- Email: [email protected]
Endosteal implants in the irradiated lower jaw
Journal of Cranio-MaxillofitcialSurgery (1996) 24, 237-244 © 1996European Association for Cranio-Maxillofacial Surgery
Endosteal implants in the irradiated lower jaw F. Watzinger, R. Ewers, A. Henninger, G. Sudasch, A. Babka*, G. Woelfl**
University Clinicfor Maxillofaeial Surgery, (Head." Prof. Dr. Dr. Rolf Ewers), Medical School, * University Clinic for Dentistry, (Head." Prof. Dr. Rudolf Slavicek), Medical School, **Institute of Medical Statistics (Head." Prof. Dr. Peter Bauer), University of Vienna, Vienna, Austria
SUMMARY. Since 1990 Endosteal implants have been inserted in the irradiated lower jaw at our clinic. 1MZ implants have been used for dental rehabilitation in 26 patients (21 male, 5 female) suffering from squamous cell carcinomas stage T2-T4136. The implants were either placed in local bone and soft tissue (group 1, n = 6 0 implants), or in local bone after marginal mandibulectomy and transplanted soft tissue (group 2, n--26 implants), or in transplanted bone and soft tissue (group 3, n=52 implants). Life-table analysis according to Kaplan-Meier demonstrated a 3-year implant survival rate of 87.8% in Group 1, 69.1% in Group 2 and 58.3% in Group 3. There was no statistical significant difference in the amount of marginal bone loss and the degree of marginal infection between the three groups (P > 0.29). Major complications: A mandibular fracture passing through an empty implant socket 8 months after implant loss (Group 2) was caused by postradiation-osteonecrosis; implant removal and bone resection was mandatory. The poor results of the bone graft group may be explained by two patients, in whom simultaneous placement of implants in nonvascularized bone grafts was carried out, intraoral tissue breakdown led to graft failure and loss of the implants (n = 10).
restoration in patients having had mandibular resection and bone graft (Urken et al., 1991; Martin et al., 1992; Zlotow et al., 1992; Sclaroff et al., 1994; Donovan et al., 1994; Moscoso et al., 1994). Komisar (1990) asserted that restoration of mandibular continuity alone does not enhance function in the majority of head and neck cancer patients. The degree to which mastication is affected depends on the amount of mandible removed, but the status of tongue function is equally important. The use of osseointegrated implants can minimize masticatory limitations as well as improve facial contour.
INTRODUCTION Radiotherapy is an essential part of the treatment modalities in patients suffering from squamous cell carcinoma of the oral cavity. Denture retention is frequently compromised by inadequate saliva production following irradiation (Larsen et al., 1993). Moreover, many patients have surgical defects which cannot be adequately reconstructed without implants. In these patients endosteal implants may be placed either in irradiated local bone or in bone grafts. It is well known that irradiation causes tissue damage to structures adjacent to the tumour. Hypovascular, hypocellular and hypoxaemic tissue results (Marx, 1983; Marx and Johnson, 1987). Risks that must be discussed include postradiationosteonecrosis (PRON), fracture, development or recurrence of tumour with unknown risks of treatment, nonintegration of implants (early or delayed) and soft tissue problems (McKenzie et al., 1993). Accidental or surgical trauma leads to delayed wound healing and may include the risk of PRON. The risk of developing PRON depends on the radiation dose (Murray et al., 1980; Beumer et al., 1982), as well as on fractionation and volume of irradiated tissue. Nevertheless, some authors present good results of endosteal implants placed in irradiated bone (Albrektsson, 1988; Parel and TjellstrOm, 1991; Granstroem et al., 1992; Taylor and Worthington, 1993). Endosteal implants may also serve for prosthetic
MATERIAL AND METHODS Since 1990, endosteal implants have been placed in the irradiated lower jaw at our clinic. In 26 patients suffering from squamous cell carcinomas stage T2-T4, 136 IMZ implants have been used for dental rehabilitation. Twenty one patients were male and 5 female, their ages ranged between 41 and 79 (mean 62) years. After tumour staging including tattooing, preoperative radiochemotherapy was applied. Fractionated radiotherapy with a total dosage of 50 Gray was given. Surgery followed 4 weeks-3 months after irradiation. Radical tumour resection was carried out as a marginal mandibulectomy in five cases and segmental resection in 12 cases. Soft tissue reconstruction was carried out by a 237
238
Journal of Cranio-Maxillofacial Surgery
Table 1 - Distribution of the implants concerning function and implant loss Number of implants In function Without function Lost No osseointegration Marginal bone loss Recurrent tu., death Sum
All groups Group 1 Group 2
Group 3
78 16
38 8
15 0
25 8
10 16 16 136
0 7 7 60
0 5 4 24
10 4 5 52
GINGIVALINDEX
$ULCU$ BLEEDING INDEX
3~
3
251-
25
2-1 15 105 0. . . .
. . . .
• ,,
°o
2
--
15 --
1
,.°°
05 0
Fig. 3 - Gingival index (GI) according to Loe and Silness, 0-3; (0 = no inflammation, 3 = distinct inflammation; simplified). Sulcus bleeding index (BI) according to Muehlemann, 0-3; (0 = no bleeding on probing, 3 =distinct bleeding; simplified). Median values per patient (.); Median values per group (-).
Survival rate
60 j.
L_ 58.3%
50 40 30 20 100
i o
~
group 1
--
group 2
--
group 3
I
I
I
I
I
I
1
5
10
15
20
25
30
35
I mths 40
Fig. 1 - Implant survival rate according to Kaplan-Meier.
M A R G I N A L BONE LOSS
C R E V I C U L A R PROBING DEPTH
4
-" 3
!:
q
•
.I.
--
¸
2.
,*
=•
Fig. 4 - Implants inserted in the area of marginal resection of the mandible (Group 2). Fig. 2 - Marginal bone loss and crevicular probing depth (mm), mean values per patient (.); mean values per group (-).
local flap in twelve cases, by a myocutaneous pectoralis muscle flap in five cases, by a microvascular jejunal flap in seven cases, and by a microvascular osteomyocutaneous iliac graft in two cases. Bone reconstruction was performed by a microvascular iliac bone graft in three cases, by a free iliac crest bone graft in five cases, by a rib graft in two cases and by a cancellous iliac bone graft in Titanium mesh in two patients. Prosthetic rehabilitation was carried out by using endosteal implants, the minimum interval between irradiation and implant insertion was 12 months. We differentiate between three groups (Table 1, Figs. 1, 2, 3): Group 1: The implant socket irradiated local bone and soft tissue.
consisted
of
Group 2: The implant socket consisted of irradiated local bone in which marginal mandibulectomy had been carried out; the implant was surrounded by transplanted soft tissue (Fig. 4). Group 3: The implant socket consisted of transplanted bone (Fig. 5) and soft tissue, the transplant recipient region had been irradiated preoperatively. This group is rather heterogenous, since it contains microvascutar anastomosed bone grafts and different types of avascular bony reconstruction, primary and second step implant placement as well. These were summarized so as not to have too many small groups and to obtain a general view of implant placement in these patients. However, Table 2 presents the distribution of the implants and the rate of implant loss according to different types of bone grafting. In the event of two-step surgery the implants were placed at least 6 months after bony reconstruction.
Endosteal implants in the irradiated lower jaw
239
to estimate marginal infection: gingival index (L6e and Silness, 1963) and sulcus bleeding index (Miihlemann, 1978). The function of denture was evaluated regarding retention of the implantsupported overdenture and occlusion. The patients were questioned whether they felt satisfied with their masticatory function and whether speech function was satisfactory. Statistical methods
Fig. 5 - Implants inserted in bone grafts after segmental resection (Group 3). Table 2 - Distribution of implants in Group 3 according to the variable extent of resection and the various type of bone grafting Type of bone grafting Microvascular anastomosed bone graft and second stage implant placement Avascular bone graft and simultaneous implant placement Avascular bone graft and second stage implant placement
Mean resection Number of (cm) implants
Lost implants
6.5
19
1
5.5
18
10
5
15
3
We used 2-6 IMZ cylinder implants (Friatec, Mannheim, Germany). Uncovering of the implants took place at least 6 months after implantation. Prosthetic rehabilitation followed using a rigid bar screw--retained on the implants and a removable overdenture. The patients had a routine follow-up every 3 months during the first year following implantation and every 6 months thereafter. Radiographic studies included an orthopantomogram and dental films, using a standard filmholder and a rectangular technique for standard documentation. The marginal bone loss was taken from the orthopantomogram and dental films, the distances from the superior border of the implants without abutments to the apical border of the radiolucencies surrounding the implants were measured mesially and distally to the implants; geometric distortion was corrected by the known length of the implants. Apart from radiographic signs, osseointegration was proved by palpable stability. Peri-implant crevicular probing was measured mesial, distal, buccal and lingual to the implant. Further clinical parameters were established
Kaplan-Meier analysis of implant survival per implant was estimated, ignoring the dependence between implants in the same patient. Comparison of implant survival times between the three groups was performed on minimal survival time of the implants per patient. Since the most critical phase of implant survival is the time of osseointegration, the generalized Wilcoxon test for censored survival times was applied as it attributes more weight to the early phase as compared with the log-rank test. Marginal bone loss, crevicular probing depth, gingival index and sulcus bleeding index in patients 2 years after implantation were examined and analysed statistically (Group 1 : 1 0 patients, Group 2 : 4 patients, Group 3:4 patients). Concerning marginal bone loss and crevicular probing depth, mean values for implants per patient were established; concerning gingival index and sulcus bleeding index medians of the implants per patient were used. Patients, not single implants, were used as the sample unit for the statistical analysis. The Kruskal-Wallis test was used to assess the independent effect of Groups 1-3 classification on the outcome of marginal bone loss, crevicular probing depth, gingival index and sulcus bleeding index. All P-values are results of two-sided tests. The SAS statistical software system (SAS Institute, Cary, NC) was used for calculation. P-values <0.05 were considered as statistically significant. The aim of the study is to evaluate differences of osseointegration, condition of peri-implant bone and soft tissue, and implant survival rate, depending on the site of bone and soft tissue in which the implants had been placed.
RESULTS The results are presented in the Table 1 and Figures 1-3. Table 1 deals with the results of the implants having been placed (in total 136), the corresponding data of the single groups are presented in the Table 1. Figure 1 presents the Kaplan-Meier analysis (Kaplan and Meier 1958) of implant survival, showing a 3 years survival rate of 87.8% in Group 1, 69.1% in Group 2 and 58.3% in Group 3.
240
Journal of Cranio-Maxillofacial Surgery
The comparison of minimal implant survival times per patient gave a hint on possible differences between the groups (P < 0.10): Implants in transplanted bone showed a slightly lower minimum survival time. Figure 2 presents the results of marginal bone loss and probing depth: mean values for implants in each patient and mean values for each group are presented. There was no statistically significant difference between the groups (P>0.29). Figure 3 presents the results of gingival index and sulcus bleeding index: median values of the implants in each patient and median values of the patients in each group are presented. There was no statistically significant difference between the groups ( P > 0.68). The results of clinical investigation of denture retention and occlusion, and of the patients' satisfaction with masticatory and speech function are presented in Table 3.
DISCUSSION In patients who have been treated for squamous cell carcinoma of the oral cavity, conventional prosthetic restoration is often impossible. Scars, defects of soft tissue and bone result in an inadequate denture base for a mucosally-worn prosthesis. The placement of endosteal implants in irradiated bone is discussed controversially. Some authors present good results (Albrektsson, 1988; Parel and TjellstrOrn, 1991; Granstroem et al., 1992; Taylor and Worthington, 1993), others refuse to employ implant placement, considering the risk of postradiation osteonecrosis overshadowing the possible benefit of making prosthetic restoration (Fischer-Brandies, 1990). Most authors (Granstroem et al., 1992; Taylor and Worthington, 1993; Esser, 1994) agree that a long interval between radiotherapy and implant placement is preferable. Waechter and Stoll (1994) proved maximum bone damage to be at 6 months after irradiation. Therefore the implants were placed at least 1 year after irradiation. The uncovering of the implants was carried out 6 months after placement, since it is known that increased integration time also increases the amount of osseointegration in irradiated bone (Larsen et al., 1993). Regarding the results of implant survival according
to Kaplan-Meier, the survival rate in Group 1 was best (87.8%), no severe complication occurred in these patients. The survival rate in Group 2 was 69.1%. Four primarily osseointegrated implants were lost in one patient due to PRON. This patient had had a marginal resection of the anterior mandible and soft tissue reconstruction with a microvascular jejunal flap. One of four implants was lost 18 months after placement, caused by progressive loss of osseointegration (Fig. 6). The patient had very bad oral hygiene and after a further 8 months the rigid bar connecting the implants was removed to treat massive peri-implant inflammation. Two months later, the patient suffered from a mandibular fracture passing through the empty implant socket (Fig. 7). The rest of the implants had to be removed and a mandibular resection (Fig. 8) was carried out, histological evaluation proved PRON. It is known that primary radiotherapy of tumours, adjacent to the mandible or clinically invading it, as in the patient presented, is more likely to result in PRON (Murray et al., 1980). Therefore implant placement in the area of a marginal mandibular resection (Group 1) may be somewhat questionable. Probably, it would be more favourable to carry out segmental resection and bone grafting in these patients, if implant placement is considered later on. It has been reported that PRON occurs most frequently within the first year following irradiation but may also present many years later (Murray et al., 1980; Epstein et al., 1987). Therefore, whenever implant loss happens in irradiated bone, very careful follow-up is mandatory not to overlook development of PRON. We are concerned about this problem occurring in our patient, nevertheless in the other patients there has been no evidence of PRON after implant loss until now. It is remarkable that in the bone graft group (Group 3) there was a considerable amount of implant loss within the first months. Deficient osseointegration of all implants (10 in total) occurred in two patients within 6 months. In the other patients of Group 3, only four implants have been lost. Therefore the low survival rate (58.3%) in this group results from the failure in two patients. In one patient a bicortical iliac crest bone graft was transplanted and implants were placed simultaneously. Due to intraoral tissue breakdown, graft failure occurred and
Table 3 - Function of prostheses in patients wearing implant-supported overdenture (n = 17)
Group I Group II Group III All groups
Satisfactory Unsatisfactory Satisfactory Unsatisfactory Satisfactory Unsatisfactory Satisfactory Unsatisfactory
Denture retention, occlusion
Masticatory function
Speech function
3 1 7 3 4 0 14 4
2 2 6 4 3 1 11 7
3 1 7 3 3 1 13 5
Endosteal implants in the irradiated lower jaw
241
Fig. 6 - Orthopantomogram,demonstratingthe loss of one implant (arrow) 18 months after placementin a patient of Group 2.
Fig. 7 - Fracture of the mandible passing through the empty implant socket (arrow), histologyproved postradiation-osteonecrosis (PRON) 10 months later. all implants were lost. In the other patient, an iliac crest cancellous bone graft in Titanmesh ® was incorporated, implants were placed simultaneously, too. Postoperative wound dehiscence led to the intraoral exposure of the Titanmesh ® and grafted bone, graft and implants were lost. Dumbach et al. (1994) also presented poor results with the last mentioned method in irradiated patients. Since then, we no longer use these methods together with simultaneous implant placement. If ever simultaneous implant placement is contemplated, we think that it should be carried out only in vascularized grafts. They do not depend on the blood supply from the surrounding tissue
(Riediger, 1987), primary osseointegration of endosteal implants may be expected (Donovan et al., 1994). Concerning marginal bone loss, the best results have been observed in Group 3. In Group 2 the results were slightly better than in Group 1 as a considerable amount of marginal bone loss (mean 9 ram) was observed in one individual in the latter group. However, since these four implants are clinically stable, they are not presented as implant loss in the life table analysis. The crevicular probing depth presented higher mean values in Group 2 and Group 3 than in Group 1. The deeper pockets in Group 2 and 3 may be explained by the missing attached gingiva
242
Journal of Cranio-MaxillofacialSurgery
Fig. 8 - The implants were removedand segmental resectionof the mandible was carried out.
Fig. 9 - Orthopantomogramof a patient of Group 3: bone graftingwith a free iliac crest graft 1 year after tumour resection.Four IMZ implants placed in a secondstage procedure 8 months later. compared with Group 1, in which the implants are surrounded by local mucosa. The results of gingival index and sulcus bleeding index, indicating the degree of marginal infection, demonstrated inflammation of the pen-implant soft tissue in the majority of the implants. Therefore the median values are relatively high in all groups. On the one hand, the patients' bad oral hygiene is responsible for the marginal infection, on the other hand it is known that chronic soft tissue complications are relatively common in implants placed in transplanted soft tissue. (Mitchell et al., 1990). All of the above mentioned parameters may only be regarded as tendencies in our small
groups of patients, none of these values showed statistically significant differences between the three groups. In all groups, removable implant-supported prostheses have been used, since these give patients the ability to remove their prostheses to maintain meticulous hygiene, which is considered to be critical for long-term success (Sclaroffet al., 1994). Nevertheless, as presented above, good oral hygiene was seldom achieved in our patients. Moreover, in some patients masticatory function could not be reconstructed by incorporating an implant-supported denture prosthesis (Table3). The impaired tongue function
Endosteal implants in the irradiated lower jaw
243
Fig. 10 - Intraoral view of the patient after a further 8 months and the placement of a rigid bar screw--retained by the implants.
Fig. 11 - Intraoral view of the prosthetic restoration.
(Komisar et al., 1990) and an extreme postirradiation xerostomia was to a certain degree responsible for this problem. However, depending on the patient's compliance and efforts, the masticatory function gradually improved with time and the aesthetic improvement was a benefit to all the patients (Figs. 9, 10, 11). References Albrektsson, T.: A multicenter report on osseointegrated oral implants. J. Prosthet. Dent. 60 (1988) 337-340 Beumer, J., R. Harrison, B. Sanders, M. Kurrasch: Postradiation dental extractions: a review of literature and a report of 72 episodes. Head Neck Surg. 6 (1982) 581-586 Donovan, M. G., N. C. Dickerson, L. J.. Hanson, R. B. Gustafson: Maxillary and mandibular reconstruction using calvarial bone
grafts and Branemark implants: a preliminary report. J. Oral Maxillofac. Surg. 52 (1994) 588-594 Dumbach, J., H. Rodemer, W.. J. Spitzer, E. Bender: Grenzen der knoechernen Rekonstruktion des Unterkiefers mit autogener Spongiosa, Hydroxylapatitgranulat und Titangitter, insbesondere nach Strahlentherapie. Fortschr. Kiefer Gesichtschir. 39 (1994) 93-95 Epstein, J. B., F L. Wong, P. Stevenson Moore: Osteoradionecrosis: Clinical experience and a proposal for classification. J. Oral Maxillofac. Surg. 45 (1987) 104-110 Esser, E.: Enossale Implantate im radiogen belasteten Kiefer nach Tumorradikaloperation. Z. Zahnaerztl. Implantol. 10 (1994) 167-170 Fischer-Brandies, E.: Das Risiko enossaler Implantationen nach Radiatio. Quintessenz 5 (1990)873-876 Granstroem, G., M. Jacobsson, A. Tjellstroem: Titanium implants in irradiated tissue: Benefits from hyperbaric oxygen. Int. J. Oral Maxillofac. Implants 7 (1992) 15-25 Kaplan, E. L., P. Meier: Non-parametric estimation from incomplete observations. J. Am. Statistic. Assoc. 53 (1958) 457-65
244
Journal of Cranio-Maxillofacial Surgery
Komisar, A.: The functional result of mandible reconstruction. Laryngoscope 100 (1990) 364-374 Larsen, P. E., M. J. Stronczek, F. M. Beck, M. Rohrer: Osteointegration of implants in radiated bone with and without hyperbaric oxygen. J. Oral Maxillofae. Surg. 51 (1993) 280-287 Loe H., J. Silness: Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol. Scand. 22 (1963) 533-36 Martin, I. C., J. I. Cawood, E. D. Vaughan, N. Barnard." Endosseous implants in the irradiated composite radial forearm free flap. Int. J. Oral Maxillofac. Surg. 21 (5) (1992) 266-270 Marx, R. E.: Osteoradionecrosis: A new concept of its pathophysiology. Int. J. Oral Maxillofac. Surg. 41 (1983) 283-288 Marx, R. E., R. P. Johnson." Studies in the radiobiology of osteoradionecrosis and their clinical significance. Oral Surg. Oral Med. Oral Pathol. 64 (1987) 379-390 MeKenzie, M. R., F. L. Wong, J. B. Epstein, M. Lepawsky: Hyperbaric oxygen and postradiation osteonecrosis of the mandible. Oral Oncol. Eur. J. Cancer 29B (1993) 201-207 Mitchell, D., S. Synnott, J. Van Dercreek: Tissue reaction involving an intraoral skin graft and CP titanium abutments: a clinical report. Int. J. Oral Maxillofac. Implants 5 (1990) 79-84 Moseoso, J. F., J. Keller, E. Genden, H. Weinberg, H. F. Biller, D. Buchbinder, M. L. Urken: Vascularized bone flaps in oromandibular reconstruction. A comparative study of bone stock from various donor sites to assess suitability for enosseous dental implants. Arch. Otolaryngol. Head Neck Surg. 120 (1994) 36-43 Muehlemann, H. R.: Patientenmotivation mit individuellem Intensivprogramm fuer orale Gesundheit. In: Peters, S., (ed), Prophylaxe. Berlin: Quintessenz 1978, 137-49 Murray, C. G., J. Herson, Z E. Daly, S. Zimmermann: Radiation necrosis of the mandible: A 10-year study. I. Factors influencing the onset of necrosis. Int. J. Radiat. Oncol. Biol. Phys. 6 (1980) 543-548
Parel, S., A. Tjellstr6m: The United States and Swedish experience with osseointegration and facial prosthesis. Int. J. Oral Maxillofac. Implants 6 (1991) 75-79 Riediger, D.: Restoration of masticatory function by microsurgically revascularized iliac crest bone grafts using enosseous implants. Plast. Reconstr. Surg. 81 (1987) 861-876 Selaroff, A., B. Haughey, W. D. Gay, R. Paniello: Immediate mandibular reconstruction and placement of dental implants. At the time of ablative surgery. Oral Surg. Oral Med. Oral Pathol. 78 (1994) 711-717 Taylor, T. D., P. Worthington: Osseointegrated implant rehabilitation of the previously irradiated mandible: Results of a limited trial at 3 7 years. J. Prosthet. Dent. 69 (1993) 60-69 Urken, M. L., D. Buchbinder, H. Weinberg, C. Viekery, A. Sheiner, R. Parker, J. Schaefer, P. Som, A. Shapiro, W. Lawson: Functional evaluation following microvascular oromandibular reconstruction of the oral cancer patient: A comparative study of reconstructed and nonreconstructed patients. Laryngoscope 101 ( 1991) 935-950 Waeehter, R., P. Stoll: Moeglichkeiten und Grenzen enossaler Implantate bei der oralen Rehabilitation yon Tumorpatienten nach Bestrahlung. Z. Zahnaerztl. Implantol. 10 (1994) 171-176 Zlotow, I. M., Y. M. Huryn, Y. D. Piro, E. Lenchewski, D. A. Hidalgo: Osseointegrated implants and functional prosthetic rehabilitation in microvascular fibula free flap reconstructed mandibles. Am. J. Surg. 164 (6) (1992) 677-681 Dr Franz Watzinger Universit~tsklinik ft~r Kiefer-und Gesichtschirurgie Neue Universit~tskliniken Wien W~thringer Gt~rtel 18-20 A - 1090 Wien Austria Paper received 15 December 1995 Accepted 20 May 1996
Endosteal implants in the irradiated lower jaw F. Watzinger, R. Ewers, A. Henninger, G. Sudasch, A. Babka*, G. Woelfl**
University Clinicfor Maxillofaeial Surgery, (Head." Prof. Dr. Dr. Rolf Ewers), Medical School, * University Clinic for Dentistry, (Head." Prof. Dr. Rudolf Slavicek), Medical School, **Institute of Medical Statistics (Head." Prof. Dr. Peter Bauer), University of Vienna, Vienna, Austria
SUMMARY. Since 1990 Endosteal implants have been inserted in the irradiated lower jaw at our clinic. 1MZ implants have been used for dental rehabilitation in 26 patients (21 male, 5 female) suffering from squamous cell carcinomas stage T2-T4136. The implants were either placed in local bone and soft tissue (group 1, n = 6 0 implants), or in local bone after marginal mandibulectomy and transplanted soft tissue (group 2, n--26 implants), or in transplanted bone and soft tissue (group 3, n=52 implants). Life-table analysis according to Kaplan-Meier demonstrated a 3-year implant survival rate of 87.8% in Group 1, 69.1% in Group 2 and 58.3% in Group 3. There was no statistical significant difference in the amount of marginal bone loss and the degree of marginal infection between the three groups (P > 0.29). Major complications: A mandibular fracture passing through an empty implant socket 8 months after implant loss (Group 2) was caused by postradiation-osteonecrosis; implant removal and bone resection was mandatory. The poor results of the bone graft group may be explained by two patients, in whom simultaneous placement of implants in nonvascularized bone grafts was carried out, intraoral tissue breakdown led to graft failure and loss of the implants (n = 10).
restoration in patients having had mandibular resection and bone graft (Urken et al., 1991; Martin et al., 1992; Zlotow et al., 1992; Sclaroff et al., 1994; Donovan et al., 1994; Moscoso et al., 1994). Komisar (1990) asserted that restoration of mandibular continuity alone does not enhance function in the majority of head and neck cancer patients. The degree to which mastication is affected depends on the amount of mandible removed, but the status of tongue function is equally important. The use of osseointegrated implants can minimize masticatory limitations as well as improve facial contour.
INTRODUCTION Radiotherapy is an essential part of the treatment modalities in patients suffering from squamous cell carcinoma of the oral cavity. Denture retention is frequently compromised by inadequate saliva production following irradiation (Larsen et al., 1993). Moreover, many patients have surgical defects which cannot be adequately reconstructed without implants. In these patients endosteal implants may be placed either in irradiated local bone or in bone grafts. It is well known that irradiation causes tissue damage to structures adjacent to the tumour. Hypovascular, hypocellular and hypoxaemic tissue results (Marx, 1983; Marx and Johnson, 1987). Risks that must be discussed include postradiationosteonecrosis (PRON), fracture, development or recurrence of tumour with unknown risks of treatment, nonintegration of implants (early or delayed) and soft tissue problems (McKenzie et al., 1993). Accidental or surgical trauma leads to delayed wound healing and may include the risk of PRON. The risk of developing PRON depends on the radiation dose (Murray et al., 1980; Beumer et al., 1982), as well as on fractionation and volume of irradiated tissue. Nevertheless, some authors present good results of endosteal implants placed in irradiated bone (Albrektsson, 1988; Parel and TjellstrOm, 1991; Granstroem et al., 1992; Taylor and Worthington, 1993). Endosteal implants may also serve for prosthetic
MATERIAL AND METHODS Since 1990, endosteal implants have been placed in the irradiated lower jaw at our clinic. In 26 patients suffering from squamous cell carcinomas stage T2-T4, 136 IMZ implants have been used for dental rehabilitation. Twenty one patients were male and 5 female, their ages ranged between 41 and 79 (mean 62) years. After tumour staging including tattooing, preoperative radiochemotherapy was applied. Fractionated radiotherapy with a total dosage of 50 Gray was given. Surgery followed 4 weeks-3 months after irradiation. Radical tumour resection was carried out as a marginal mandibulectomy in five cases and segmental resection in 12 cases. Soft tissue reconstruction was carried out by a 237
238
Journal of Cranio-Maxillofacial Surgery
Table 1 - Distribution of the implants concerning function and implant loss Number of implants In function Without function Lost No osseointegration Marginal bone loss Recurrent tu., death Sum
All groups Group 1 Group 2
Group 3
78 16
38 8
15 0
25 8
10 16 16 136
0 7 7 60
0 5 4 24
10 4 5 52
GINGIVALINDEX
$ULCU$ BLEEDING INDEX
3~
3
251-
25
2-1 15 105 0. . . .
. . . .
• ,,
°o
2
--
15 --
1
,.°°
05 0
Fig. 3 - Gingival index (GI) according to Loe and Silness, 0-3; (0 = no inflammation, 3 = distinct inflammation; simplified). Sulcus bleeding index (BI) according to Muehlemann, 0-3; (0 = no bleeding on probing, 3 =distinct bleeding; simplified). Median values per patient (.); Median values per group (-).
Survival rate
60 j.
L_ 58.3%
50 40 30 20 100
i o
~
group 1
--
group 2
--
group 3
I
I
I
I
I
I
1
5
10
15
20
25
30
35
I mths 40
Fig. 1 - Implant survival rate according to Kaplan-Meier.
M A R G I N A L BONE LOSS
C R E V I C U L A R PROBING DEPTH
4
-" 3
!:
q
•
.I.
--
¸
2.
,*
=•
Fig. 4 - Implants inserted in the area of marginal resection of the mandible (Group 2). Fig. 2 - Marginal bone loss and crevicular probing depth (mm), mean values per patient (.); mean values per group (-).
local flap in twelve cases, by a myocutaneous pectoralis muscle flap in five cases, by a microvascular jejunal flap in seven cases, and by a microvascular osteomyocutaneous iliac graft in two cases. Bone reconstruction was performed by a microvascular iliac bone graft in three cases, by a free iliac crest bone graft in five cases, by a rib graft in two cases and by a cancellous iliac bone graft in Titanium mesh in two patients. Prosthetic rehabilitation was carried out by using endosteal implants, the minimum interval between irradiation and implant insertion was 12 months. We differentiate between three groups (Table 1, Figs. 1, 2, 3): Group 1: The implant socket irradiated local bone and soft tissue.
consisted
of
Group 2: The implant socket consisted of irradiated local bone in which marginal mandibulectomy had been carried out; the implant was surrounded by transplanted soft tissue (Fig. 4). Group 3: The implant socket consisted of transplanted bone (Fig. 5) and soft tissue, the transplant recipient region had been irradiated preoperatively. This group is rather heterogenous, since it contains microvascutar anastomosed bone grafts and different types of avascular bony reconstruction, primary and second step implant placement as well. These were summarized so as not to have too many small groups and to obtain a general view of implant placement in these patients. However, Table 2 presents the distribution of the implants and the rate of implant loss according to different types of bone grafting. In the event of two-step surgery the implants were placed at least 6 months after bony reconstruction.
Endosteal implants in the irradiated lower jaw
239
to estimate marginal infection: gingival index (L6e and Silness, 1963) and sulcus bleeding index (Miihlemann, 1978). The function of denture was evaluated regarding retention of the implantsupported overdenture and occlusion. The patients were questioned whether they felt satisfied with their masticatory function and whether speech function was satisfactory. Statistical methods
Fig. 5 - Implants inserted in bone grafts after segmental resection (Group 3). Table 2 - Distribution of implants in Group 3 according to the variable extent of resection and the various type of bone grafting Type of bone grafting Microvascular anastomosed bone graft and second stage implant placement Avascular bone graft and simultaneous implant placement Avascular bone graft and second stage implant placement
Mean resection Number of (cm) implants
Lost implants
6.5
19
1
5.5
18
10
5
15
3
We used 2-6 IMZ cylinder implants (Friatec, Mannheim, Germany). Uncovering of the implants took place at least 6 months after implantation. Prosthetic rehabilitation followed using a rigid bar screw--retained on the implants and a removable overdenture. The patients had a routine follow-up every 3 months during the first year following implantation and every 6 months thereafter. Radiographic studies included an orthopantomogram and dental films, using a standard filmholder and a rectangular technique for standard documentation. The marginal bone loss was taken from the orthopantomogram and dental films, the distances from the superior border of the implants without abutments to the apical border of the radiolucencies surrounding the implants were measured mesially and distally to the implants; geometric distortion was corrected by the known length of the implants. Apart from radiographic signs, osseointegration was proved by palpable stability. Peri-implant crevicular probing was measured mesial, distal, buccal and lingual to the implant. Further clinical parameters were established
Kaplan-Meier analysis of implant survival per implant was estimated, ignoring the dependence between implants in the same patient. Comparison of implant survival times between the three groups was performed on minimal survival time of the implants per patient. Since the most critical phase of implant survival is the time of osseointegration, the generalized Wilcoxon test for censored survival times was applied as it attributes more weight to the early phase as compared with the log-rank test. Marginal bone loss, crevicular probing depth, gingival index and sulcus bleeding index in patients 2 years after implantation were examined and analysed statistically (Group 1 : 1 0 patients, Group 2 : 4 patients, Group 3:4 patients). Concerning marginal bone loss and crevicular probing depth, mean values for implants per patient were established; concerning gingival index and sulcus bleeding index medians of the implants per patient were used. Patients, not single implants, were used as the sample unit for the statistical analysis. The Kruskal-Wallis test was used to assess the independent effect of Groups 1-3 classification on the outcome of marginal bone loss, crevicular probing depth, gingival index and sulcus bleeding index. All P-values are results of two-sided tests. The SAS statistical software system (SAS Institute, Cary, NC) was used for calculation. P-values <0.05 were considered as statistically significant. The aim of the study is to evaluate differences of osseointegration, condition of peri-implant bone and soft tissue, and implant survival rate, depending on the site of bone and soft tissue in which the implants had been placed.
RESULTS The results are presented in the Table 1 and Figures 1-3. Table 1 deals with the results of the implants having been placed (in total 136), the corresponding data of the single groups are presented in the Table 1. Figure 1 presents the Kaplan-Meier analysis (Kaplan and Meier 1958) of implant survival, showing a 3 years survival rate of 87.8% in Group 1, 69.1% in Group 2 and 58.3% in Group 3.
240
Journal of Cranio-Maxillofacial Surgery
The comparison of minimal implant survival times per patient gave a hint on possible differences between the groups (P < 0.10): Implants in transplanted bone showed a slightly lower minimum survival time. Figure 2 presents the results of marginal bone loss and probing depth: mean values for implants in each patient and mean values for each group are presented. There was no statistically significant difference between the groups (P>0.29). Figure 3 presents the results of gingival index and sulcus bleeding index: median values of the implants in each patient and median values of the patients in each group are presented. There was no statistically significant difference between the groups ( P > 0.68). The results of clinical investigation of denture retention and occlusion, and of the patients' satisfaction with masticatory and speech function are presented in Table 3.
DISCUSSION In patients who have been treated for squamous cell carcinoma of the oral cavity, conventional prosthetic restoration is often impossible. Scars, defects of soft tissue and bone result in an inadequate denture base for a mucosally-worn prosthesis. The placement of endosteal implants in irradiated bone is discussed controversially. Some authors present good results (Albrektsson, 1988; Parel and TjellstrOrn, 1991; Granstroem et al., 1992; Taylor and Worthington, 1993), others refuse to employ implant placement, considering the risk of postradiation osteonecrosis overshadowing the possible benefit of making prosthetic restoration (Fischer-Brandies, 1990). Most authors (Granstroem et al., 1992; Taylor and Worthington, 1993; Esser, 1994) agree that a long interval between radiotherapy and implant placement is preferable. Waechter and Stoll (1994) proved maximum bone damage to be at 6 months after irradiation. Therefore the implants were placed at least 1 year after irradiation. The uncovering of the implants was carried out 6 months after placement, since it is known that increased integration time also increases the amount of osseointegration in irradiated bone (Larsen et al., 1993). Regarding the results of implant survival according
to Kaplan-Meier, the survival rate in Group 1 was best (87.8%), no severe complication occurred in these patients. The survival rate in Group 2 was 69.1%. Four primarily osseointegrated implants were lost in one patient due to PRON. This patient had had a marginal resection of the anterior mandible and soft tissue reconstruction with a microvascular jejunal flap. One of four implants was lost 18 months after placement, caused by progressive loss of osseointegration (Fig. 6). The patient had very bad oral hygiene and after a further 8 months the rigid bar connecting the implants was removed to treat massive peri-implant inflammation. Two months later, the patient suffered from a mandibular fracture passing through the empty implant socket (Fig. 7). The rest of the implants had to be removed and a mandibular resection (Fig. 8) was carried out, histological evaluation proved PRON. It is known that primary radiotherapy of tumours, adjacent to the mandible or clinically invading it, as in the patient presented, is more likely to result in PRON (Murray et al., 1980). Therefore implant placement in the area of a marginal mandibular resection (Group 1) may be somewhat questionable. Probably, it would be more favourable to carry out segmental resection and bone grafting in these patients, if implant placement is considered later on. It has been reported that PRON occurs most frequently within the first year following irradiation but may also present many years later (Murray et al., 1980; Epstein et al., 1987). Therefore, whenever implant loss happens in irradiated bone, very careful follow-up is mandatory not to overlook development of PRON. We are concerned about this problem occurring in our patient, nevertheless in the other patients there has been no evidence of PRON after implant loss until now. It is remarkable that in the bone graft group (Group 3) there was a considerable amount of implant loss within the first months. Deficient osseointegration of all implants (10 in total) occurred in two patients within 6 months. In the other patients of Group 3, only four implants have been lost. Therefore the low survival rate (58.3%) in this group results from the failure in two patients. In one patient a bicortical iliac crest bone graft was transplanted and implants were placed simultaneously. Due to intraoral tissue breakdown, graft failure occurred and
Table 3 - Function of prostheses in patients wearing implant-supported overdenture (n = 17)
Group I Group II Group III All groups
Satisfactory Unsatisfactory Satisfactory Unsatisfactory Satisfactory Unsatisfactory Satisfactory Unsatisfactory
Denture retention, occlusion
Masticatory function
Speech function
3 1 7 3 4 0 14 4
2 2 6 4 3 1 11 7
3 1 7 3 3 1 13 5
Endosteal implants in the irradiated lower jaw
241
Fig. 6 - Orthopantomogram,demonstratingthe loss of one implant (arrow) 18 months after placementin a patient of Group 2.
Fig. 7 - Fracture of the mandible passing through the empty implant socket (arrow), histologyproved postradiation-osteonecrosis (PRON) 10 months later. all implants were lost. In the other patient, an iliac crest cancellous bone graft in Titanmesh ® was incorporated, implants were placed simultaneously, too. Postoperative wound dehiscence led to the intraoral exposure of the Titanmesh ® and grafted bone, graft and implants were lost. Dumbach et al. (1994) also presented poor results with the last mentioned method in irradiated patients. Since then, we no longer use these methods together with simultaneous implant placement. If ever simultaneous implant placement is contemplated, we think that it should be carried out only in vascularized grafts. They do not depend on the blood supply from the surrounding tissue
(Riediger, 1987), primary osseointegration of endosteal implants may be expected (Donovan et al., 1994). Concerning marginal bone loss, the best results have been observed in Group 3. In Group 2 the results were slightly better than in Group 1 as a considerable amount of marginal bone loss (mean 9 ram) was observed in one individual in the latter group. However, since these four implants are clinically stable, they are not presented as implant loss in the life table analysis. The crevicular probing depth presented higher mean values in Group 2 and Group 3 than in Group 1. The deeper pockets in Group 2 and 3 may be explained by the missing attached gingiva
242
Journal of Cranio-MaxillofacialSurgery
Fig. 8 - The implants were removedand segmental resectionof the mandible was carried out.
Fig. 9 - Orthopantomogramof a patient of Group 3: bone graftingwith a free iliac crest graft 1 year after tumour resection.Four IMZ implants placed in a secondstage procedure 8 months later. compared with Group 1, in which the implants are surrounded by local mucosa. The results of gingival index and sulcus bleeding index, indicating the degree of marginal infection, demonstrated inflammation of the pen-implant soft tissue in the majority of the implants. Therefore the median values are relatively high in all groups. On the one hand, the patients' bad oral hygiene is responsible for the marginal infection, on the other hand it is known that chronic soft tissue complications are relatively common in implants placed in transplanted soft tissue. (Mitchell et al., 1990). All of the above mentioned parameters may only be regarded as tendencies in our small
groups of patients, none of these values showed statistically significant differences between the three groups. In all groups, removable implant-supported prostheses have been used, since these give patients the ability to remove their prostheses to maintain meticulous hygiene, which is considered to be critical for long-term success (Sclaroffet al., 1994). Nevertheless, as presented above, good oral hygiene was seldom achieved in our patients. Moreover, in some patients masticatory function could not be reconstructed by incorporating an implant-supported denture prosthesis (Table3). The impaired tongue function
Endosteal implants in the irradiated lower jaw
243
Fig. 10 - Intraoral view of the patient after a further 8 months and the placement of a rigid bar screw--retained by the implants.
Fig. 11 - Intraoral view of the prosthetic restoration.
(Komisar et al., 1990) and an extreme postirradiation xerostomia was to a certain degree responsible for this problem. However, depending on the patient's compliance and efforts, the masticatory function gradually improved with time and the aesthetic improvement was a benefit to all the patients (Figs. 9, 10, 11). References Albrektsson, T.: A multicenter report on osseointegrated oral implants. J. Prosthet. Dent. 60 (1988) 337-340 Beumer, J., R. Harrison, B. Sanders, M. Kurrasch: Postradiation dental extractions: a review of literature and a report of 72 episodes. Head Neck Surg. 6 (1982) 581-586 Donovan, M. G., N. C. Dickerson, L. J.. Hanson, R. B. Gustafson: Maxillary and mandibular reconstruction using calvarial bone
grafts and Branemark implants: a preliminary report. J. Oral Maxillofac. Surg. 52 (1994) 588-594 Dumbach, J., H. Rodemer, W.. J. Spitzer, E. Bender: Grenzen der knoechernen Rekonstruktion des Unterkiefers mit autogener Spongiosa, Hydroxylapatitgranulat und Titangitter, insbesondere nach Strahlentherapie. Fortschr. Kiefer Gesichtschir. 39 (1994) 93-95 Epstein, J. B., F L. Wong, P. Stevenson Moore: Osteoradionecrosis: Clinical experience and a proposal for classification. J. Oral Maxillofac. Surg. 45 (1987) 104-110 Esser, E.: Enossale Implantate im radiogen belasteten Kiefer nach Tumorradikaloperation. Z. Zahnaerztl. Implantol. 10 (1994) 167-170 Fischer-Brandies, E.: Das Risiko enossaler Implantationen nach Radiatio. Quintessenz 5 (1990)873-876 Granstroem, G., M. Jacobsson, A. Tjellstroem: Titanium implants in irradiated tissue: Benefits from hyperbaric oxygen. Int. J. Oral Maxillofac. Implants 7 (1992) 15-25 Kaplan, E. L., P. Meier: Non-parametric estimation from incomplete observations. J. Am. Statistic. Assoc. 53 (1958) 457-65
244
Journal of Cranio-Maxillofacial Surgery
Komisar, A.: The functional result of mandible reconstruction. Laryngoscope 100 (1990) 364-374 Larsen, P. E., M. J. Stronczek, F. M. Beck, M. Rohrer: Osteointegration of implants in radiated bone with and without hyperbaric oxygen. J. Oral Maxillofae. Surg. 51 (1993) 280-287 Loe H., J. Silness: Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol. Scand. 22 (1963) 533-36 Martin, I. C., J. I. Cawood, E. D. Vaughan, N. Barnard." Endosseous implants in the irradiated composite radial forearm free flap. Int. J. Oral Maxillofac. Surg. 21 (5) (1992) 266-270 Marx, R. E.: Osteoradionecrosis: A new concept of its pathophysiology. Int. J. Oral Maxillofac. Surg. 41 (1983) 283-288 Marx, R. E., R. P. Johnson." Studies in the radiobiology of osteoradionecrosis and their clinical significance. Oral Surg. Oral Med. Oral Pathol. 64 (1987) 379-390 MeKenzie, M. R., F. L. Wong, J. B. Epstein, M. Lepawsky: Hyperbaric oxygen and postradiation osteonecrosis of the mandible. Oral Oncol. Eur. J. Cancer 29B (1993) 201-207 Mitchell, D., S. Synnott, J. Van Dercreek: Tissue reaction involving an intraoral skin graft and CP titanium abutments: a clinical report. Int. J. Oral Maxillofac. Implants 5 (1990) 79-84 Moseoso, J. F., J. Keller, E. Genden, H. Weinberg, H. F. Biller, D. Buchbinder, M. L. Urken: Vascularized bone flaps in oromandibular reconstruction. A comparative study of bone stock from various donor sites to assess suitability for enosseous dental implants. Arch. Otolaryngol. Head Neck Surg. 120 (1994) 36-43 Muehlemann, H. R.: Patientenmotivation mit individuellem Intensivprogramm fuer orale Gesundheit. In: Peters, S., (ed), Prophylaxe. Berlin: Quintessenz 1978, 137-49 Murray, C. G., J. Herson, Z E. Daly, S. Zimmermann: Radiation necrosis of the mandible: A 10-year study. I. Factors influencing the onset of necrosis. Int. J. Radiat. Oncol. Biol. Phys. 6 (1980) 543-548
Parel, S., A. Tjellstr6m: The United States and Swedish experience with osseointegration and facial prosthesis. Int. J. Oral Maxillofac. Implants 6 (1991) 75-79 Riediger, D.: Restoration of masticatory function by microsurgically revascularized iliac crest bone grafts using enosseous implants. Plast. Reconstr. Surg. 81 (1987) 861-876 Selaroff, A., B. Haughey, W. D. Gay, R. Paniello: Immediate mandibular reconstruction and placement of dental implants. At the time of ablative surgery. Oral Surg. Oral Med. Oral Pathol. 78 (1994) 711-717 Taylor, T. D., P. Worthington: Osseointegrated implant rehabilitation of the previously irradiated mandible: Results of a limited trial at 3 7 years. J. Prosthet. Dent. 69 (1993) 60-69 Urken, M. L., D. Buchbinder, H. Weinberg, C. Viekery, A. Sheiner, R. Parker, J. Schaefer, P. Som, A. Shapiro, W. Lawson: Functional evaluation following microvascular oromandibular reconstruction of the oral cancer patient: A comparative study of reconstructed and nonreconstructed patients. Laryngoscope 101 ( 1991) 935-950 Waeehter, R., P. Stoll: Moeglichkeiten und Grenzen enossaler Implantate bei der oralen Rehabilitation yon Tumorpatienten nach Bestrahlung. Z. Zahnaerztl. Implantol. 10 (1994) 171-176 Zlotow, I. M., Y. M. Huryn, Y. D. Piro, E. Lenchewski, D. A. Hidalgo: Osseointegrated implants and functional prosthetic rehabilitation in microvascular fibula free flap reconstructed mandibles. Am. J. Surg. 164 (6) (1992) 677-681 Dr Franz Watzinger Universit~tsklinik ft~r Kiefer-und Gesichtschirurgie Neue Universit~tskliniken Wien W~thringer Gt~rtel 18-20 A - 1090 Wien Austria Paper received 15 December 1995 Accepted 20 May 1996