients received allogeneic cancellous bone chips and one patient received ground allogeneic bone. Preparation of the bone included reconstitution with saline and antibiotic as reported by Nique et aLI The surgical technique*’ involved full palate flaps for nasal, labial, and palatal closure. This technique is specifically designed to bring attached gingiva into the cleft defect. An acrylic resin splint was routinely wired to the teeth to protect the palate during healing. Fabrication of the splint necessitated relieving the maxillary cast with several layers of baseplate wax anteriorly and extending the acrylic resin just over the ridge crest of the surgical site. All patients were given preoperative antibiotics and steroids. They continued to receive the antibi-
MAXSONET AL
935
otic for 7 to 10 days and the steroid for 2 days postoperatively. Early ambulation, use of a bedside humidifier, and administration of a topical nasal decongestant were also part of the postoperative protocol. l9 Chart review and examination of all previous radiographs provided an historical data base for each patient. At the follow-up examination, periapical radiographs and anterior occlusal films were made of the grafted cleft area and adjacent teeth. These were evaluated by two oral surgeons for evidence of bone bridging and development of unerupted teeth. Patients were questioned about past or present problems related to the surgery, and each patient was examined and evaluated by a surgeon, an orthodontist, and a prosthodontist. Periodontal evaluation was performed by a single examiner using a University of Michigan periodontal probe. Plaque (Silness and Loe), gingivitis (Loe and Silness), exudate, calculus (Ramfjord), mobility (modified Miller), bleeding (Saxer and Muhlemann), pocket depth (Ramfjord), exposed root surface, and attached gingiva (labial only) were scored for each tooth immediately adjacent to the cleft and its antimere. Periodontal scores were averaged for each side and compared for differences with Student’s t test or a nonparametric alternative, the Wilcoxon test. Although most of the periodontal data were derived from ordinal scales, the two scores for each subject represented mean values from a number of observations which would approximate a normal distribution. Therefore, for some of the parameters where the assumption of normalcy could be made, the t test was applied. Results PREOPERATIVEFINDINGS
The average age of the patients (21 male, 3 female) at the time of surgery was 12 years 9 months (range, 9 years 0 months to 16 years 11 months). The presenting chief complaint at the time of surgery was need for alveolar cleft graft (lo), oronasal fistula (l), or both (13). Preoperative radiographs revealed no missing teeth in 12 patients, 1 missing tooth in 19 patients, and 3 patients missing 2 teeth associated with the cleft site. Canine root formation associated with the cleft was complete in 13 patients, but in 10 patients root formation was incomplete, and 1 patient was missing the succedaneous canine tooth. The average cleft width was 5.02 mm (range, 0 to 12.5 mm). One patient without a radiolucency in the cleft site
required the surgical procedure for closure of an oronasal fistula. Preoperatively, eight patients presented with retained deciduous or supernumerary teeth that required extraction at the time of the bone graft. Twelve patients received preoperative orthodontic treatment. OPERATIVE FINDINGS
Average estimated blood loss at surgery was 187 mL (range, 20 to 600 mL). Postoperative hospital stay was 1 to 2 days, with a mean of 1.46 days. Eleven patients in this sample had other surgical procedures in addition to the alveolar cleft graft in the same surgical field. These included 1 closure of a nasopalatine tistula, 1 lip revision, 1 nose revision, and extraction of retained primary or supernumerary teeth in 8 patients. POSTOPERATIVEFINDINGS
Splint removal occurred in an average of 10 days (range, 6 to 16 days). Postoperative infection developed in one patient 2 months after surgery. This patient was treated with antibiotics and proceeded to heal uneventfully. One patient experienced recurrence of the oronasal fistula and underwent a second procedure with autogenous iliac bone. The prevalence of dehiscence and sequestration is presented in Table 1. LONG-TERM FOLLOW-UP
Patients presenting for the follow-up examination were between 1 year 8 months and 3 years 11 months postsurgery (mean, 3 years 2 months). Of those interviewed, 15 patients recalled sequestration, but none recalled infection. Radiographic examination showed complete canine root formation in 21 patients. The remaining 3 patients varied in root development, 1 being threeTable 1. Prevalence of PostoPerative Dehircence and Sequestration
Natureof Finding
No. of Patients
Dehiscence
12
Sequestration
9
Occurrence 1-8 (mean,2.6) 1-7 (mean,2.3)
Time From Surgery
(mo) 1-14 l-18
936
ALL0 BONE FOR ALVEOLAR
Table 2.
CLEFT GRAFT
Periodontal Differences Between Tooth Antimeres (Parametric) t Test
Periodontal Parameter Plaque Gingivitis Sulcus depth (mm) Attached gingiva (mm)
Cleft 0.58 0.90 2.97 3.94
” 0.56 * 0.39 “_ 0.44 + 1.02
Noncleft 0.55 0.84 2.86 4.56
(O-1.75) (0.17-1.58) (2.25-3.92) (1.5-6.0)
-+ 0.40 2 0.37 f 0.34 2 1.05
(0.0-1.25) (0.0-1.50) (2.33-3.58) (3.0-6.5)
PS
P P P P
= = = =
.05 .74 .ll .23 .005
Values are given as mean i SD (range in parentheses).
quarters formed, 1 seven-eighths formed, and in 1 patient the cleft-associated canine tooth was absent preoperatively . Radiographic bony bridging was apparent in 21 patients. In the remaining 3 patients, findings were as follows: a gap of 1 mm in the graft site which appeared less radiopaque than the surrounding bone (this patient had one of the largest preoperative clefts), a l-mm radiolucent gap in a second patient, and in the third patient a 6-mm radiolucency that had been associated with a persistent fistula. This cleft was regrafted with autogenous bone 36 months later. Results from the periodontal examination are presented in Tables 2 and 3. No significant differences between cleft-associated teeth and their antimeres were found, except with regard to mobility and amount of attached gingiva. Chart review indicated that 15 patients had preoperative orthodontic treatment, while postoperative treatment had been performed for 20 patients. Of these, 5 were in active treatment and 5 had finished definitive orthodontic treatment at time of follow-up. In 21 patients, no surgical exposure of the canine tooth associated with the cleft site was necessary. In 2 other patients, development had not progressed sufficiently to determine the need for surgical exposure. In 1 patient, the tooth was absent. Orthodontic treatment to assist eruption and repositioning of the cleft-associated canine tooth was needed in 4 patients. In 18 patients, eruption of the canine tooth occurred uneventfully and in 1 patient, it was too soon to determine. From clinical and radiographic examination it was apparent that the permanent canine tooth had Table 3.
erupted into the bone graft in 9 patients (Fig 1). Movement of the adjacent teeth into the grafted cleft was demonstrated in 15 of the 24 patients in this study. Orthodontic and prosthodontic treatment, as well as orthognathic surgery, were recommended for some of the patients in this sample. The only patient in whom the allogeneic bone graft was unsuccessful had a cleft-associated tooth with loss of periodontal attachment and thus a compromised long-term prognosis. Prosthodontic examination indicated that no restorative treatment was necessary in nine patients in whom space closure was achieved orthodontitally. Eleven patients demonstrated a need for prosthodontic management. Five of these had a previous restoration that included one acrylic resin temporary fixed partial denture, one acid-etched composite resin-retained fixed partial denture, and three definitive fixed partial dentures. In four patients receiving active orthodontic treatment, prosthodontic treatment needs could not yet be determined. All patients had stable maxillary segments and, therefore, all were candidates for prosthodontic treatment with a fixed rather than removable partial denture (Fig 2). Of the 15 patients who had a residual edentulous space at the cleft site, seven demonstrated an adequate alveolar ridge for routine ridgelapped pontic placement. Four patients demonstrated deficiency in alveolar ridge which would require gingival porcelain to attain an acceptable esthetic result with fixed prosthodontics (Fig 3). In four patients it was too early to determine the need for prosthodontic treatment.
Periodontal Differences Between Tooth Antimeres (Nonparametric)
Periodontal Parameter Calculus Bleeding Exposed root (mm)* Mobility Exudate
Noncleft
Cleft 0.33 0.21 0.08 0.60
-+ 0.37 * 0.25 r 0.24 2 0.50 None
(O-1.0) (O-1.5) (o-1.0) (O-1.5)
Values are given as mean + SD (range in parentheses). * Since the distribution of these real numbers was skewed, a nonparametric
0.19 0.17 0.00 0.33
f + + 2
0.35 0.24 0.0 0.34 None
(o-1.0) (O-1.5) (.OO) (O-1.5)
test was applied to this data set.
Wiicoxon test (P s .05
P = .07 P = .56 P = .ll P=.oo4
937
MAXSON ET AL
FIGURE 1. The canine tooth will erupt through the ailogeneic bone graft if surgery is appropriately timed. A, Unerupted canine tooth asociated with the mature allogeneic bone graft. B, The canine tooth has been moved orthodontically through the graft to occupy the position of the missing lateral incisor.
Discussion The reduced morbidity from eliminating a second surgical donor site with allogeneic bone grafting is
probably most significant from the patient’s perspective. Typically, complaints concerning the iliac crest donor site relate to pain and difIiculty with ambulation. These far exceed complaints about the grafted area. Average blood loss with the single-site procedure was 187 mL as compared with 335 mL previously reported for the two-site procedure using iliac crest as donor bone.21 The surgical risks are reduced when a second surgical site is eliminated as a possible source of infection, increased blood loss, and additional anesthesia time. However, skepticism regarding the ability of allogeneic bone to produce comparable results to those using autogenous bone has been reported. 16,18*‘9 The results of this study indicate that freeze-dried allogeneic bone appears to be comparable in many respects to autogenous bone for alveolar cleft grafting. The ability of teeth to erupt through the graft and to respond to orthodontic forces makes allogeneic bone an alternative grafting option. The findings presented here are comparable to those from clinical studies that have used autogenous bone. Enemark et al’ found similar periodontal results when grafting prior to the eruption of the canine tooth and with adequate attached gingiva for teeth associated with the cleft. The need for secondary gingivoplasty, if attached gingiva is absent, is a prerequisite for an acceptable periodontal result. Our findings demonstrate that, although the height of attached gingiva was significantly less at the labial surface for the cleft-associated teeth than their antimeres, periodontal support was not compromised. In other words, significantly greater pocket depth or exposed root surface was not found as long as some attached gingiva was present. Enemark et al7 also described root resorption associated with the cleft grafts in a number of older patients which had previously been reported by Ames and Maki.23 External root resorption has also been associated with iliac crest cancellous bone used for augmentation of periodontal defects.24 Exposure of cementum or damage to the periodontal ligament is perhaps an explanation for failure rather than the type or origin of the bone graft material. Root resorption was not observed in our patients when allogeneic bone was used, provided that the timing of the graft was appropriate and the unerupted tooth not damaged during the surgery. Enemark found the optimum time for bone grafting of the unilateral cleft alveolus to be when maxillary growth was almost complete (8 to 9 years of age),’ prior to the eruption of the permanent canine tooth. Patients in this study who did not require prosthodontic treatment (37.5%) compared favorably with Enemark’s findings for unilateral clefts with autog-
FIGURE 2. Postoperative
Allogeneic bone grafting can be done in preparation for a fixed partial denture. A and B, Preoperative radiograph. D, There is satisfactory ridge form for esthetic pontic placement.
enous bone (youngest, 49%; middle, 27%; oldest, 8%). Since some of the patients in this sample were too young for final evaluation, the results are probably an underestimate. Hinrichs et a12’ reported the periodontal condition of teeth associated with unilateral cleft palate 2 to 8 years after secondary osteoplasty with autogenous iliac crestal bone. No significant difference between the cleft-associated canine tooth and the contralateral control canine tooth was found, which is in agreement with our clinica results and/or treatment outcomes. Statistically significant differences found in our study were not necessarily clinically significant. Differences in amount of attached gingiva appear to be significant for periodontal health only if there is a total absence of attached gingiva. Differences found in tooth mobility, although statistically significant, were so small that they were clinically insignificant.
findings. C,
FIGURE 3. When alveolar ridge contour after grafting is inadequate, but the alveolar segments are stabilized by the graft, gingival porcelain can be added to the pontic area of the fixed prosthesis.
MAXSON ET AL
FIGURE 4. Delayed osteogenesis of the bone graft is characteristic for the allogeneic alveolar cleft bone graft. A and B, Preoperative findings. C, Three-month postoperative radiograph. D, Seven-month postoperative radiograph. E, Ten-month postoperative radiograph. F and G, Twenty-eight-month postoperative findings.
940
Maxillary expansion is often indicated prior to the bone graft. Orthodontic tooth movement into the allogeneic bone graft site should be delayed for 3 months after surgery. The differences in biological response between autogenous and allogeneic bone can be explained by the autogenous bone graft which elicits an angioblastic proliferation from the recipient site during the first week after surgery. Survival of some of the transplanted osteoblasts allows osteogenesis to occur during the first few weeks of healing. In contrast, the allogeneic bone graft demonstrates a slower revascularization, with migration and proliferation of endothelial cells occurring 1 to 2 weeks later. The graft contributes no viable osteogenic cells, but apparently promotes osteoinduction. The angiogenic response is accompanied by new bone which is laid down at the periphery of the recipient site. As the osteoid is replaced by new bone, the nonviable graft bone is sequestered or removed as a foreign body by macrophages (Fig 4). Given these biologic differences, some cleft sites may be more responsive to autogenous bone. When the cleft is bilateral or there is an extensive alveolar defect with communicating oronasal Iistula, autogenous bone may be the preferred grafting material because of its ability to interact directly with the host tissues. A consideration associated with allogeneic bone grafts is the possibility of human immunodeficiency virus (HIV) transmission through the donor bone. The risk of transmitting HIV, as reported by Buck et al, is negligible. 26 Although safeguards against allowing infected tissue to enter the donor pool are not always infallible, estimates of the risk of receiving contaminated donor tissue can be made.27 However, it may be prudent for the surgeon to verify the safeguards used by the company producing the freeze-dried bone and be prepared to discuss the risks and benefits with the patient at the time of obtaining informed consent. With risk-benefit and cost effectiveness being important health care concerns, reduction in length of hospital stay and operating room time is a consideration when planning elective surgical procedures. As numerous social and biological issues impinge on the decision-making process in the delivery of health care, staying informed becomes increasingly more complex. Moral and ethical issues, along with economic and social pressures, will continue to influence the treatment planning process. Responsibility for selecting a treatment modality is presently shared by the clinician, the third-party carrier, and the patient. Clinicians need to evaluate the relative efftcacy of different treatment options from both risk-benefit and cost effectiveness view-
ALL0 BONE FOR ALVEOLAR
CLEFT GRAFT
points before recommending a treatment plan. logeneic bone grafts, with reduced morbidity similar outcome to autogenous bone grafts, may come a viable alternative treatment option in future.
Aland bethe
Acknowledgment The authors wish to thank Dr Charles J. Kowalski for assistance with data management.
References 1. Jolleys A, Robertson NRE: A study of the effects of early bone grafting in complete clefts of the lip and palate-Five year study. Br J Plast Sura 251229. 1972 2. F&de H, Johanson B: A foiow-up study of cleft children treated with primary bone grafting. Stand J Plast Reconstr Surg 888, 1974 3. Semb G: Effect of alveolar bone grafting on maxillary growth in unilateral cleft lip and palate patients. Cleft Palate J 25:288, 1988 4. Koberg WR: Present view on bone grafting in the cleft palate (A review of the literature). J Maxillofac Surg 1:185, 1973 5. Witzenburg B: The reconstruction of anterior residual bone defects in patients with cleft lip, alveolus, and palate. A review. J Maxillofac Surg 42:717, 1984 6. Bergland 0, Semb G, Abyholm FE: Elimination of the residual alveolar cleft by secondary bone grafting and subsequent orthodontic treatment. Cleft Palate J 23:175, 1986 7. Enemark H, Sindet-Pedersen S, Bundgaard M, et al: Combined orthodontic-surgical treatment of alveolar clefts. Ann Plast Surg 21: 127, 1988 8. Loh SA, Lee ST, Yeap CL: Evaluation of the effects of secondary bone grafting in both adults and children with cleft lip and palate. Ann Acad Med Singapore 17:4OO,1988 9. Rosenstein SW, Monroe CW, Kemahan DA, et al: The case for early bone grafting in cleft lip and palate. Plast Reconstr Surg 70:297, 1982 10. Helms JA, Speidel TM, Denis KL: Effect of timing on longterm clinical success of alveolar cleft bone grafts. Am-J Orthod Dentofac Orthoo 92:232. 1987 11. Sindet-Pedersen S, Enemark H: Mandibular bone grafts for reconstruction of alveolar clefts. J Oral Maxillofac Surg 46:533, 1988 12. Wolfe SA, Berkowitz S: The use of cranial bone grafts in the closure of alveolar and anterior palatal clefts. Plast Reconstr Surg 72:659, 1983 13. Feinberg SE, Fonseca RJ: Biological aspects of transplantation of grafts, in Fonseca RJ, Davis WH (eds): Reconstructive Preprosthetic Oral and Maxillofacial Surgery. Philadelphia, PA, Saunders, 1986 14. Narang R, Wells H, Laskin DM: Ridge augmentation with decalcified allogeneic bone matrix in dogs. J Oral Surg 30:722, 1972 15. Pike RL, Boyne PJ: Use of surface-decalcified allogeneic bone and autogenous marrow in extensive mandibular defects. J Oral Surg 32: 177, 1974 16. Marx RE, Miller RI, Ehler WJ, et al: A comparison of particulate allogeneic and particulate autogenous bone grafts into maxillary alveolar clefts in dogs. J Oral Maxillofac Surg 42~3, 1984 17. Marx RE: The use of freeze-dried allogeneic bone in oral and maxillofacial surgery. J Oral Surg 39:264, 1981 18. Allard RH, Lekkas C, Swart JG: Autologous versus homologous bone grafting in osteotomies, secondary cleft repairs and ridge augmentation: A clinical study. Oral Surg Oral Med Oral Path01 64:269, 1987 19. Nique T, Fonseca RJ, Upton LG, et al: Particulate allogeneic bone grafts into maxillary alveolar clefts in humans: A preliminary report. J Oral Maxillofac Surg 45:386, 1987
MAXSON ET AL
20. Kraut RA: The use of allogeneic bone for alveolar cleft grafting. Oral Med Oral Surg Oral Path01 64:278, 1987 21. Troxell JB, Fonseca RJ, Osbon DB: A retrospective study of alveolar cleft grafting. J Oral Maxillofac Surg 40:721, 1982 22. Ramtjord SP, Ash MM: Periodontology and Periodontics: Modem Theory and Practice. St Louis, MO, Ishiyaku EuroAmerica, Inc, 1989 23. Ames JR, Maki KA: The autogenous particulate cancellous bone marrow graft in alveolar clefts. Oral Surg 51:588, 1981 24. Dragoo RM, Sullivan HC: A clinical and histological evalu-
941
ation of autogenous iliac bone grafts in humans. Il. External tooth resorptions. J Periodontol44:615, 1973 25. Himichs JE, El-Deeb ME, Waite DE, et al: Periodontal evaluation of canines erupted through grafted alveolar cleft defects. J Oral Maxillofac Surg 42:717, 1984 26. Buck BE, Malinin TI, Brown MD: Bone transplantation and the human immunodeficiency virus, in Urist MR (ed): Clinical Orthopaedics and Related Research. Philadelphia, PA, Lippincott, 1988 27. Friedland GH, Klein RS: Transmission of the human immunodeficiency virus. N Engl J Med 317:1125, 1987
