A radio-isotope study of the healing of mandibular bone grafts in patients

British Journal of Oral Surgery (1983) 21, 277-289 @ 1983 The British Association of Oral and Maxillofacial Surgeons

A RADIO-ISOTOPE STUDY OF THE HEALING OF MANDIBULAR BONE GRAFTS IN PATIENTS

J. W. FRAME, Ph.D., M.Sc., B.D.s.,F.D.S.R.C.S., H.D.EDMoNDsoN,M.B.c~.B.,D.D.s., F.D.s.R.c.s., M.R.c.s., L.R.c.P., D.A. and M. M. O’KANE, B.D.S.

Department of Oral Surgery and Oral Medicine, The Dental School, St. Chad’s Queensway, Birmingham, B4 6NN

Summary. Radionucleotide scanning is now accepted as a reliable method of visualising the metabolic activity of the skeletal system. Its aplication to the maxillo-facial region is reviewed, and its possible role in monitoring the healing of bone grafts is discussed. The radio-isotope 99m technetium-methylene di- phosphonate was used to study the revascularisation and healing of large autogenous bone grafts to the mandible in eight patients. The scans demonstrated the dynamic activity in the grafts and showed varying patterns in different types of grafts.

Introduction

Reconstruction of the jaw using autogenous bone grafts is an important part of clinical oral surgery, and has been the subject of numerous studies in the past. Much valuable information on the revascularisation and remodelling process has been obtained by using animal models to investigate histologic, micro-angiographic, and radiographic aspects (Hunsuck, 1969; Canzona et al., 1976; Roser et al., 1977; Nathanson, 1978; Frame et al., 1982). However, many of the invasive procedures cannot be applied to patients, and most of the previously published investigations in humans have relied mainly on clinical and radiological follow-up to monitor graft incorporation and repair (Obwegeser, 1966; Seward, 1967; Bell, 1968; Weinstein, 1968; De Champlain, 1973; Adekeye, 1978; Kudo & Fujioka, 1978). These techniques do not reveal the early dynamic activity which occurs in the grafts and the adjacent host bone, and it is only at a much later stage in the remodelling process that changes are evident on conventional radiographs. At present, certain aspects remain obscure:

(1) The exact nature of the revascularisation and remodelling process. (2) The source of the blood vessels which grow into the graft, and whether they

proliferate from the surrounding soft tissues or mainly from the adjacent bone ends.

(3) the duration of the revascularisation and healing phase. (4) whether there is any difference between the healing of full-thickness and

decorticated grafts from the iliac crest. In order to elucidate these points, a clinical study of mandibular bone graft healing

was undertaken using radioisotope bone scanning techniques.

Radio-isotope bone imaging This procedure allows visualisation of the metabolic activity of the skeletal system,

and is widely used in the investigation of patients with primary and secondary malignant disease to locate any bone metastase (Pendergrass et al., 1973; Freeman,

(Received 14 April 1982; accepted 1 June 1982)

277

278 BRITISH JOURNAL OF ORAL SURGERY

1975; Citrin, 1977; Elletal., 1978). The increased uptake ofthe tagged materialisin the reactive bone and not in the neoplasm itself. Although radio-isotopes had been used clinically for many years, a major advance in bone scanning technology was the introduction of a group of bone-seeking compounds which could be labelled with technetium-99m (Subramanian & McAfee, 1971). These new agents combined low radiation dose, high photon yield, detailed anatomical information, and general availability. The radio-isotope is injected intravenously and is concentrated in areas of increased blood supply and increased bone metabolism (Merrick, 1975). The emitted gamma rays are detected and recorded by a gamma camera which displays them as relatively dark areas on the scan. The physiological basis of the technique depends on the changes which occur within bone. During the formation of new bone the hydroxyapatite crystals are small, imperfect, and surrounded by a large hydration shell into which the radio-isotope enters and exchanges with the ions on the crystal surface. Imperfections within the crystal lattice result in a slower exchange continuing between the surface and interior of the crystal (Neuman & Neuman, 1957). As the bone matures, the crystals become more perfect and less hydrated, and the mineral phase becomes less available for exchange with administered isotopes (McLean, 1958). Brookes and Helal(l970) showed that under physiological conditions blood supply and mineral turnover are interrelated, and Merrick (1975) concluded that it is impossible to distinguish between their respective contributions to radio-siotope uptake.

The value of radio-isotope scanning in the early detection and differential diagnosis of benign and malignant lesions in the maxillo-facial region was discussed by Alexander (1976) who stated that earlier and more accurate detection is possible on bone scans than on radiographs. Although the procedure is very sensitive it is not selective, and caution must be exercised in interpreting positive images since they may be caused by common and relatively harmless conditions such as chronic periapical infection, periodontitis, and healing extraction sockets (Matteson et al., 1980). In addition, facial bone scans may show background activity from the base of skull, vertebral column, skull suture lines, and areas of continuing growth. Radio- isotope scanning was used by Beirne and Leake (1980) to locate an area of condylai hyperplasia. Its role in the post-operative evaluation of bone grafts was first described by Bright et al. (1973) who found that the scans provided sensitive and reliable information about the rate and location of graft incorporation in dogs which had received distal ulnar implants. A similar study by Stevenson et al. (1974) concluded that radio-isotope scanning is more sensitive than radiographs for the serial assessment of graft healing in long bones of dogs. Experimental studies of bone grafting to the mandible of dogs confirmed the value of the technique in monitoring healing and remodelling in the jaws (Kellyet al., 1975,1976; Roser & Mena, 1978). Bone grafts which failed to incorporate the isotope underwent resorption, and resul- ted in a residual gap between the bone ends. There has only been one brief report of radio-isotope scanning of an autogenous bone graft to the mandible in a patient (Alexander, 1976). The present study was undertaken to monitor the healing of iliac crest grafts to the mandible, with long-term follow-up at standard time intervals, and to compare different types of grafts.

Patients and Methods

The eight patients in the study had received autogenous bone grafts to reconstruct the mandible following resection of locally invasive tumours, and in one case of developmental anomaly. All the grafts were obtained from the iliac crest between the

HEALING OF MANDIBULAR BONE GRAFTS IN PATIENTS 279

anterior superior iliac spine and the tubercle of the iliac crest, and sometimes extending posteriorly towards the posterior superior iliac spine, using a technique similar to that advocated by Mrazik et al. (1980). The grafts were secured to the remainder of the mandible with 0.5 mm. diameter soft stainless steel wires, and intermaxillary fixation which was effected by cast metal splints was maintained for six weeks after surgery. Five different types of grafts were compared in this study (Fig. 1): (a) free-end bone grafts used to restore the body and ramus, and fixed to the mandible at their anterior end only; these were both full thickness grafts from the iliac crest consisting of the inner and outer cortical tables and the interspaced cancellous bone, and also partial thickness grafts composed of one cortical plate and its attached cancellous tissue; (b) segmental grafts used to restore discontinuities in the body, and attached at both ends to the mandible; these were both full and partial thickness grafts; (c) one onlay graft to restore the angle and ramus of the mandible.

As far as possible radionucleotide scans were obtained for each patient about 1 and 6 months after surgery and then at yearly intervals until no further increase in activity was demonstrated. Conventional radiographs were obtained 1 week post- operatively and afterwards at the same time intervals as the radionucleotide images. The radio-isotope which was used was 12 mCi of 99m technetium-methylene di- phosphonate which has a half-life of 6 hours, and emits 140 keV gamma energy. The scans of the jaw were recorded 3 hours after the administration of the isotope.

Clinically, healing was satisfactory in all cases and none of the grafts became infected or was lost. At the time of release of the intermaxillary fixation, the grafts had united with the adjacent bone of the mandible and all patients achieve good jaw function and aesthetics. One patient developed an infection of the hip wound, but this resolved after a few days.

/ FULL THICKNESS

FREE-END GRAFTS \ PARTIAL THICKNESS

FULL THICKNESS

PARTIAL THICKNESS

ONLAY GRAFTS

Fig. 1

Figure l-Five types of autogenous bone grafts from the iliac crest are compared in this study.


Fig. 2

Figure 2-Radiograph of a full-thickness, free-end autograft to the let? mandible. (A) One week after surgery. (B) One year after surgery.

R

POST

Fig. 3

Figure 3-Radio-isotope scan of patient in Fig. 2 shows increased activity in the graft (arrow). (A) One month after surgery (B) One year after surgery.

1

HEALING OF MANDIBULAR BONE GRAFTS IN PATIENTS

Free-end grafts-full thickness

281

Conventional radiographs show little change from 1 week to 1 year after surgery (Figs. 2A and 2B), although there has been some remodelling of the graft and of the separate piece of bone at its superior end. The radiographs give little indication of viability or of the dynamic activity within the autograft. This is better demonstrated on the radio-isotope scans, where as early as one month post-operatively, there is considerable activity in the graft and adjacent mandible (Fig. 3A). Initially the main uptake of isotope is at the junction between graft and host bone and in the region of the separate block of bone. After one year, the activity has spread to involve the whole of the graft and is equally distributed throughout (Fig. 3B). This enhanced uptake of isotope is still evident two years after surgery, although less marked than previously, and after three years has returned to normal. The scans indicate that the increased vascular and metabolic activity in the full-thickness autograft is concentrated initially at the anterior end adjacent to the mandible, and posteriorly in the separate piece, and eventually involves the whole length of the graft. During this period of intense metabolic activity, little changes are seen on the radiographs.

Free-end grafts-partial thickness The post-operative radiograph of one of the grafts (Fig. 4A) shows it securely

wired to the mandible and demonstrates its rather inert appearance. Neither the clinical (Fig. 5) nor the radiographic features give a true indication of the great activity which is taking place in and around the graft at this time. On the other hand, the scintiscans demonstrate the early revascularisation and healing along the whole length of the graft (Fig 6A). There is an equal distribution of radio-isotope uptake

Fig. 4

Figure 4-Radiographs of a partial thickness, free-end autograft to the left mandible. (A) One week after surgery (B) One year after surgery.


. Fig. 5

Figure 5-Clinical appearance of graft eight weeks after surgery.

A Fig. 6

Figure GScintiscans of patient in Fig. 5 demonstrate increased metabolic activity and vascularisation within the graft (arrow). (A) One month after surgery (B) One year after surgery.


Figure 7-Radiographs of full-thickness autograft from iliac crest replacing part of right body of mandible. (A) One week after surgery. (B) One year after surgery.

A R. L&T Figure S-Scintiscansofpatient in Fig. 7 showing metabolic activity (arrow). (A) One monthafter surgery

(B) eighteen months after surgery.


throughout the autograft with no concentration of activity at the junction between graft and mandible as in the full-thickness ones. After one year, the radiograph (Fig. 4B) confirms that there has been greater and more rapid remodelling of the partial thickness graft compared to the full thickness one. The scintiscans (Fig. 6B) show that the increased uptake of isotope is beginning to decline, but is still equally distributed throughout the graft. Fifteen months after surgery, there is very little uptake of the isotope implying that revascularisation and remodelling is almost complete. The radionucleotide images indicate that during the healing of partial thickness free-end bone grafts to the mandible the activity takes place equally throughout the graft, and is completed approximately 15 months after surgery.

Segmental Grafts-Full thickness A radiograph of one of the full thickness grafts from the iliac crest one week after

surgery is shown in Figure 7A. Subsequent views indicate that there has been considerable remodelling taking place during the first year (Fig. 7B). On the scans obtained one month post-operatively (Fig. 8A) the main uptake of the isotope is at the two ends of the graft adjacent to the mandible and there is little activity in the

Fig. 9

Figure 9-Radiograph of partial thickness iliac crest graft replacing left body of mandible. (A) One week after surgery. (B) One year after surgery.


central portion. One year after surgery, the activity is seen to extend to involve the whole of the graft but is less intense, and by 18 months has almost ceased (Fig. 8B). The scans indicate that when full thickness grafts from the iliac crest are used to restore a segmental defect in the mandible, the increased vascular and metabolic activity is concentrated initially at the two ends adjacent to the mandible but eventually spreads to involve the whole graft during a period of about l& years. This

Fig. 10

Figure lO-Clinical appearance of patient in Fig. 9, 6 weeks after surgery.

::

Fig. 11

Figure 11-Scintiscans of patient in Fig. 9 showing increased uptake of isotope (arrow). (A) One month after surgery (B) One year after surgery.


concentration of activity at the graft/mandible interface is similar to that noted in the full thickness, free-end grafts.

Segmental grafts-partial thickness The healing of these grafts differed from those in the full-thickness segmental

group. A post-operative radiograph at one week shows one of the partial thickness grafts consisting of one cortical plate and the attached cancellous bone (Fig. 9A). Satisfactory clinical healing has been achieved (Fig. 10) and scintiscans display the revascularisation and metabolic activity in and around the autograft (Fig. 11A). The

Fig. 12

Figure 12-Radiograph of onlay graft to let? angle and vertical ramus of mandible. (A) One week after surgery (B) Two years after surgery.


L. LAT Fig. 13

Figure 13-Scintiscans of patient in Fig. 12, one month after surgery. (A) antero-posterior (B) lateral.

increased uptake of the radio-isotope takes place along its whole length, although there is a greater amount at the anterior and posterior ends adjacent to the mandible. Subsequent scans show a more rapid decline in activity, and after one year (Fig. 11B) there is little uptake of the technetium di-phosphonate except at the anterior end, indicating that revascularisation is almost complete. Conventional radiographs at that time confirm that remodelling has taken place, although the outline of the graft is still clearly evident (Fig. 9B). In this segmental group, as with the free-end grafts, the partial thickness cortico-cancellous grafts heal more rapidly (that is 12-15 months) than the full thickness grafts (that is up to 18 months). In both partial and full thickness grafts which are used to reconstruct segmental defects in the mandible, the metabolic and vascular activity is greater at the two ends adjacent to the mandible. However, the central areas of the autografts undergo more rapid revascularisation in the cortico-cancellous grafts.

Onlay graft This patient received an onlay graft to restore the left angle and vertical ramus of

the mandible (Fig. 12A). The graft consisted of two slabs of bone wired together to produce greater bulk at the angle of the jaw. Radiographs taken at yearly intervals showed only slight remodelling with minimal reduction in its bulk (Fig. 12B). The scintiscans obtained one month after surgery demonstrated high uptake of isotope in the region of the graft corresponding to its outline (Fig. 13). This revascularisation and remodelling persisted for 2 years.

Discussion

This initial study of the revascularisation and remodelling process in patients suggests that the radio-isotope technetium methylene di-phosphonate provides a

288 BRITISH JOURNAL OF ORAL SUiGERY

useful means of monitoring the activity in and around autogenous bone grafts to the mandible. The scans indicate the viability or not of the autograft, and their findings correlate well with the clinical and long-term radiographic evidence of healing and remodelling. A major advantage of the scintiscans is their ability to demonstrate the early dynamic activity at a time when no changes are seen on radiographs. The scans also give some indication of the revascularisation process in the different types of grafts. In the free-end grafts to the mandible, the healing is more rapid in the partial thickness than full thickness ones, and also the distribution of activity within the grafts is different: in the full-thickness autografts, the isotope uptake is concentrated initially at the junction between graft and mandible, while in the partial thickness group the initial isotope uptake is more equally distributed throughout the graft. This suggests that with the partial thickness grafts the blood vessels can penetrate rapidly into the graft from the overlying soft tissues, throughout its length, whereas with the full thickness grafts, the main source of blood vessels initially may be the adjacent bone of the mandible. In the segmental defects in the mandible, the partial thickness grafts heal more rapidly than the full thickness ones. In both types of segmental grafts, the metabolic activity is greater at their two ends adjacent to the mandible, although the central areas undergo more rapid revascularisation in the partial thickness ones. This again suggests that during the healing of the decorticated segmental autografts, the blood vessels may be able to penetrate both from the overlying soft tissues and from the adjacent bone ends, whereas in the full-thickness ones, the main sources of the blood vessels may be the adjacent host bone.

It should be remembered that positive images may be caused by a variety of conditions including infection or recurrence of the original lesion which can often be detected earlier on the scans than on radiographs (Alexander, 1976). However, in this present study none of the grafts became infected and recurrence is unlikely since the increased uptake of the isotope diminished after several months, and subsequent radiographs and clinical examination did not show any pathology. It can be assumed that the uptake of technetium di-phosphonate was related to the increased blood supply and metabolic activity associated with revascularisation and remodelling of the grafts.

Radio-isotope scanning techniques are useful for monitoring the dynamic activity in autogenous bone grafts to the mandible in patients. However, conventional radiographs are also required to assess the extent of bony remodelling and consolida- tion, and to exclude any recurrence of the original pathological lesion. This prelimi- nary report illustrates the value of radionucleotide scanning in assessing bone graft repair and a larger clinical study is underway to verify the reliability of the technique.

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A radio-isotope study of the healing of mandibular bone grafts in patients

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