Biologic Basis for Maxillary Osteotomies WILLIAM H. BELL Division of Oral Surgery, University of Texas Southwestern Medical School, Dallas, Texas 75235 ABSTRACT Adult Rhesus monkeys were used as experimental models to investigate revascularization and bone healing in different single-stage anterior, posterior and total maxillary osteotomy techniques. Microangiographic and histologic studies demonstrated that intraosseous and intrapulpal circulation to the mobilized maxillary segments were maintained by the experimental flap designs which maintained intact soft tissue; the fragments healed by osseous union within six weeks without immobilization of the mandible. The treatment of many severe dental-facial deformities is difficult and challenging. Functional and stable occlusions with facial balance and harmony have been attained in many adult patients by maxillary osteotomy techniques. The Rhesus monkey serves as an excellent experimental model to develop new biologically sound maxillary surgical orthodontic techniques. A large proportion of the adult population with dental-facial deformities due to severe malocclusion may never receive the benefits of orthodontic treatment. Many adults object to wearing orthodontic appliances for the prolonged period of time necessary to properly treat their malocclusion. Professional careers preclude many patients from wearing fixed appliances. The condition of the periodontium and missing posterior teeth which would usually serve a s anchorage teeth, may contraindicate treatment by orthodontics alone. The goal of surgical-orthodontic treatment of dental-facial deformities is to provide a functional occlusion with facial balance and harmony. Multiple operations may be necessary to attain these objectives as the clinical manifestations of such deformities often defy correction by a single surgical procedure. Unit recent years, surgical correction was focused on the mandible and frequently failed. However, with the introduction of anterior (CohnStock, '21; Wassmund, '35) and posterior maxillary osteotomies (Schuchardt, '61 ) and total maxillotomy (Axhausen, '34; Wassmund, '35), techniques which were pioneered by European surgeons, restoration of occlusal balance and facial harAM. J. PHYS.ANTHROP., 38: 279-290. mony was attainable in practically all cases. When maxillary surgical procedures were introduced to the United States (Kole, '59; Murphey and Walker, '63; Mohnac, '65; Obwegeser, '66), the rationale for using the various surgical techniques for correcting dental-facial deformities was empirical. Basic questions concerned with the healing of the surgical wounds produced by maxillary osteotomies had not been investigated. Many surgeons felt that the maxilla healed by fibrous union. Devitalization of teeth and bone in the mobilized segments had been reported. Varying degrees of relapse subsequent to posterior maxillary osteotomy (Schuchardt, '61 ) and total maxillary osteotomy were reported. The blood vessels necessary to maintain circulation to the mobilized bony segments and teeth had not been studied. Consequently both one-stage and two stage procedures were devised to prevent impairment of the vascular supply to the mobilized dental-alveolar segments (Schuchardt, '54). In 1965, a n animal investigation was designed to delineate the biology of maxillary osteotomy wound healing. Since then adult Rhesus monkeys have been used a s experimental models to investigate the re279 280 WILLIAM H. BELL Fig. 1 * Perfusion technique (modified after Rhinelander a n d Baragry). AV, air vent; CC, cannulated common carotid artery; FA, cannulated femoral artery; Hg, mercury; HP, house air pressure; M, “U” tube manometer; and P, perfusant. vascularization and bone healing associated with various maxillary techniques (Bell, ’69; Bell and Levy, ’70, ’71). The Rhesus monkey, Macaca mulatta, was selected as the experimental animal because of anatomic, physiologic, and dental similarities to the human. Since maxillary osteotomies are usually performed in adults, large, male Rhesus monkeys, 8 to 14 years of age, weighing a n average of 9 kg, were chosen for study. Acrylic splints were made from stone study models of each monkey’s dentition. Various one-stage anterior maxillary, posterior maxillary (fig. 3 ) and total maxillary osteotomies were performed by various flap designs. The mobilized maxillary segments were fixed with acrylic splints ligated to the anterior and posterior teeth with interdental wires. Because the mandible was not immobilized, the animals were fed a normal diet.’ Unoperated monkeys served as controls. The animals were killed 1, 3, 6 and 24 weeks after surgery. Before death each animal was premedicated and anesthetized. The right and left common carotid arteries were exposed, cannulated, heparinized and perfused with barium sulfate * under a constant pressure of 120 mm Hg (Rhinelander and Baragry, ’62; Bell, ’69) (fig. 1) . The heads were disarticulated and fixed in formalin. Microangiographic and histologic study was carried out after 1 Zu/Preem Science Diet, Theracon Laboratories, Topeka, Kansas. 2 Micropaque. Illustrations in figures 1-6 were included in the article, “Revascularization and bone healing after anterior maxillary osteotomy,” by W. H. Bell and B. L. Levy, in Journal of Oral Surgery April 1969. Illustrations in figure 7 were included i i the article, “Correction of skeletal type of anterior open bite,” by W. H. B,ell, in Journal of Oral Surgery, October 1971. Copyright by the American Dental Association. Reprinted by permission. BIOLOGIC BASIS FOR MAXILLARY OSTEOTOMIES 281 Fig. 2 Microangiograms of 1 mm transverse tissue slices from premolar (A) and molar region ( B ) of control animal: buccal (B), palatal (Pa), maxillary sinus (MS) and nasal cavity ( N ) blood vessels penetrating bone and anastomosing with intramedullary blood vessels ( I ) and periodontal vascular plexus (Pe); P, premolar tooth; M, molar tooth; T, turbinate. each maxilla was decalcified, dehydrated, cleared, and embedded in paraffin and beeswax. Serial 1 mm transverse, sagittal and horizontal tissue slices were cut from the specimens for microangiographic study. Each 1 mm tissue slice was then cut at 7 for histologic study. RESULTS Control animals. The injection medium was distributed through most of the cancellous intraosseous, intrapulpal and soft tissue blood vessels (fig. 2). The maxilla was vascularized by a highly complex interconnected network of vessels that terminated in the gingiva and mucosa as capillary loops of variable length (Bell and Levy, '71). All dental osseous components received blood from a multiplicity of sources. Gingival, buccal, labial, palatal, nasal, and maxillary sinus vessels penetrated and traversed the cortical bone and anastomosed with the periodontal plexus encircling the teeth. Dental pulps were vascularized by interosseous dental alveolar vessels and branches from the periodontal plexus. Submucosal palatal vessels anastomosed near the midline of the palate with vessels from the opposite side. Buccal and gingival tissues received blood from buccal soft tissues and from intraalveolar vessels. Soft tissue and intraosseous vessels 282 WILLIAM H . BELL supplied blood to the reticulated vascular plexus making up the periosteum. Vessels of the gingiva, periodontal plexus, lingual mucosa and labial alveolar mucosa were interconnected by vascular anastomoses. The nasal cavity was lined with a vascular net work of variable thickness; the turbinates by a relatively thick vascular plexus that was surrounded by a thin reticulated vascular plexus. The avascular nasal septum was covered by a reticulated vascular plexus. Experimental animals. The surgical soft tissue wounds produced by various flap designs healed by primary intention, without detectable postoperative infection. The dental alveolar segments were freely movable one week after surgery and slightly movable after three weeks. After six weeks there was clinical union of the osteotomized segments. The individual teeth in the mobilized bone segments remained stable. There was generalized distribution of the micropaque throughout the intraosseous and intrapulpal tissues of all mobilized osseous segments (figs. 4, 5). The pulp BIOLOGIC BASIS FOR MAXILLARY OSTEOTOMIES e Fig. 3 Schematic drawing of soft tissue and bone incisions used for posterior maxillary osteotomy in experimental animals. canals of several teeth adjacent to the vertical interdental bone cuts were not vascularized because their apical blood supply was severed by labial and buccal bone cuts through the teeth apices. The pulp canals of all other teeth, however, were viable and vascularized despite the fact that vertical interdental osteotomies were made between closely spaced teeth and subapical bone cuts just above the apices of teeth, Microangiographic study of the one week 283 specimens revealed focal areas of intraosseous ischemia in the margins of the sectioned alveolar bone segments that were separated by a n avascular zone (fig. 4). Within three weeks the circulation between all of the sectioned bone fragments had been reconstituted. The raised buccal and labial soft tissue flaps were reattached to the underlying bone as shown by the many periosteal blood vessels penetrating the buccal and palatal cribriform plates and anastomosing with intraosseous blood vessels and the periodontal vascular plexus (fig. 5 A ) . Histologically, there was a n intense osteoblastic proliferation within the marrow spaces and around many of the spicules of the spongiosa (fig. 5B). Minimal osteonecrosis was found throughout the mobilized maxillary bone segments. Some empty lacunas were present in the proximal and distal margins of the bone incisions. Six weeks after the osteotomies there was no detectable intraosseous or intrapulpal ischemia. The reparative response in the endosteal vascular bed appeared more intense than it did in the periosteal vascular bed. Histologically, the proximal and distal bony segments were united with cancellous bone. Twenty-four weeks after maxillary osteotomies, the periosteal and endosteal circulatory beds had been virtually reconstituted to their normal vascular architecture. The endosteal-periosteal anastomosis through cortical bone had been restored. Histological examination of the osteotomy wounds revealed healing of the cortical bone and remodeling of the spongiosa. DISCUSSION The results of these clinically analogous animal studies indicated that single-stage anterior, posterior, and total maxillarv osteotomies were biologically sound surgical procedures. Preservation of the integrity of the incisive canal or greater palatine arteries was not essential to maintain circulation to the anterior or posterior maxillary dental alveolar segments. The intraosseous and soft tissue collateral circulation and the freely anastomosing gingival, palatal, floor of the nose, maxillary sinus, and periodontal plexuses, per- 284 WILLIAM H . BELL Fig. 4 osteotomy avascular maxillary Microangiogram of 1 mm sagittal tissue slice one week after posterior maxillary shows generalized intraosseous and intrapulpal distribution of injection medium; zone (arrows) between margins of vertical bone cut between premolar teeth; MS, sinus; C, canine tooth; T, tuberosity. mitted many technical variations of maxillary osteotomies, without jeopardizing the blood supply to the maxillary dental alveolar segments (fig. 6). Intraosseous and intrapulpal circulation was not significantly altered by interdental and subapical alveolar osteotomies when the bone cuts were made away from the apices of the teeth; maximal attachment of the mucoperiosteum on the lingual or buccolabial surface of the mobilized osseous or dentalosseous segments was preserved. When carefully pedicled flaps were used to maintain these attachments, the segments could be mobilized and transposed safely in any direction. The encouraging results attained in the animal wound healing studies generated much enthusiasm and confidence in clinical maxillary osteotomies. Adult dentalfacial deformities which previously could not be treated by either mandibular surgery or orthodontics without severely compromising the result, could now be treated in a practical period of time. Treatment of such a case (skeletal type of anterior open bite) is shown in figure 7. Multiple maxillary osteotomies, genioplasty and orthodontics effected a stable and functional occlusion with facial balance in 14 months. Since 1967, 20 skeletal Class I1 malocclusions have been treated by anterior maxillary osteotomy, genioplasty and orthodontics (12 patients had no orthodontics; 8 patients had orthodontics). The average treatment time was approximately nine BIOLOGIC BASIS FOR MAXILLARY OSTEOTOMIES 285 Fig. 5A Microangiogram of 1 mm transverse tissue slice from first molar region three weeks after posterior maxillary osteotomy shows proliferation of endosteal ( E ) and periosteal ( P ) circulatory beds; reattachment of buccal and palatal mucoperiosteal flaps to underlying bone; vascularization of pulp canal from periodontal vascular plexus and accessory root canal (arch); Buccal ( B ) ; and palatal osteotomy sites ( P a ) ; nasal cavity ( N C ) ; first molar tooth ( T ) . months. Five patients with retromaxillism associated with mandibular prognathism were treated by surgically advancing the entire maxilla (total maxillary osteotomy). Seventeen patients with bimaxillary dental protrusion were treated by surgical ortho- dontic techniques in a n average of 8.5 months. Long-term clinical and radiographic studies of the patients who have had maxillary alveolar surgery showed no periodontal problems and minimal crestal alveolar Fig. 5B Photomicrograph of buccal bone. Periosteum is thickened by fibrous connective tissue. Osteophytes are seen beneath periosteum. Osteoid and new bone bridge fragments. Endosteal osteoid appears limited to proximal fragment ( H & E, original magnification X 8). Fig. 6 Schematic composite illustration of showing freely anastornosing gingival plexus, artery, intraalveolar vessels, apical vessels, and mits anterior maxillary osteotomies without maxillary segment and teeth. blood supply to anterior maxillary region palatal plexus, periodontal plexus, labial pulp vessels. This vascular architecture percompromising circulation to the anterior BIOLOGIC BASIS FOR MAXILLARY OSTEOTOMIES Fig. 7A Facial profile before treatment Fig. 7B 287 Facial profile after treatment. Fig. 7 Case Report. Skeletal type of anterior open bite with Class I1 malocclusion treated in 14 months by surgical-orthodontic techniques. Maxillary canine teeth were extracted to facilitate posterior maxillary osteotomies and retraction of procumbent maxillary incisors. Lower first premolar teeth were extracted to allow orthodontic correction of crowded mandibular dental arch. Fig. 7C Occlusion before treatment. 288 WILLIAM H. BELL Fig. 7D Occlusion after 14 months of surgical-orthodontic treatment. of treated cases demonstrated remarkable stability of dental-skeletal changes effected by maxillary osteotomies. They also showed minimal resorption of the transposed mental symphysis bone segments. ACKNOWLEDGMENTS The author wishes to thank Miss Rebecca Sprowls, Miss Judy Peterson, and Mrs. Dorothy Gilbert for technical assistance in preparing this paper. Fig. 7E Posterior maxillary osteotomy to level maxillary occlusal plane; vertical facial dimension is reduced and chin contour restored by anterior sliding genioplasty. bone loss in the interdental osteotomy sites (between 1 and 2 m m ) . (Bell and Dann, in press). All teeth in the alveolar segments, except one (subsequently retained by endodontic therapy), tested vital within eight months after surgery. There was no radiographic evidence of root resorption. Long-term cephalometric studies LITERATURE CITED Axhausen, G. 1934 Zur Behandlung veralteter disloziert gehhilter Oberkieferbrueche. Dtsch. Zahn Kieferheilkd, I : 334. Bell, W. H . 1969 Revascularization and bone healing after anterior maxillary osteotomy: a studying using adult rhesus monkeys. J. Oral Surg., 27: 249-255. 1971 Correction of skeletal type of anterior open bite. J. Oral Surg., 29: 706-714. Bell, W. H., and B. M. Levy 1970 Healing after anterior maxillary osteotomy. J. Oral Surg., 28: 728-734. 1971 Revascularization and bone healing after posterior maxillary osteotomy. J. Oral Surg., 29: 313-320. BIOLOGIC BASIS FOR MAXILLARY OSTEOTOMIES 289 'Lr Fig. 7F Schematic diagram showing buccolabial mucoperiosteal flap design for anterior maxillary osteotomy; horizontal subapical osteotomy is directed palatally to and through palatal cortical plate; digital pressure on palatal mucosa indicates when lingual cortices are sectioned; vertical interdental bone cuts are facilitated by envelope type of flaps of labial epithelium ( incision ). Bell, W. H., and J. Dann 1973 Correction of Class I1 Malocclusion by anterior maxillary ostectomy and genioplasty. Amer. J. Orthodont., in press. Cohn-Stock, G. 1921 Die chirurgische Immediatregulierung der Kiefer, speziell die chirurgische Behandlung der Prognathie. Vjschr. Zahnhk., 37: 320. Kde, H. 1959 Surgical operations on the alveolar ridge to correct occlusal abnormalities. Oral Surg., 1 2 : 515. Mohnac, A. M. 1965 Surgical correction of maxillomandibular deformities. J. Oral Surg., 23: 393-407. Murphey, P. J., and R. V. Walker 1963 Correction of maxillary protrusion by ostectomy and Fig. 7G Cephalometric tracings before (solid line) and after (broken line) treatment, showing reduction of anterior facial height, restoration of chin contour, closure of open bite, improved lip posture and lip seal, and leveled maxillary occlusal plane. orthodontic therapy. J . Oral Surg., Anesth., Hosp. Dent. Serv., 21: 275-290. Obwegeser, H. 1966 American Society of Oral Surgery comprehensive conference on oral surgery, Walter Reed Army Medical Center, Washington, D. C., June 20. Rhinelander, F. W., and R. A. Baragry 1962 Microangiography in bone healing. I. Undisplaced closed fractures. J . Bone Joint Surg., 44-A: 1273-1298. Schuchardt, K. 1954 Die Chirurgie als Helferin in der Kieferoethopadie. Fortschr. Kieferorthrop., 1 5 : 1. 1961 Experiences with the surgical treatment of some deformities of the jaws: prognathia, micrognathia, and open bite. In: International Society of Plastic Surgeons, transactions of second congress, London, 1959, E. & H. Livingstone, Publishers, Edinburgh. Wassmund, J. 1935 Lehrbuch der praktischen Chirurgie des Mundes und der Kiefer. Vol. 1. Leipzig, Meusser.