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Tooth pulp changes following Le Fort I maxillary osteotomy in a primate model
Bririch Journal 0
of Ora/
1990 The British
and MeriNofocinl
Association
Surgery
(1590) 28, l-7
of Oral and Maxillofacial
Surgeons
Tooth pulp changes following Le Fort I maxillary osteotomy in a primate model R. M. Browne, C. L. Brady, J. W. Frame Department of Oral Surgery and Oral Pathology, Birmingham Dental School, Birmingham West Midlands Plastic and Jaw Surgery Unit, Wordsley Hospital, West Midlands _-
.~.
~
-
_
and The
.~.
SUMMARY. Le Fort I maxillary ‘down-fracture’ osteotomy with 8 mm advancement was performed in 15 adult rhesus monkeys. Forty-five tooth pulps were examined histologically at intervals from 0 to 24 weeks after surgery. Cell degeneration occurred in 31% of pulps examined, necrosis in 16% of pulps and osteo-dentine was found in 7% of pulps. Almost half of the teeth examined (47%) showed marked cellular changes, more frequently found in posterior teeth. Other features noted were inflammation (13%) and reactive dentine in pulps (24%). Axons degenerated initially but recovered by 24 weeks. It is concluded that Le Fort I maxillary osteotomy caused pulpal disturbances in an animal model and the extent to which this occurs in patients needs to be carefully monitored. .-.~ .--..
of pulps showed pathological changes. Conflicting results have also been reported of tooth response after segmental osteotomy procedures in the maxilla. Studies in patients show the incidence of non-responsive teeth to electrical stimulation varying from 6 to 43% after surgery (Table 1). Animal studies have also demonstrated wide variation in the effect on the pulp, varying fron nil to marked cellular changes (Table 2). It is interesting to note that in the animal studies where there was minimal movemen af the bone and tooth segments little effect on the pulp was noted. However, in the two experiments where the total maxilla was superiorly repositioned 5 mm (Nanda et al., 1982) and the anterior maxilla moved 10 mm (Poswillo, 1972), changes were detected in the tooth pulps. These latter two studies were more analogous to the clinical situation in patients where substantial movement of the osteotomiscd bone and teeth is undertaken to correct the dento-facial deformity. The aim of this present study was to determine in an animal model the effect on the tooth pulps of Le Fort I maxillary osteotomy, where the maxilla was moved forwards a distance which simulated normal clinical practice in patients.
INTRODUCTION
A common clinical finding after Le Fort I maxillary osteotomy is that the patient initially experiences some loss of tooth sensitivity, which gradually resolves after several months. However, it is unclear what effect maxillary osteotomy has on the structure of tooth pulps and what are the possible long term sequelae. Studies after Le Fort I maxillary osteotomics in patients and animals have provided conflicting results. Tajima (1975) found 15% of 245 teeth in 27 patients non-responsive to electric pulp testing 14 months after Le Fort 1 ostcotomy or fracture. In the study by de Jongh et al. (1986), 29% of 128 teeth tested in 10 patients after a mean period of 14 months were non-responsive. However, Kahnberg and Engstrom (1987) reported that 90 to 100% of teeth in 20 patients gave a positive response to electric pulp stimulation 18 months after surgery. The variation in the results of these studies may be partly due to the unreliability of electric pulp testing in evaluating the health of the pulp. It has been shown that a tooth responding to electrical stimulation may have a pulp histology varying from normal to fibrosis and inflammation (Mumford, 1967). A study by Bell et al. (1975) in 12 adult rhesus monkeys showed early osseous union, minimal transient vascular ischaemia and minimal osteonecrosis after Lc Fort I osteotomies. However, the maxilla was not transposed into a new position and no tension applied to the soft tissue pediclc. In addition, the authors relied mainly on angiograms to assess pulp vascularisation and health, with little histological data. Nanda et al. (1982) surgically repositioned the maxilla 5 mm superiorly in four adult Macaca irus monkeys and after 150 days the majority
MATERIALS
AND METHODS
The animal model chosen was the adult rhesus monkey because of its anatomical and vascular similarities to humans (Castelli & Huelke, 1965). They weighed between 4.5 and 6 Kg and females were utilised because of the short canine teeth. The surgical procedures were performed under general endotrachcal anaesthesia using nitrous oxide, oxygen and halothane. A standard Le Fort I maxillary 1
2
British Journal of Oral and Maxillofacial Surgery
Table 1 - Tooth Pulp Response to Electric Pulp Stimulation after Segmental Maxillary Osteotomy
Johnson & Hinds (1969) Leibold et al. (1971) \ I
(2-36) 6 12
Hutchinson & MacGregor (1972) Pepersack (1973) Theisen & Guernsey (1976)
No. of teeth
% nonresponsive
17
169
20
18
108
43
12 143 10
58 588 72
7 6 10
No. of patients
Months after surgery (range)
Author
Table 2 _ Tooth Pulp Changes after Anterior Maxillary Segmental Gsteotomy in an Animal Model Author
Animals
Bell, (1969)
6 macaca mulata monkeys 9 rhesus monkeys 2 macaca irus monkeys
Ware & Ashamalia (1971) Poswillo (1972)
Segments moved 0
Follow-up (weeks)
Histology of pulp
l-6
Intra-pulpal circulation maintained. No histology of pulps No histological abnormalities Loss of odontoblasts and nerves. Progressive fibrosis. Islands of metaplastic bone in pulps No degenerative changes apart from nerves, which later regenerated Mild changes-reduction in odontoblast layer-pulpal fibrosis. All DUIDS vital
2mm 10 mm
l-24 8-24
Sugg et al. (1981)
6 macaca fascicularis monkeys
2mm
l-24
Zisser & Gattinger (1982)
9 dogs
0
l-8
in 15 animals (Bell et 1977). A horizontal incision was made through the mucoperiosteum high in the buccal and labial sulcus, extending from first molar to first molar. The margins of the superior flap were raised to expose the anterior and lateral walls of the maxilla and identify the infra-orbital nerves. The subperiosteal dissection was tunnelled back to the pterygomaxillary junction. The osteotomy cut was made with a fissure bur, extending from the pyriform aperture to pterygoid region bilaterally. The bone cuts were made at least 5 mm above the apices of the teeth. However, because of the length of the roots, the apices of the canine teeth were usually transected. Osteotomes were used to section the nasal septum and lateral walls of the nasal cavity and to separate the posterior maxilla from the pterygoid plates. The maxilla was ‘downfractured’ using manual pressure, retaining its blood supply through the soft-tissue pedicle of the palate and buccal gingivae. Some trimming of the vertical portions of bone was required to allow 8 mm forward movement of the maxilla. Fixation of the maxilla was achieved by two vertical and one oblique interosseous wire on each side, to stabilise the maxilla in its anteriorly displaced position. The lateral walls of the maxilla were relatively thick and no other fixation was necessary. Intermaxillary fixation was not required. The soft tissues were closed with 3-O silk sutures. Postoperative antibiotics and analgesics were given for 1 week. The monkeys recovered well after surgery and managed food and fluids without difficulty. Liquidised foods was provided for the first week, osteotomy
was performed
al., 1975; Bell, 1975; Bell & McBride,
Table 3 - Duration of Follow-up After Surgery
Time after surgery (weeks) Number of animals
Immediately
1 2
1
22122
3
4
8
12 16 24 212
then soft food for 1 week, after which the animals resumed a normal laboratory diet. Palpation indicated that the maxilla in each animal united satisfactorily in its new position. Two unoperated monkeys served as controls. The 15 operated animals were killed at intervals after surgery ranging from immediately to 24 weeks (Table 3). At the end of the experimental period, each animal was anaesthetised, the common carotid arteries were exposed bilaterally, cannulated and perfused with barium sulphate (‘Micropaque’) in normal saline, using a technique similar to that of Bell (1973). The perfusion medium was then changed to barium sulphate in 10% neutral buffered formalin. The major blood vessels in the neck were ligated, the head removed and placed irrlO% neutral buffered formalin. The perfusion procedure ensured that the formalin fixed the delicate pulp tissue to preserve cellular detail and the barium sulphate allowed demonstration of vascular architecture using microradiographs. After fixation for at least 48 h, the maxilla was dissected out, radiographed and then sectioned in the midline sagittal plane using a rotating diamond saw. From each animal, one half maxilla was processed to investigate the healing process of the bone
Tooth pulp changes following Le Fort I
3
Table 4 - Summary of the Main Histological Features
Number of Weeks after Surgery Immediate _ Cell degeneration Necrosis Inflammation Reactive dentine Osteodentine Axons
1
1
PM
IPM
223
4
M
M
4
8
PM
8 M
P PM IPM
M
M I
IPM
IPM P = Premolar;
defect. The other half was used to study the histology of the tooth pulps and is the subject of this report. Each half maxilla was sectioned with a diamond saw to produce six separate tissue blocks, each containing a single.tooth together with the surrounding hard and soft tissues. Blocks were prepared of each of the following: central incisor, lateral incisor, first premolar, second premolar, first molar, second molar. The canine was omitted because its large, curved root made orientation difficult and the apex had often been transected during the osteotomy procedure. The central incisors, second premolars and .second molars were prepared for routine histology. The blocks were decalcified in 10% formic acid, double embedded in celloidin and paraffin wax and serial sections ‘prepared at ‘8 urn through the tooth pulps in the bucco-palatal plane. Every tenth section was stained with haemotoxylin ,and eosin and selected sections by Linder’s nerve staining method. The lateral incisor, first ‘premolar and first molar were plastic embedded in LR Epoxy Resin (hard mix). The teeth were again sectioned ‘in the buccopalatal plane. After, initial orientation of the blocks, a 1 mm thick section’was cut for microradiography using the Leitz 1600 saw microtome. The 1 mm slices were demineralised in 10% formic acid and microradiographs prepared using a Grenz X-ray machine.
RESULTS Thel,‘histological features are described below land sum@rarise~din Table 4. Im~ediute: The pulps of the teeth ,from the osteotomy specimen obtained immediately ‘after ,,the operative: procedure and from unope&ated animals served as ‘controls. All the pulps were essentially norm& in appearance (Fig. l), with peril&rally placed ‘regular layers of odontoblasts and cellular fibro-vascular tissue comprising the majority of ‘the tissue. There was some slight irregularity of “the odontoblast layer in the premolar an& molar teeth from the immediate postoperative animal which might have arisen as a consequence of the surgery. Linder’s stain demonstrated prominent nerve bundles in the root canals (Fig. 2) a&coronal pulps of all teeth with individual axons periiherally in the subodontoblastic and odontoblastic layers.
24
24
PM
PM
I PM IPM
I M IPM
I PM M M IMI
I I
(I = Incisor;
12 12 16
IP PM
I I
IP
Pulps affected 14 (31%) 7 (16%) 6 (13%) 11 (24%) 3 (7%)
M = Molar tooth)
One week. There was evidence of degenerative changes in the pulps of the premolar and molar teeth in both animals and of the incisor of one. The odontoblast layer was less regular than normal, contained fewer cells and those present were shrunken with rounded pyknotic nucleii (Fig. 3). The pulps of all three teeth from one animal were diffusely infiltrated by polymorphonuclear leucocytes (Fig. 4). The apex of one root of the molar in this animal had been sectioned in the oestotomy cut. In all the teeth, the pulpal nerves exhibited neuronal degeneration, staining in an irregularly granular pattern. Two weeks. Apart from one molar, all the pulps appeared healthy. Odontoblasts were slightly irregular where the predentine layer exhibited’ a slight increase in width. In one molar, there was marked degeneration of the fibroblasts and complete degeneration of the odontoblasts, A diffuse infiltrate of polymorphonuclear leucocytes and’ macrophages was present. Again, in this molar the apical ,part of one of the roots had been sectioned in the osteotomy cut. Axonal degeneration was complete in ,a11 the pulps so that the nerve bundles persisted but did not contain any stainable axons. Three weeks. The incisor and premolar pulps appeared normal. The incisor exhibited some incisal attrition with a small deposit of reparative dentine at the pulpo-dentinal junction and contained a pulp stone in the root canal. The molar tooth showed advanced necrosis of ‘*the pulp with nearly total degeneration of the odontoblasts and fibroblasts and some scattered polymorphonuclear leucocytes and macrophages in the tissue remnants. Again axonal degeneration was complete and the neurilemmal bundles persisted (Fig.8 5), even in the degenerating pulp, but contained only occasional globules of stainable axonal tissue : Four weeks. Both incisor pulps were of normal appearance apart from the presence of substantial deposits of reparative dentine (Fig. 6) incise-palatally at the pulpo-dentinal :boundary. There was’incisal attrition in both teeth? In one of the animals1 there was some reduction in cell numbers in the ddontoblast layer in both the premolar and molar reeth, together with slight deposition of reparative dentine occlmally. In the other animal, although the premolar pulp was nearly totally necrotic (Fig. 7), the molar pulp appeared normal apart from the persistence of an occasional cell with pyknotic nucleus. All pulps demonstrated total axonal degeneration.
4
British Journal of Oral and Maxillofacial Surgery
Fig. 1 - Incisor (immediate): normal pulp with pseudostratified odontoblast nuclei peripherally and cellular fibro-vascular tissue. Haematoxylin and eosin. Original magnification x200.
Fig. 4 - Premolar, 1 week postoperatively. The odontoblast layer is shrunken and composed of cells with pyknotic nuclei. The pulp contains a diffuse infiltrate of polymorphonuclear leucocytes. Haematoxylin and eosin. Original magnification x 125.
Fig. 2 - Incisor (immediate): normal pulp showing several nerve bundles containing darkly staining axons. Linder’s method. Original magnification X310.
Fig. 5 - Incisor, 3 weeks postoperatively. A neurilemmal bundle crosses the field containing occasional dark-staining axonal remnants. Linder’s method. Original magnification x310.
Fig. 3 - Premolar, 1 week postoperatively. The odontoblast layer is shrunken and the cell nuclei, rounded and pyknotic. Haematoxylin and eosin. Original magnification x200.
Fig. 6 - Incisor, 4 weeks postoperatively. An irregular deposit of reactive dentine is present in&o-palatally. Haematoxylin and eosin. Original magnification X310.
Tooth
Fig. 7 - Premolar, 4 weeks postoperatively. The pulp is necrotic but contains the residual outlines of blood vessels. Haematoxylin and eosin. Original magnification x50.
Eight weeks. The incisors of both animals appeared normal, containing small deposits of reparative dentine incisally where there had been attrition. In one animal the premolar and molar pulps demonstrated some reduction in cellularity in both the odontoblast and fibroblast populations and in the molar, focal groups of chronic inflammatory cells were also present. In the other animal, both the premolar and molar had undergone complete pulpal necrosis. In the molar there was a periapical abscess in association with the buccal root. The osteotomy cut had passed very close to this root apex, although not actually through it. In only one incisor pulp were there any axons demonstrable. In all the other teeth, there were no stainable axons. Twelve weeks. The incisor pulp of one animal had undergone complete necrosis and there was marked incisal attrition. The premolar and molar pulps were essentially normal although there was a slight reduction in the number of odontoblasts. In both teeth there was deposition of reparative dentine occlusally and in one of them on the vertical walls of the coronal pulp as well. In the other animal, the incisor pulp was normal apart from a small deposit of reparative dentine incisally at the pulpo-dentinal junction. There was evidence of incisal attrition. The pulps of the premolar and molar were both almost totally necrotic, although a small remnant of vital pulp tissue was present in the apical part of the root canal of the premolar. A localised deposit of reparative dentine was present in one pulp horn of the molar. In the three teeth with vital pulps, numerous nerve bundles with clearly defined axons were present. Sirfeen weeks. The pulps of the incisor and premolar were normal apart from some reduction in the number of cells in the odontoblast layer. Both exhibited attrition of the incisal or occlusal surfaces beneath which, in the incisor, there was a localised deposit of reparative dentine. Both pulps contained numerous darkly staining axonal fibres. In the molar, the pulp had undergone total necrosis. Twenty-four weeks. The incisors had normal pulps. In both there had been incisal attrition with small
pulp changes
following
Le Fort I
5
Fig. 8 - Molar, 24 weeks postoperatively. The pulp tissue has been replaced by osteodentinc. Iiaematoxylin and eosin. Original magnification X50.
Fig. 9 - Premolar, 24 weeks postoperatively. Numerous darkly staining axons are present in the peripheral part of the pulp. Linder’s method. Original magnification x200.
deposits of reparative dentine at the pulpo-dentinal junction. In one animal the most recently formed circumpulpal dentine showed a less homogenous staining reaction of its matrix, suggesting a disturbance in dentinogcncsis. Of the two premolars, one pulp was of normal structure apart from some reduction in the cell population of the odontoblast layer. The other pulp exhibited total degeneration of the odontoblasts and a marked reduction in the number of fibroblasts in the pulp stoma, which had undergone fibrosis. The entire pulpal surface of the dentine was covered by a layer of osteodentine which was also present as discrete deposits throughout the pulp. The molar tooth from both animals exhibited similar changes, namely marked cellular degeneration, pulpal fibrosis and extensive deposition of osteodentine (Fig. 8). However, in one tooth the roots had been sectioned in the osteotomy cut and the gaps between the cut surfaces had been repaired by deposition of osteodentine. Deposition of osteodentine at the apex of one root had resulted in ankylosis. Although cellular degeneration and tibrosis were marked in both molars and in one premolar, there were a number of patent blood vessels present, all of which contained the perfused radiopaque
6
British Journal
of Oral and
MaxillofacialSurgery
Fig. 10 - Microradiographs demonstrating the vasculature of a vital premolar (A) and its absence in a molar with necrotic pulp (W.
medium. In all the teeth axons were demonstrated by nerve staining (Fig. 9). The microradiographs confirmed the histological findings concerning the viability and vascularity of the pulp (Fig. 10A). However, no obvious differences on microradiographs were observed between normal pulps and those exhibiting features of cellular degeneration. In necrotic pulps no vessels containing contrast medium were present (Fig. 10B).
DISCUSSION Histological examination of 45 teeth in 15 monkeys at varying times after Le Fort I maxillary osteotomy indicated that 14 pulps (31%) exhibited cell degeneration and 7 pulps (16%) were necrotic. Thus, 21 teeth (47%) showed signs of marked cellular changes,
affecting mainly the premolars and molars. Three molar teeth had apices inadvertently transected during osteotomy of the bone and in one other molar, the cut was close to the apex. The pulps of these four molars all showed cellular degeneration or necrosis. Histological examination of the molar with the transected apex after 24 weeks demonstrated that the gap in the root was repaired with osteodentine, and that the pulpal blood vessels were patent. If these four molar teeth are eliminated from the data, 11 pulps (25%) showed cellular degeneration and 6 pulps (13%) necrosis, resulting in 17 teeth (38%) with marked cellular changes after surgery. Other less severe histological changes were also observed. Inflammation was noted in 6 pulps (13%) within the first 8 weeks after surgery, but not at later stages. Reparative dentine was found in 11 pulps (24%) at times from 2 weeks to 24 weeks, and affected mainly incisors. It was deposited on the pulpal surface of the dentine, predominantly beneath the incisal edges, and usually associated with attrition of the enamel. The formation of the reparative dentine may have been caused by occlusal trauma related to the abnormal occlusion after surgery. The odontoblasts and pulp tissue in these teeth were otherwise normal in appearance. Osteodentine occurred in 3 teeth (7%) at 24 weeks, and was associated with marked cellular degeneration and fibrosis of the pulp. Although osteodentine formation is probably a consequence of impaired blood supply, patent blood vessels containing barium sulphate were present within these 3 pulps. Axons degenerated after surgery and regeneration, which began after 8 weeks, appeared complete by 24 weeks. The microradiographs confirmed the histological findings in healthy or necrotic pulps, but were not sufficiently sensitive to detect subtle changes. It is important that histological data is also available when microradiographs are used to study revascularisation and healing after surgery. Although angiograms show the presence of blood circulation in bone and teeth, they do not provide evidence that pathological changes have not occurred nor provide information about their innervation. Several clinical and laboratory studies have been published on the effect of maxillary osteotomy procedures on tooth pulps. The lack of agreement in the clinical investigations may be related to the unreliability of electrical stimulation as a means of assessing the health of the pulp. The results of the animal studies also vary, and the effect on the tooth pulps seems to depend on whether the bone and teeth were moved appreciably after surgery. In the two studies where the total maxilla was moved 5 mm (Nanda et al., 1982) and the anterior maxilla moved 10 mm (Poswillo, 1972), the pulps showed pathological changes. There is very little histological information available from patients. MacGregor (1971) reported a normal pulp in a maxillary central incisor tooth which was lost 6 months after anterior maxillary osteotomy. However Summers and Booth (1975) found variable histological appearances in 10 teeth from two patients
Tooth pulp changes following Lc Fort I
who had undergone segmental maxillary surgery 4 and 10 weeks previously. Pulpal changes included degeneration of myelinated nerves, osteodentine and osteoid formation, and coagulative necrosis. From the present study in rhesus monkeys it is concluded that Le Fort I maxillary ‘down-fracture’ osteotomy with 8 mm advancement caused pulpal disturbances in an appreciable number of teeth. The extent to which this occurs in patients should be carefully monitored.
Mumford, J. M. (1967). Pain perception threshold on stimulating _ human teeth and the histblogical condition of the pulp. British Dental Journal.
Oral Surgery, 1, 87.
Sugg, G. R., Fonseca, R. J., Lecb, I. J. & Howell, R. M. (1981). Early pulp changes after anterior maxillarv osteotomv. o? Oral Surgery, 39, 14.
Summers, L. & Booth, D. R. (1975). The early effects of segmental surgery on the human pulp. International Journal
The assistance of Dr J I Langford, Department of Physics, University of Birmingham in the preparation of the microradiographs is gratefully acknowledged. The study was supported by a grant from the West Midlands Regional Health Authority.
References
of Oral Surgery, 4, 236.
Tajima, S. (1975). A longitudinal study on electrical pulp testing following Le Fort I type osteotomy and Lc Fort I type fracture. Journal of Maxillofacial Surgery, 3,74. Theisen. F. C. & Guernsev. L. H. (1976). Post-ooerative scauelae after anterior segme&I osteitomi&. Oral iurgery, Ok Medicine, Oral Pathology, 41, 139.
Bell, W. H. (lY69). Revascuiarization and bone healing after anterior maxillary osteotomy: a study using adult rhesus monkeys. Journal of Oral Surgery, 27,249. Bell, W. H. (1973). Biologic basis for maxillary ostcotomies. American Journal of Physical Anthropology,
123. 427.
Nanda, R., Legan, H. L. & Langeland, K. (1982). Pulpal and radicular response to maxillary osteotomy in monkeys. Oral Surgery, Oral Medicine, Oral Pathology, 53, 624. Pepcrsack, W. J. (1973). Tooth vitality after alveolar senmental ostcotomy. J&rnai of Maxillofac~al Surgery, 1, 85. Poswillo. D. E. (1972). Earlv DUIDchanges followine reduction of open bites by segmeniai suigery. ?nternationaTJournal of
/our&
Acknowledgements
38, 279.
Bell, W. H. (1975). Le Fort I osteotomy for correction of maxillary deformities. Journal of Oral Surgery, 33, 412. Bell, W. H., Fonseca, R. J., Kennedy, J. W. III & Levy, B. M. (1975). Bone healing and revascularization after total maxillary ostcotomy. Journal of Oral Surgery, 33,253. Bell, W. H. & McBride, K. L. (1977). Correction of the long face syndrome by Lc Fort I osteotomy. Oral Surgery, Orul Medicine, Oral Pathology, 44, 493.
Castelli, W. A. & Huelkc, D. F. (1965). The arterial system of the head and neck of the rhesus monkey with emphasis on the external carotid system. American Journal of Anatomy, 116, 149.
De Jongh, M., Barnard, D. & Birnie, D. (1986). Sensory nerve morbidity following Le Fort I osteotomy. Journal of Maxillofacial Surgery, 14, 10. Hutchinson, D. & MacGregor, A. J. (1972). Tooth survival following various methods of sub-apical osteotomy. International Journal o/Oral Surgery, 1,81. Johnson, J. V. & Hinds, E. C. (1%9). Evaluation of teeth vitality after subapical osteotomy. iour& of Oral Surgery, 27, 256: Kahnbcrg, K.-E. & Engstrom, H. (1987). Recovery of maxillary sinus and tooth sensibility after Le Fort I osteotomy. British Journal of Oral & Maxillofacial Surgery, 25, 68.
Leibold. D. G.. Tilson. H. B. & Rask. K. R. (1971). ~ , A subiective evaluation of the re-establishment of the neurovascular supply of teeth involved in anterior maxillary osteotomy procedures. Oral Surgery, Orul Medicine, Oral Pathology,
Ware, W. H. & Ashamalia, M. (1971). Pulp response following anterior maxillary osteotomy. American Journal of Orthodontics, 60, 156.
Zisscr, G. & Gattinger, B. (1982). Histological investigation of pulpal changes following maxillary and mandibular alveolar osteotomies in the dog. Journal of Oral & Maxillofacial Surgery, 40, 332.
The Authors Professor R. M. Browne PhD, DDS, PDSRCS, FRCPath Professor of Oral Pathology Department of Oral Surgery and Oral Pathology Birmingham Dental School St Chad’s Queensway Birmingham B4 6NN Mr C. L. Brady BDS FDSRCS
Consultant Oral and Maxillofacial Surgeon The West Midlands Plastic and Jaw Surgery Unit Wordsley Hospital Wordslcy Stourbridge West Midlands Mr J. W. Frame PhD, M!k, BDS, FDSRCS Reader and Honorary Consultant Oral Surgeon Birmingham Dental School and Queen Elizabeth Ilospital Birmingham Correspondence and requests for offprints to Mr J. W. Frame, Queen EliTabcth Hospital, Edgbaston, Birmingham B15 2TH
32,531.
MacGregor, A. J. (1971). Histology of a pulp following segmental osteotomy. Rritish Journal of Oral Surgery, 8, 292.
7
Paper received I4 July 1989 Accepted 3 August 1989
of Ora/
1990 The British
and MeriNofocinl
Association
Surgery
(1590) 28, l-7
of Oral and Maxillofacial
Surgeons
Tooth pulp changes following Le Fort I maxillary osteotomy in a primate model R. M. Browne, C. L. Brady, J. W. Frame Department of Oral Surgery and Oral Pathology, Birmingham Dental School, Birmingham West Midlands Plastic and Jaw Surgery Unit, Wordsley Hospital, West Midlands _-
.~.
~
-
_
and The
.~.
SUMMARY. Le Fort I maxillary ‘down-fracture’ osteotomy with 8 mm advancement was performed in 15 adult rhesus monkeys. Forty-five tooth pulps were examined histologically at intervals from 0 to 24 weeks after surgery. Cell degeneration occurred in 31% of pulps examined, necrosis in 16% of pulps and osteo-dentine was found in 7% of pulps. Almost half of the teeth examined (47%) showed marked cellular changes, more frequently found in posterior teeth. Other features noted were inflammation (13%) and reactive dentine in pulps (24%). Axons degenerated initially but recovered by 24 weeks. It is concluded that Le Fort I maxillary osteotomy caused pulpal disturbances in an animal model and the extent to which this occurs in patients needs to be carefully monitored. .-.~ .--..
of pulps showed pathological changes. Conflicting results have also been reported of tooth response after segmental osteotomy procedures in the maxilla. Studies in patients show the incidence of non-responsive teeth to electrical stimulation varying from 6 to 43% after surgery (Table 1). Animal studies have also demonstrated wide variation in the effect on the pulp, varying fron nil to marked cellular changes (Table 2). It is interesting to note that in the animal studies where there was minimal movemen af the bone and tooth segments little effect on the pulp was noted. However, in the two experiments where the total maxilla was superiorly repositioned 5 mm (Nanda et al., 1982) and the anterior maxilla moved 10 mm (Poswillo, 1972), changes were detected in the tooth pulps. These latter two studies were more analogous to the clinical situation in patients where substantial movement of the osteotomiscd bone and teeth is undertaken to correct the dento-facial deformity. The aim of this present study was to determine in an animal model the effect on the tooth pulps of Le Fort I maxillary osteotomy, where the maxilla was moved forwards a distance which simulated normal clinical practice in patients.
INTRODUCTION
A common clinical finding after Le Fort I maxillary osteotomy is that the patient initially experiences some loss of tooth sensitivity, which gradually resolves after several months. However, it is unclear what effect maxillary osteotomy has on the structure of tooth pulps and what are the possible long term sequelae. Studies after Le Fort I maxillary osteotomics in patients and animals have provided conflicting results. Tajima (1975) found 15% of 245 teeth in 27 patients non-responsive to electric pulp testing 14 months after Le Fort 1 ostcotomy or fracture. In the study by de Jongh et al. (1986), 29% of 128 teeth tested in 10 patients after a mean period of 14 months were non-responsive. However, Kahnberg and Engstrom (1987) reported that 90 to 100% of teeth in 20 patients gave a positive response to electric pulp stimulation 18 months after surgery. The variation in the results of these studies may be partly due to the unreliability of electric pulp testing in evaluating the health of the pulp. It has been shown that a tooth responding to electrical stimulation may have a pulp histology varying from normal to fibrosis and inflammation (Mumford, 1967). A study by Bell et al. (1975) in 12 adult rhesus monkeys showed early osseous union, minimal transient vascular ischaemia and minimal osteonecrosis after Lc Fort I osteotomies. However, the maxilla was not transposed into a new position and no tension applied to the soft tissue pediclc. In addition, the authors relied mainly on angiograms to assess pulp vascularisation and health, with little histological data. Nanda et al. (1982) surgically repositioned the maxilla 5 mm superiorly in four adult Macaca irus monkeys and after 150 days the majority
MATERIALS
AND METHODS
The animal model chosen was the adult rhesus monkey because of its anatomical and vascular similarities to humans (Castelli & Huelke, 1965). They weighed between 4.5 and 6 Kg and females were utilised because of the short canine teeth. The surgical procedures were performed under general endotrachcal anaesthesia using nitrous oxide, oxygen and halothane. A standard Le Fort I maxillary 1
2
British Journal of Oral and Maxillofacial Surgery
Table 1 - Tooth Pulp Response to Electric Pulp Stimulation after Segmental Maxillary Osteotomy
Johnson & Hinds (1969) Leibold et al. (1971) \ I
(2-36) 6 12
Hutchinson & MacGregor (1972) Pepersack (1973) Theisen & Guernsey (1976)
No. of teeth
% nonresponsive
17
169
20
18
108
43
12 143 10
58 588 72
7 6 10
No. of patients
Months after surgery (range)
Author
Table 2 _ Tooth Pulp Changes after Anterior Maxillary Segmental Gsteotomy in an Animal Model Author
Animals
Bell, (1969)
6 macaca mulata monkeys 9 rhesus monkeys 2 macaca irus monkeys
Ware & Ashamalia (1971) Poswillo (1972)
Segments moved 0
Follow-up (weeks)
Histology of pulp
l-6
Intra-pulpal circulation maintained. No histology of pulps No histological abnormalities Loss of odontoblasts and nerves. Progressive fibrosis. Islands of metaplastic bone in pulps No degenerative changes apart from nerves, which later regenerated Mild changes-reduction in odontoblast layer-pulpal fibrosis. All DUIDS vital
2mm 10 mm
l-24 8-24
Sugg et al. (1981)
6 macaca fascicularis monkeys
2mm
l-24
Zisser & Gattinger (1982)
9 dogs
0
l-8
in 15 animals (Bell et 1977). A horizontal incision was made through the mucoperiosteum high in the buccal and labial sulcus, extending from first molar to first molar. The margins of the superior flap were raised to expose the anterior and lateral walls of the maxilla and identify the infra-orbital nerves. The subperiosteal dissection was tunnelled back to the pterygomaxillary junction. The osteotomy cut was made with a fissure bur, extending from the pyriform aperture to pterygoid region bilaterally. The bone cuts were made at least 5 mm above the apices of the teeth. However, because of the length of the roots, the apices of the canine teeth were usually transected. Osteotomes were used to section the nasal septum and lateral walls of the nasal cavity and to separate the posterior maxilla from the pterygoid plates. The maxilla was ‘downfractured’ using manual pressure, retaining its blood supply through the soft-tissue pedicle of the palate and buccal gingivae. Some trimming of the vertical portions of bone was required to allow 8 mm forward movement of the maxilla. Fixation of the maxilla was achieved by two vertical and one oblique interosseous wire on each side, to stabilise the maxilla in its anteriorly displaced position. The lateral walls of the maxilla were relatively thick and no other fixation was necessary. Intermaxillary fixation was not required. The soft tissues were closed with 3-O silk sutures. Postoperative antibiotics and analgesics were given for 1 week. The monkeys recovered well after surgery and managed food and fluids without difficulty. Liquidised foods was provided for the first week, osteotomy
was performed
al., 1975; Bell, 1975; Bell & McBride,
Table 3 - Duration of Follow-up After Surgery
Time after surgery (weeks) Number of animals
Immediately
1 2
1
22122
3
4
8
12 16 24 212
then soft food for 1 week, after which the animals resumed a normal laboratory diet. Palpation indicated that the maxilla in each animal united satisfactorily in its new position. Two unoperated monkeys served as controls. The 15 operated animals were killed at intervals after surgery ranging from immediately to 24 weeks (Table 3). At the end of the experimental period, each animal was anaesthetised, the common carotid arteries were exposed bilaterally, cannulated and perfused with barium sulphate (‘Micropaque’) in normal saline, using a technique similar to that of Bell (1973). The perfusion medium was then changed to barium sulphate in 10% neutral buffered formalin. The major blood vessels in the neck were ligated, the head removed and placed irrlO% neutral buffered formalin. The perfusion procedure ensured that the formalin fixed the delicate pulp tissue to preserve cellular detail and the barium sulphate allowed demonstration of vascular architecture using microradiographs. After fixation for at least 48 h, the maxilla was dissected out, radiographed and then sectioned in the midline sagittal plane using a rotating diamond saw. From each animal, one half maxilla was processed to investigate the healing process of the bone
Tooth pulp changes following Le Fort I
3
Table 4 - Summary of the Main Histological Features
Number of Weeks after Surgery Immediate _ Cell degeneration Necrosis Inflammation Reactive dentine Osteodentine Axons
1
1
PM
IPM
223
4
M
M
4
8
PM
8 M
P PM IPM
M
M I
IPM
IPM P = Premolar;
defect. The other half was used to study the histology of the tooth pulps and is the subject of this report. Each half maxilla was sectioned with a diamond saw to produce six separate tissue blocks, each containing a single.tooth together with the surrounding hard and soft tissues. Blocks were prepared of each of the following: central incisor, lateral incisor, first premolar, second premolar, first molar, second molar. The canine was omitted because its large, curved root made orientation difficult and the apex had often been transected during the osteotomy procedure. The central incisors, second premolars and .second molars were prepared for routine histology. The blocks were decalcified in 10% formic acid, double embedded in celloidin and paraffin wax and serial sections ‘prepared at ‘8 urn through the tooth pulps in the bucco-palatal plane. Every tenth section was stained with haemotoxylin ,and eosin and selected sections by Linder’s nerve staining method. The lateral incisor, first ‘premolar and first molar were plastic embedded in LR Epoxy Resin (hard mix). The teeth were again sectioned ‘in the buccopalatal plane. After, initial orientation of the blocks, a 1 mm thick section’was cut for microradiography using the Leitz 1600 saw microtome. The 1 mm slices were demineralised in 10% formic acid and microradiographs prepared using a Grenz X-ray machine.
RESULTS Thel,‘histological features are described below land sum@rarise~din Table 4. Im~ediute: The pulps of the teeth ,from the osteotomy specimen obtained immediately ‘after ,,the operative: procedure and from unope&ated animals served as ‘controls. All the pulps were essentially norm& in appearance (Fig. l), with peril&rally placed ‘regular layers of odontoblasts and cellular fibro-vascular tissue comprising the majority of ‘the tissue. There was some slight irregularity of “the odontoblast layer in the premolar an& molar teeth from the immediate postoperative animal which might have arisen as a consequence of the surgery. Linder’s stain demonstrated prominent nerve bundles in the root canals (Fig. 2) a&coronal pulps of all teeth with individual axons periiherally in the subodontoblastic and odontoblastic layers.
24
24
PM
PM
I PM IPM
I M IPM
I PM M M IMI
I I
(I = Incisor;
12 12 16
IP PM
I I
IP
Pulps affected 14 (31%) 7 (16%) 6 (13%) 11 (24%) 3 (7%)
M = Molar tooth)
One week. There was evidence of degenerative changes in the pulps of the premolar and molar teeth in both animals and of the incisor of one. The odontoblast layer was less regular than normal, contained fewer cells and those present were shrunken with rounded pyknotic nucleii (Fig. 3). The pulps of all three teeth from one animal were diffusely infiltrated by polymorphonuclear leucocytes (Fig. 4). The apex of one root of the molar in this animal had been sectioned in the oestotomy cut. In all the teeth, the pulpal nerves exhibited neuronal degeneration, staining in an irregularly granular pattern. Two weeks. Apart from one molar, all the pulps appeared healthy. Odontoblasts were slightly irregular where the predentine layer exhibited’ a slight increase in width. In one molar, there was marked degeneration of the fibroblasts and complete degeneration of the odontoblasts, A diffuse infiltrate of polymorphonuclear leucocytes and’ macrophages was present. Again, in this molar the apical ,part of one of the roots had been sectioned in the osteotomy cut. Axonal degeneration was complete in ,a11 the pulps so that the nerve bundles persisted but did not contain any stainable axons. Three weeks. The incisor and premolar pulps appeared normal. The incisor exhibited some incisal attrition with a small deposit of reparative dentine at the pulpo-dentinal junction and contained a pulp stone in the root canal. The molar tooth showed advanced necrosis of ‘*the pulp with nearly total degeneration of the odontoblasts and fibroblasts and some scattered polymorphonuclear leucocytes and macrophages in the tissue remnants. Again axonal degeneration was complete and the neurilemmal bundles persisted (Fig.8 5), even in the degenerating pulp, but contained only occasional globules of stainable axonal tissue : Four weeks. Both incisor pulps were of normal appearance apart from the presence of substantial deposits of reparative dentine (Fig. 6) incise-palatally at the pulpo-dentinal :boundary. There was’incisal attrition in both teeth? In one of the animals1 there was some reduction in cell numbers in the ddontoblast layer in both the premolar and molar reeth, together with slight deposition of reparative dentine occlmally. In the other animal, although the premolar pulp was nearly totally necrotic (Fig. 7), the molar pulp appeared normal apart from the persistence of an occasional cell with pyknotic nucleus. All pulps demonstrated total axonal degeneration.
4
British Journal of Oral and Maxillofacial Surgery
Fig. 1 - Incisor (immediate): normal pulp with pseudostratified odontoblast nuclei peripherally and cellular fibro-vascular tissue. Haematoxylin and eosin. Original magnification x200.
Fig. 4 - Premolar, 1 week postoperatively. The odontoblast layer is shrunken and composed of cells with pyknotic nuclei. The pulp contains a diffuse infiltrate of polymorphonuclear leucocytes. Haematoxylin and eosin. Original magnification x 125.
Fig. 2 - Incisor (immediate): normal pulp showing several nerve bundles containing darkly staining axons. Linder’s method. Original magnification X310.
Fig. 5 - Incisor, 3 weeks postoperatively. A neurilemmal bundle crosses the field containing occasional dark-staining axonal remnants. Linder’s method. Original magnification x310.
Fig. 3 - Premolar, 1 week postoperatively. The odontoblast layer is shrunken and the cell nuclei, rounded and pyknotic. Haematoxylin and eosin. Original magnification x200.
Fig. 6 - Incisor, 4 weeks postoperatively. An irregular deposit of reactive dentine is present in&o-palatally. Haematoxylin and eosin. Original magnification X310.
Tooth
Fig. 7 - Premolar, 4 weeks postoperatively. The pulp is necrotic but contains the residual outlines of blood vessels. Haematoxylin and eosin. Original magnification x50.
Eight weeks. The incisors of both animals appeared normal, containing small deposits of reparative dentine incisally where there had been attrition. In one animal the premolar and molar pulps demonstrated some reduction in cellularity in both the odontoblast and fibroblast populations and in the molar, focal groups of chronic inflammatory cells were also present. In the other animal, both the premolar and molar had undergone complete pulpal necrosis. In the molar there was a periapical abscess in association with the buccal root. The osteotomy cut had passed very close to this root apex, although not actually through it. In only one incisor pulp were there any axons demonstrable. In all the other teeth, there were no stainable axons. Twelve weeks. The incisor pulp of one animal had undergone complete necrosis and there was marked incisal attrition. The premolar and molar pulps were essentially normal although there was a slight reduction in the number of odontoblasts. In both teeth there was deposition of reparative dentine occlusally and in one of them on the vertical walls of the coronal pulp as well. In the other animal, the incisor pulp was normal apart from a small deposit of reparative dentine incisally at the pulpo-dentinal junction. There was evidence of incisal attrition. The pulps of the premolar and molar were both almost totally necrotic, although a small remnant of vital pulp tissue was present in the apical part of the root canal of the premolar. A localised deposit of reparative dentine was present in one pulp horn of the molar. In the three teeth with vital pulps, numerous nerve bundles with clearly defined axons were present. Sirfeen weeks. The pulps of the incisor and premolar were normal apart from some reduction in the number of cells in the odontoblast layer. Both exhibited attrition of the incisal or occlusal surfaces beneath which, in the incisor, there was a localised deposit of reparative dentine. Both pulps contained numerous darkly staining axonal fibres. In the molar, the pulp had undergone total necrosis. Twenty-four weeks. The incisors had normal pulps. In both there had been incisal attrition with small
pulp changes
following
Le Fort I
5
Fig. 8 - Molar, 24 weeks postoperatively. The pulp tissue has been replaced by osteodentinc. Iiaematoxylin and eosin. Original magnification X50.
Fig. 9 - Premolar, 24 weeks postoperatively. Numerous darkly staining axons are present in the peripheral part of the pulp. Linder’s method. Original magnification x200.
deposits of reparative dentine at the pulpo-dentinal junction. In one animal the most recently formed circumpulpal dentine showed a less homogenous staining reaction of its matrix, suggesting a disturbance in dentinogcncsis. Of the two premolars, one pulp was of normal structure apart from some reduction in the cell population of the odontoblast layer. The other pulp exhibited total degeneration of the odontoblasts and a marked reduction in the number of fibroblasts in the pulp stoma, which had undergone fibrosis. The entire pulpal surface of the dentine was covered by a layer of osteodentine which was also present as discrete deposits throughout the pulp. The molar tooth from both animals exhibited similar changes, namely marked cellular degeneration, pulpal fibrosis and extensive deposition of osteodentine (Fig. 8). However, in one tooth the roots had been sectioned in the osteotomy cut and the gaps between the cut surfaces had been repaired by deposition of osteodentine. Deposition of osteodentine at the apex of one root had resulted in ankylosis. Although cellular degeneration and tibrosis were marked in both molars and in one premolar, there were a number of patent blood vessels present, all of which contained the perfused radiopaque
6
British Journal
of Oral and
MaxillofacialSurgery
Fig. 10 - Microradiographs demonstrating the vasculature of a vital premolar (A) and its absence in a molar with necrotic pulp (W.
medium. In all the teeth axons were demonstrated by nerve staining (Fig. 9). The microradiographs confirmed the histological findings concerning the viability and vascularity of the pulp (Fig. 10A). However, no obvious differences on microradiographs were observed between normal pulps and those exhibiting features of cellular degeneration. In necrotic pulps no vessels containing contrast medium were present (Fig. 10B).
DISCUSSION Histological examination of 45 teeth in 15 monkeys at varying times after Le Fort I maxillary osteotomy indicated that 14 pulps (31%) exhibited cell degeneration and 7 pulps (16%) were necrotic. Thus, 21 teeth (47%) showed signs of marked cellular changes,
affecting mainly the premolars and molars. Three molar teeth had apices inadvertently transected during osteotomy of the bone and in one other molar, the cut was close to the apex. The pulps of these four molars all showed cellular degeneration or necrosis. Histological examination of the molar with the transected apex after 24 weeks demonstrated that the gap in the root was repaired with osteodentine, and that the pulpal blood vessels were patent. If these four molar teeth are eliminated from the data, 11 pulps (25%) showed cellular degeneration and 6 pulps (13%) necrosis, resulting in 17 teeth (38%) with marked cellular changes after surgery. Other less severe histological changes were also observed. Inflammation was noted in 6 pulps (13%) within the first 8 weeks after surgery, but not at later stages. Reparative dentine was found in 11 pulps (24%) at times from 2 weeks to 24 weeks, and affected mainly incisors. It was deposited on the pulpal surface of the dentine, predominantly beneath the incisal edges, and usually associated with attrition of the enamel. The formation of the reparative dentine may have been caused by occlusal trauma related to the abnormal occlusion after surgery. The odontoblasts and pulp tissue in these teeth were otherwise normal in appearance. Osteodentine occurred in 3 teeth (7%) at 24 weeks, and was associated with marked cellular degeneration and fibrosis of the pulp. Although osteodentine formation is probably a consequence of impaired blood supply, patent blood vessels containing barium sulphate were present within these 3 pulps. Axons degenerated after surgery and regeneration, which began after 8 weeks, appeared complete by 24 weeks. The microradiographs confirmed the histological findings in healthy or necrotic pulps, but were not sufficiently sensitive to detect subtle changes. It is important that histological data is also available when microradiographs are used to study revascularisation and healing after surgery. Although angiograms show the presence of blood circulation in bone and teeth, they do not provide evidence that pathological changes have not occurred nor provide information about their innervation. Several clinical and laboratory studies have been published on the effect of maxillary osteotomy procedures on tooth pulps. The lack of agreement in the clinical investigations may be related to the unreliability of electrical stimulation as a means of assessing the health of the pulp. The results of the animal studies also vary, and the effect on the tooth pulps seems to depend on whether the bone and teeth were moved appreciably after surgery. In the two studies where the total maxilla was moved 5 mm (Nanda et al., 1982) and the anterior maxilla moved 10 mm (Poswillo, 1972), the pulps showed pathological changes. There is very little histological information available from patients. MacGregor (1971) reported a normal pulp in a maxillary central incisor tooth which was lost 6 months after anterior maxillary osteotomy. However Summers and Booth (1975) found variable histological appearances in 10 teeth from two patients
Tooth pulp changes following Lc Fort I
who had undergone segmental maxillary surgery 4 and 10 weeks previously. Pulpal changes included degeneration of myelinated nerves, osteodentine and osteoid formation, and coagulative necrosis. From the present study in rhesus monkeys it is concluded that Le Fort I maxillary ‘down-fracture’ osteotomy with 8 mm advancement caused pulpal disturbances in an appreciable number of teeth. The extent to which this occurs in patients should be carefully monitored.
Mumford, J. M. (1967). Pain perception threshold on stimulating _ human teeth and the histblogical condition of the pulp. British Dental Journal.
Oral Surgery, 1, 87.
Sugg, G. R., Fonseca, R. J., Lecb, I. J. & Howell, R. M. (1981). Early pulp changes after anterior maxillarv osteotomv. o? Oral Surgery, 39, 14.
Summers, L. & Booth, D. R. (1975). The early effects of segmental surgery on the human pulp. International Journal
The assistance of Dr J I Langford, Department of Physics, University of Birmingham in the preparation of the microradiographs is gratefully acknowledged. The study was supported by a grant from the West Midlands Regional Health Authority.
References
of Oral Surgery, 4, 236.
Tajima, S. (1975). A longitudinal study on electrical pulp testing following Le Fort I type osteotomy and Lc Fort I type fracture. Journal of Maxillofacial Surgery, 3,74. Theisen. F. C. & Guernsev. L. H. (1976). Post-ooerative scauelae after anterior segme&I osteitomi&. Oral iurgery, Ok Medicine, Oral Pathology, 41, 139.
Bell, W. H. (lY69). Revascuiarization and bone healing after anterior maxillary osteotomy: a study using adult rhesus monkeys. Journal of Oral Surgery, 27,249. Bell, W. H. (1973). Biologic basis for maxillary ostcotomies. American Journal of Physical Anthropology,
123. 427.
Nanda, R., Legan, H. L. & Langeland, K. (1982). Pulpal and radicular response to maxillary osteotomy in monkeys. Oral Surgery, Oral Medicine, Oral Pathology, 53, 624. Pepcrsack, W. J. (1973). Tooth vitality after alveolar senmental ostcotomy. J&rnai of Maxillofac~al Surgery, 1, 85. Poswillo. D. E. (1972). Earlv DUIDchanges followine reduction of open bites by segmeniai suigery. ?nternationaTJournal of
/our&
Acknowledgements
38, 279.
Bell, W. H. (1975). Le Fort I osteotomy for correction of maxillary deformities. Journal of Oral Surgery, 33, 412. Bell, W. H., Fonseca, R. J., Kennedy, J. W. III & Levy, B. M. (1975). Bone healing and revascularization after total maxillary ostcotomy. Journal of Oral Surgery, 33,253. Bell, W. H. & McBride, K. L. (1977). Correction of the long face syndrome by Lc Fort I osteotomy. Oral Surgery, Orul Medicine, Oral Pathology, 44, 493.
Castelli, W. A. & Huelkc, D. F. (1965). The arterial system of the head and neck of the rhesus monkey with emphasis on the external carotid system. American Journal of Anatomy, 116, 149.
De Jongh, M., Barnard, D. & Birnie, D. (1986). Sensory nerve morbidity following Le Fort I osteotomy. Journal of Maxillofacial Surgery, 14, 10. Hutchinson, D. & MacGregor, A. J. (1972). Tooth survival following various methods of sub-apical osteotomy. International Journal o/Oral Surgery, 1,81. Johnson, J. V. & Hinds, E. C. (1%9). Evaluation of teeth vitality after subapical osteotomy. iour& of Oral Surgery, 27, 256: Kahnbcrg, K.-E. & Engstrom, H. (1987). Recovery of maxillary sinus and tooth sensibility after Le Fort I osteotomy. British Journal of Oral & Maxillofacial Surgery, 25, 68.
Leibold. D. G.. Tilson. H. B. & Rask. K. R. (1971). ~ , A subiective evaluation of the re-establishment of the neurovascular supply of teeth involved in anterior maxillary osteotomy procedures. Oral Surgery, Orul Medicine, Oral Pathology,
Ware, W. H. & Ashamalia, M. (1971). Pulp response following anterior maxillary osteotomy. American Journal of Orthodontics, 60, 156.
Zisscr, G. & Gattinger, B. (1982). Histological investigation of pulpal changes following maxillary and mandibular alveolar osteotomies in the dog. Journal of Oral & Maxillofacial Surgery, 40, 332.
The Authors Professor R. M. Browne PhD, DDS, PDSRCS, FRCPath Professor of Oral Pathology Department of Oral Surgery and Oral Pathology Birmingham Dental School St Chad’s Queensway Birmingham B4 6NN Mr C. L. Brady BDS FDSRCS
Consultant Oral and Maxillofacial Surgeon The West Midlands Plastic and Jaw Surgery Unit Wordsley Hospital Wordslcy Stourbridge West Midlands Mr J. W. Frame PhD, M!k, BDS, FDSRCS Reader and Honorary Consultant Oral Surgeon Birmingham Dental School and Queen Elizabeth Ilospital Birmingham Correspondence and requests for offprints to Mr J. W. Frame, Queen EliTabcth Hospital, Edgbaston, Birmingham B15 2TH
32,531.
MacGregor, A. J. (1971). Histology of a pulp following segmental osteotomy. Rritish Journal of Oral Surgery, 8, 292.
7
Paper received I4 July 1989 Accepted 3 August 1989