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Mandibular reconstruction using electrically stimulated periosteum
8
J. Cranio-Max.-Fac.Surg. 18 (1990)
Surg. 18 (1990) 8-13 GeorgThiemeVerlagStuttgart 9 New York Jo.Cranid-Max.-Fac.
Mandibular Reconstruction Using Electrically Stimulated Periosteum Akihide KahmgaiI, Masahiko Mori I, Shiro Inoue2 l Dept. of Oral and MaxillofacialSurgery(Head:Prof. M. Mori, MD, and Prof. K. Shibata, MD),AsahiUniversitySchoolof Dentistry Dept. of OrthopaedicSurgery(Head:Prof. S. Inoue,MD),Murakami Memorial Hospital,Asahi University Submitted 7.2. 1989; accepted 30.5. 1989
Summary Electrically stimulated periosteum (ESP) grafting to a 12-year-old female patient who had had a segmental mandibulectomy in the anterior region following a diagnosis of Ewing's sarcoma was tried for the mandibular reconstruction. One year after the ESP transplantation, examination of the patient showed that fine, radio-opaque bone formation had occurred. The new technique consists of 1) electrical stimulation of the tibial periosteum with 20 microamperes for five weeks, and then 2) ESP transplantation into a titanium mesh tray placed in the mandibulectomized region. In the present report, these new procedures are detailed, and the process of calcification in the transplanted ESP is discussed. Key words
Introduction
Electrically stimulated periosteum (ESP) - Electric callus (EC) - Mandibular reconstruction - Bone grafting
Bone grafting methods for reconstructive surgery in oral and maxillofacial lesions,have been employed for a long time; and autogenous bone such as iliac bone (New and Many authors have demonstrated the ability of small Erich, 1944; Adekeye and Nigeria, 1978; Persson et al., amounts of electric current to stimulate bone formation in 1978), and metals and biomaterials have been used as imthe region of a cathode (Yasuda et al., 1955; Bassett et al., plant materials (Harben and Corgill, 1969; Bear et al., 1964; Minkin et al., 1968; Lavine et al., 1969; O'Connor 1971; Bear et al., 1973; Boyne, 1983; Nagamine et al., et al., 1969). When periosteum is electrically stimulated, 1987, Vuillemin et al., 1989). Compound or composite initially osteoprogenitor cells proliferated from the inner flaps (Snyder et al., 1970; Siemssen et al., 1978) with a layer of tile periosteum, and this highly proliferating perivascularized bone component (Cuono and Ariyan,1980; osteum was termed electrically stimulated periosteum Green et al., 1981) have also been employed in the field of (ESP) (Kamegai, 1986; Kamegai and Shibata, 1988; Sasaki oral-maxillofacial surgery. and lnoue, 1988). Prior to adolescence, mandibular reconstruction with iliac ESP is reported to have strong osteogenic potential (Kamebone grafts seems to be an inadequate method because gaia 1986; Kamegai and Shibata, 1988; Sasaki and Inoue, bone formation and calcification are not yet complete at 1988), and thus would be expected to be a good material that time (Crockford and Converse, 1972). In the case of il- for reconstruction of a region deficient in bone. Although iac bone grafts prior to adolescence, it disturbs the seconESP is a noncalcified bony tissue or osteoid, it has the potdary cehtres of ossification lying along the crest of the ential to differentiate into mature bone tissue in the recibone, and the bone may not develop fully (Crockford and pient bed. And since ESP is not a very hard tissue, it has Converse, 1972). the flexibility to take up various shapes in the recipient Reimplantation of autogenous freeze-dried mandibular bed. Furthermore, with ESP as a material for reconstrucbone (Bradley, 1982) is also supposed to be a useful methtion, it is possible to make bones of various shapes in the od for the reconstruction of a juvenile resected mandible, tray, when the tray as a retainer or a container is properly but this method seems to be difficult when the tumour bed applied. is too large to contain the bone tissue. Continuous electrical stimulation of the ESP forms calcifyBiomaterials of the bone augmentation type have merit as ing bone tissue, referred to as an electric callus (EC) (Yasua material for reconstruction in mature patients. However, da et al., 1955). The clinical application of the EC phenoin childhood, clinical application of such biomaterials folmel~on has been reported as a treatment for fractures lowing segmental mandibulectomy are not used because (Friedenberg et al., 1971; Lavine et al., 1972) or orthopaethese materials cannot grow along with the bone bed in dic treatment of congenital pseudoarthrosis (Brighton et the graft area. Boyne (1983)reported that a titanium mesh al., 1975). However, no report has been made on ESP implant, placed immediately in the discontinuity defect grafting i n ~ s p e c t of its clinical application in mandibular following the resection of the mandible, resulted in comreconstrucuon. plete bone regeneration without the use of bone graft maIn the present report, this new method of ESP transplantaterials in children between the ages of 5 and 14 and betion with a titanium mesh tray for the reconstruction of a lieved that a new p~riosteum was formed and bone would mandibular defect after segmental resection will be preform de novo within the titanium mesh implant. However, 9sented; and some problems of the new method, that arose in the present case, the evidences of regeneration of the during a follow-up study of one year's duration after the juvenile periosteum a n d ' b o n e regeneration could not be ESP transplantation, will also be described, as mono-layer found, only the electric callus (EC) formation within the titransplantation of the ESP was not enough to maintain tanium mesh was found. proper mandibular function.
Mandibular Reconstruction Ushtg Electrically Stimulated Periostertm
J. Cranio-Max.-Fac. Surg. 18 (I 990)
9
~
t Fig.1 a Five weeks after transplantation. Slight radiopacities were detected in the titanium tray. Fig.1
Fig.1 b Ten weeks after transplantation. Features of calcification were evident.
Fig.1 e One year after transplantation. Definite bone formation is clearly seen in the mesh tray.
Radiographs after transplantation.
Case Report A 12-year-old girl diagnosed as having Ewing's sarcoma located in tile anterior part of the mandible underwent anterior segmental mandibulectomy, and the space was retained with an AO plate. As the AO plate became partially exposed three months after operation, ESP grafting for mandibular reconstruction was planned. Following highdose M T X rescue therapy, seven months after the segmental mandibulectomy, electrical stimulation of the tibial periosteum with 20 microamperes was begun. Five weeks after continuous electrical stimulation of the tibial periosteum, the periosteum was raised and transplanted into a titanium mesh tray that was inserted into the mandibular defect following removal of the AO plate. The titanium mesh tray was used as a space maintainer and container. One year after the operation, definite bone formation could be demonstrated in the transplant region by X-ray examination (Fig. 1 c). Technique for Electrical Stimulation of the Periosteum The left tibiM periosteum of the patient was electrically stimulated for 5 weeks. The cathodic electrodes were inserted into the tibial bone through the skin under radiographic control with epidural anaesthesia, and anodes were put on the skin (Figs. 2 and 3 a). The cathodes were made of Kirschner wire of 2 mm diameter. The top 20 mm of each had a screw thread for insertion into the bone. The remainder was coated with Teflon (Fig. 4 a). The electrode of an electrocardiograph was ~ e d as the anode (Fig. 2), and had to be repositioned every t h r e e days to protect against bulla formation. The cathodes inserted into the tibial bone for the electric stimulation of the periosteum were arranged in two rows,
Fig.2 Complete view of electric stimulation for tibial periosteum (left leg). The cathodes were inserted into the tibial bone and fixed by resin. The electrode of an electrocardiogram was used as an anode. The anodes were applied to the adjacent skin near the cathodes. The power pack was bandaged to the tibia.
10
J. Cranio-Max.-Fac. 8urg. 18 (I990)
Akibide Kamegai et al.
FIg.4a The electrode for cathode. The top 2 cm was inserted into the tibial bone to touch the periosteum. The middle 7 cm was covered by Teflon for insulation.
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FIg.3a Photograph of cathodes inserted into the tibia.
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Fig.3 b No marked radiopaque area was found around the electrodes in the five-week ESP of the tibial shaft.
I
30
Flg.4 b The circuit chart. Each circuit provided the electric power to each electrode. The current should be always kept at 20 microamps.
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Fig.3c The elevation of the ESP for transplantation.
1.5 cm apart, and cathodes in each row were spaced 1 cm apart. Each row contained 10 cathodes, giving a total of 20 (Figs. 3 a and b). The electrodes thus defined an area having the same length and width as the mandibular bon6 defect as measured on X-ray and by visual inspection. After insertion of the 20 electrodes as cathodes, they were fixed to each other with r~sin, and the lead wires of the cathodes were connected to cathodes (Fig. 2). After commencing the electrical stimulation, antibiotics were admini-
200
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stered for 5"days prophylactically. The other procedures were disinfection of the skin around the cathodes with 1% 2-ethoxy-6,9-diaminoacridinium-hydrochloride paste, monitoring of the current and its maintenance at 20 mic"roamperes, and replacement of the anode every three days. The patient could live normally except that hard work was avoided. The power source was positioned outside the tibia and output was adjusted to 20 microamperes in vivo by a
Mandibular Reconstruction Using Electrically Stimulated Periosteum
J. Cranio-Max.-Fac. Surg. 18 (1990)
11
rheostat, for protection against decreasing power due to depolarization (Fig. 4b). As the current must always be kept at 20 microamperes, it was measured with an ammeter and adjusted by rheostat every three days. ESP Transplantation
The 3 • 12cm ESP was elevated (Fig. 3c) following skin incisign finder general anaesthesia and immediately transplanted into the mandibular defect after segmental mandibulectomy in the anterior region. From the follow-up study, it is clear that double or triple overlapped layers of the ESP should be used to obtain a thick and solid mandible for proper function. A titanium mesh tray was used as a space maintainer and container of the transplanted ESP. The lingual half of the tray was cut off.
i'
Fig.5 Histopathology of transplanted ESP. The ESP was conposed of a cell-rich layer and newly formed bone with osteoblasts.
Maintenance after ESP Transplantation
Intermaxillary fixation was not used. Drainage or continuous suction may sometimes be necessary for protection against infection, but any device used should be removed three days after the operation. Antibiotics should also be administered in the usual way. Just after the patient has recovered from anaesthesia and has had a bowel movement, talking and self feeding are encouraged. Because continuous electric stimulation causes the ESP to differentiate into an EC (Kamegai, 1986; Kamegai and Shibata, 1988), and because mastication produces 0.5 mV to 5 mV of piezoelectricity (Cochran et al., 1967), the piezoelectricity alone should provide reasonable electric power for bone remodelling. Hard physical work must be prohibited for at least three months, i.e., until the tibial periosteum has regenerated, to protect against pathological fracture. Histopathology of Transplanted ESP A small piece of ESP from the transplant was obtained for histopathological examination with HE staining. The transplanted ESP was composed of a thickened outer layer of periosteum, and underlying proliferated, undifferentiated mesenchymal cells, osteoblasts differentiated from proliferated undifferentiated mesenchymal cells, and osteoid (Fig. 5). X-ray Examination and Clinical Findings after the ESP Transplantation Two weeks after transplantation, radio-opacity could hardly be seen in the transplanted ESP in the mandible. By five weeks after ESP grafting, however, radio-opacities were detected'in small limited areas (Fig. I a). And by ten weeks, features of calcification were evident on X-ray (Fig. 1 b). One year after the ESP transplantation, evidence of definite bone formation was clearly seen in the mesh tray (Fig. I c), but incorporation of the newly formed bone into the mandibular bone could not be seen on the X-ray film (Fig. I c). Although slight movement of the titanium mesh tray was palpable just after the ESP transplantation, a solid mandible had formed clinically one year after the ESP transplantation.
Discussion
Periosteum has the power to change into bone tissue when it is electrically stimulated. Recently, the following reports have appeared, describing experimental bone induction by electrical stimulation. Sasaki and Inoue (1988) reported that new bone tissue was found in 40 out of 44 rats (90.9 %) when rat tibial periosteum, electrically stimulated for 6 days by 8 to 10 microamps of direct current, was grafted into the rat axillary muscle. Kamegai (1986) and Kamegai and Shibata (1988) stated that the defective palatal bone region of Maccaca monkeys was filled with newly formed bone tissue one month after transplantation of periosteum that had been electrically stimulated with 20 microamps of direct current for 2 weeks; however, no bone formation was detected in the non-ESP-transplanted region. We expected that osteogenesis of ESP would be strong enough to form bone tissue even in a defective bone region after segmental resection, and that ESP would be a useful bone source for use in children. These were the reasons why ESP grafting was planned for this child. The tibia is supposed to be the best source for producing ESP, because it is long and wide, and can provide enough ESP for defective bone in any region. As the region of the cruris anterior has thin connective tissue beneath tile skin, the ESP can easily be elevated and removed surgically. Tile lower third of tile tibia should be avoided as a source of ESP, however, because it is too slender to form enough ESP. The patient complained that the left leg felt heavy .and no'tmal physical exercise was difficult. Nonetheless, five weeks of electric stinmlation of tile periosteum should be used to ensure a sufficient amount of ESP for use in tile recipient bed. Histopathologi~ily, three phases have been noted in the progression of'ESP to EC (Kanmgai et al., 1988): 1) tile first phase exhibits proliferation of undifferentiated mesenchymal cells from the inner or cambium layer, 2) tile second phase shows the change of undifferentiated me.,enchymal cells into osteoblasts, and then osteoid tissue formation, and 3) the third phase displays bone tissue formation from the osteoid structure. The ESP thus has strong osteogenic potential and tile EC is the final stage of tile ESP, that is, a very highly calcified ESP.
12
1. Cranio-Max.-Fac. Surg. 18 (1990)
The caihodes made from Kirschner wires were carfully inserted and reconfirmed radiologically to be in the correct position to stimulate the tibial periosteum. The number of cathodes had to be determined by the length and width of the bone defect, because each cathode (electrode) may make an ESP or EC of only about 1 or 2 cm in diameter (Zengo et al., 1976). In the present case, segmental resection of.the mandible resulted in a bone defect measuring 11 e~n • 2.5 cm; therefore 20 electrodes arranged in 2 rows were inserted. Any site for the electrodes is acceptable, except-for the growing area near the epiphysis in order to prevent inhibition of growth of the tibia. The anodes are applied to the skin adjacent to the cathodes, and their position must be changed at least every three days. Otherwise the anode will induce a bulla on the skin just beneath the point of application if it remains on the same skin site too long. The current was measured and readjusted at least every two or three days to maintain 20 microamps, in vivo, continuously since depolarization decreases the current (Brighton et al., 1975). Yasuda et al. (1955) reported that a reasonable out-put for EC formation was within the range from 1 microamp, to 100 microamps, of direct current; below 1 microamp, no bone forms, over 100 microamps. cartilaginous callus appeurs, and more than 1000 microamps, causes bone destruction. Direct current electrical stimulation has been in clinical use for the treatment of nonunions and pseudarthroses of the long bones (Lavin et al., 1977; Brighton et al., 1981), and animal studies have suggested its potential for increasing healing rates of a mandibular fracture (Zengo et al., 1976; Masureik and Eriksson, 1977; Shandler et al., 1979). The application of 3 to 5 microamps, produced bone growth in the vicinity of mandibular drill holes in dogs (Zengo et al., 1976). Slot osteotomies in the dog mandible healed faster following stimulation with 12 microamps. (Shandler et al., 1979). Mobility in jaw fractures in 40 patients has been reported to be reduced, as judged from clinical examination and periodontometer measurement, following treatment with 10 to 20 microamps. (Masureik and Eriksson, 1977). The ESP is stripped from the tibia by chisel using ordinary hand pressure. The outside layer of the ESP is chiefly composed of osteoprogenitor cells that have marked osteogenic propensity (Kamegai, 1986; Kamegai and Shibata, 1988; Sasaki and Inoue, 1988) like the inner layer of the periosteum (Burman and Umansky, 1930; Haldeman, 1933); therefore the outer surface of the ESP should be removed as gently as possible. The titanium mesh tray was used as both a space maintainer and container, because the ESP itself is not calcified enough to maintain the shape o f the mandibular arch. The titanium mesh tray can be removed when definable bone formation is identified radiologically. From our follow-up study both with X-rays and clinical observation of this case, it appears that the procedure could be improved by the use of double or triple overlapping layers of ESP in order to produce a thicker and more solid mandible for psoper function. Conclusions From the present case, ESP transplantation certainly formed identifiable bone as judged by X-ray examination. ESP grafting seems to be a useful method for mandibular
Akihide Kamegai et al. reconstruction in the y o u n g patient who does not have 9enough donor bone for transplantation. References Adekeye, F~0., K. Nigeria: Reconstruction of mandibular defects by autogenous bone grafts: a review of 37 cases. J. Oral Surg. 36 (1978) 125 Basset, C. A. L, IL J. Pawluk, tL 0. Becker: Effect of electric current on bone in vivo. Nature 204 (1964) 652 Bear, S. ~, ILK. Green, W. W. Wentz: Stainless steel wire mesh - an aid in difficult oral surgery problems. J. Oral Surg. 29 (1971) 27 Bear, S. E., F. Chairsell, L Cuttino, IL L Ewing: Experimental use of stainless steel wire mesh in mandibular defects. J. Oral Surg. 31 (1973) 348 Boyne, P. J.: The restoration of resected mandibles in children without the use of bone grafts. Head Neck Surg. 6 (1983) 626 Bradley, P. F.: A two-stage procedure for reimplantation of autogenous freeze-treated mandibular bone. J. Oral Maxillofac. Surg. 40 (1982) 278 Brighton, C. T., A. Steven, B. J. Black, N. Itada, Z. B. Friedenberg: Cathodic oxygen consumption and electrically induced osteogenesis. Clin. Orthopaed. Rel. Res. 107 (1975) 277 Brighton, C. T., Z. B. Friedenberg, L M. Zemsky, P. R. Pollis: Direct current stimulation of nonunion and congenital pseudoarthrosis. J. Bone Joint Surg. 57 A (1975) 368 Brighton, C. T., J. Black, Z. B. Friedenberg, J. L Esterhall, L J. Day, J. F. Connolly: A multicenter study of the treatment of nonunion with constant direct current. J. Bone Joint Surg. 63 A (1981) 2 Burnmn, M. S., M. Umansky: An experimental study of free periosteal transplants, wrapped around tendon. J. Bone Joint Surg. 12 (1930) 579 Cochran, G. V. B., R. J. Pawluk, C. A. L. Bassett: Stress generated electric potentials in the mandible and teeth. Arch. Oral Biol. 12 (1967) 917 Crockford, D. A., J. M. Converse: The ilium as a source of bone grafts in children. Plast. Reconstr. Surg. S0 (1972) 270 Cuono, C. B., S. Ariyan: Immediate reconstruction of a mandibular defect with a regional osteomusculocutaneous flap. Plast. Reconstr. Surg. 65 (1980) 477 Friedenberg, 7_, B., M. C. Harlow, C. T. Brighton: Healing of nonunion of the medial malleolus by means of direct current. A case report. J. Trauma 11 (1971) 883 Green, M. F., J. R. Gibson, J. R. Bryson, E. Thomson: A one-stage correction of mandibular defects using a split sternum pectoralis major osteo-musculocutaneous transfer. British J. plast. Surg. 34 (1981) 11 Harben, G. W., D. A. Corgill: Chrome cobalt mesh mandibular prosthesis. J. Oral Surg. 27 (1969) 5 Haldenmn, K. 0.: The influence of periosteum on the survival of bone grafts. J. Bone Joint Surg. 15 (1933) 302 Kamegai, A.: An experimental study on boneless bone grafting for the maxillary bone defect region using the electrically stimulated periosteum. Jpn. J. Oral Maxillofac. Surg. 32 (1986) 2220 Kamegai, A,, K. Sbibata: Knochenlose Knochentransplantation d~ch elektrisch stimuliertes Periost. VorKiufiger Bericht und klinische Anwendung. Dtsch. Zahn~irztl. Z. 43 (1988) 26 Kamegai, A,, Y. Muranmts~6 Y. Matuoka, K. Sbibata, S. lnoue: Autoradiographic study for calcium detection on the process of electric callus formation. JJBERS 2 (1988) 73 Lavine, L S.,,~ Lustrin, M. H. Shamos: Experimental model for studying the effect of electric current on bone in vivo. Nature 224 (1969) 1112 Lavi,m, L S., I. Lustrin, M. H. Sbamos, IL A. Ri~mldi, A. tL Liboff: Electric enhancement of bone healing. Science 17S (1972) 1118 9Lavine, L S., I. Lustrin, M. H. Shamos: Treatment of congenital pseudoarthrosis of the tibia with constant direct current. Clin. Orthop. 124 (1977) 69 Masureik, C., C. Eriksson: Preliminary clinical evaluation of the effect of small electrical currents on the healing of jaw fractures. Clin. Orthop. 24 (1977) 84
Mandibular Reconstruction Using Electrically Stimulated Periosteum Minkin, C.,'B. R. Poultotb W. H. Hoover:The effect of direct current on bone. Clin. Orthop. 57 (1968) 303 Nagamitte, T., H. Yakata, T. Nakajima: Secondary reconstruction of the mandible with an aluminum oxide prosthesis. J. Oral Maxillofac. Surg. 45 (1987) 173 New, G. B., J. B. Erich: Bone grafts to the mandible. Am. J. Surg. 63 (1944) 155 O'Connor, B. T., H. M. Cbarlton, J. D. Currey, D. R. S. Kirby, C. Woods: Effects of electric current on bone in vivo. Nature 222 (1969) 162 Persson, G., P. tk Lundgren, S. Stenstroem: Mandibular reconstruction with bone grafts. Int. J. Oral Surg. 7 (1978) 512 Sasaki, H., S. lno~te: Electrically stimulated periosteal grafting in the rat. J. Jpn. Orthop. Assoc. 62 (1988) 57 Sbandler, H. S., S. Weinsteht, L. E. Nathan: Facilitated healing of osseous lesions in the canine mandible after electrical stimulation. J. Oral Surg. 37 (1979) 782 Siemssen, S. 0., B. Kirkby, T. P. F. O'Connor: Immediate reconstruction of a resected segment of lower jaw, using a compound flap of clavicle and sternomastoid muscle. Hast. Reconstr. Surg. 61 (1978) 724
fl Cranio-Max.-Fac. Surg. 18 (1990)
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Snyder, C. C., J. M. Bateman, G. D. Warden: Mandibulo-facial restoration with live osteocutaneous flaps. Hast. Reconstr. Surg. 45 (1970) 14 Vuillemin, T., J. Raveb, F. Sutter: Mandibular reconstruction with the Thorp condylar prosthesis after hemimandibulectomy. J. Cranio-Max.-Fac. Surg. 17 (1989) 78 Yasuda, L, K. Nogucbi, T. Sara: Dynamic callus and electric callus. J. Bone Joint Surg. 37 A (1955) 1292 Zengo, tL N., C. A. 1_, Bassett, G. Prountzos, IL J. Pawluk, A. Pilla: In vivo effects of direct current in the mandible. J. Dent. Res. 55 (1976) 383
A. Kamegai, DDS, PbD Department of Oral and Maxillofacial Surgery Asahi UniversitySchool of Dentistry 18S 1- 1 Hozumi Hozumi-cbo Motosu-gun Gift Japan
J. Cranio-Max.-Fac.Surg. 18 (1990)
Surg. 18 (1990) 8-13 GeorgThiemeVerlagStuttgart 9 New York Jo.Cranid-Max.-Fac.
Mandibular Reconstruction Using Electrically Stimulated Periosteum Akihide KahmgaiI, Masahiko Mori I, Shiro Inoue2 l Dept. of Oral and MaxillofacialSurgery(Head:Prof. M. Mori, MD, and Prof. K. Shibata, MD),AsahiUniversitySchoolof Dentistry Dept. of OrthopaedicSurgery(Head:Prof. S. Inoue,MD),Murakami Memorial Hospital,Asahi University Submitted 7.2. 1989; accepted 30.5. 1989
Summary Electrically stimulated periosteum (ESP) grafting to a 12-year-old female patient who had had a segmental mandibulectomy in the anterior region following a diagnosis of Ewing's sarcoma was tried for the mandibular reconstruction. One year after the ESP transplantation, examination of the patient showed that fine, radio-opaque bone formation had occurred. The new technique consists of 1) electrical stimulation of the tibial periosteum with 20 microamperes for five weeks, and then 2) ESP transplantation into a titanium mesh tray placed in the mandibulectomized region. In the present report, these new procedures are detailed, and the process of calcification in the transplanted ESP is discussed. Key words
Introduction
Electrically stimulated periosteum (ESP) - Electric callus (EC) - Mandibular reconstruction - Bone grafting
Bone grafting methods for reconstructive surgery in oral and maxillofacial lesions,have been employed for a long time; and autogenous bone such as iliac bone (New and Many authors have demonstrated the ability of small Erich, 1944; Adekeye and Nigeria, 1978; Persson et al., amounts of electric current to stimulate bone formation in 1978), and metals and biomaterials have been used as imthe region of a cathode (Yasuda et al., 1955; Bassett et al., plant materials (Harben and Corgill, 1969; Bear et al., 1964; Minkin et al., 1968; Lavine et al., 1969; O'Connor 1971; Bear et al., 1973; Boyne, 1983; Nagamine et al., et al., 1969). When periosteum is electrically stimulated, 1987, Vuillemin et al., 1989). Compound or composite initially osteoprogenitor cells proliferated from the inner flaps (Snyder et al., 1970; Siemssen et al., 1978) with a layer of tile periosteum, and this highly proliferating perivascularized bone component (Cuono and Ariyan,1980; osteum was termed electrically stimulated periosteum Green et al., 1981) have also been employed in the field of (ESP) (Kamegai, 1986; Kamegai and Shibata, 1988; Sasaki oral-maxillofacial surgery. and lnoue, 1988). Prior to adolescence, mandibular reconstruction with iliac ESP is reported to have strong osteogenic potential (Kamebone grafts seems to be an inadequate method because gaia 1986; Kamegai and Shibata, 1988; Sasaki and Inoue, bone formation and calcification are not yet complete at 1988), and thus would be expected to be a good material that time (Crockford and Converse, 1972). In the case of il- for reconstruction of a region deficient in bone. Although iac bone grafts prior to adolescence, it disturbs the seconESP is a noncalcified bony tissue or osteoid, it has the potdary cehtres of ossification lying along the crest of the ential to differentiate into mature bone tissue in the recibone, and the bone may not develop fully (Crockford and pient bed. And since ESP is not a very hard tissue, it has Converse, 1972). the flexibility to take up various shapes in the recipient Reimplantation of autogenous freeze-dried mandibular bed. Furthermore, with ESP as a material for reconstrucbone (Bradley, 1982) is also supposed to be a useful methtion, it is possible to make bones of various shapes in the od for the reconstruction of a juvenile resected mandible, tray, when the tray as a retainer or a container is properly but this method seems to be difficult when the tumour bed applied. is too large to contain the bone tissue. Continuous electrical stimulation of the ESP forms calcifyBiomaterials of the bone augmentation type have merit as ing bone tissue, referred to as an electric callus (EC) (Yasua material for reconstruction in mature patients. However, da et al., 1955). The clinical application of the EC phenoin childhood, clinical application of such biomaterials folmel~on has been reported as a treatment for fractures lowing segmental mandibulectomy are not used because (Friedenberg et al., 1971; Lavine et al., 1972) or orthopaethese materials cannot grow along with the bone bed in dic treatment of congenital pseudoarthrosis (Brighton et the graft area. Boyne (1983)reported that a titanium mesh al., 1975). However, no report has been made on ESP implant, placed immediately in the discontinuity defect grafting i n ~ s p e c t of its clinical application in mandibular following the resection of the mandible, resulted in comreconstrucuon. plete bone regeneration without the use of bone graft maIn the present report, this new method of ESP transplantaterials in children between the ages of 5 and 14 and betion with a titanium mesh tray for the reconstruction of a lieved that a new p~riosteum was formed and bone would mandibular defect after segmental resection will be preform de novo within the titanium mesh implant. However, 9sented; and some problems of the new method, that arose in the present case, the evidences of regeneration of the during a follow-up study of one year's duration after the juvenile periosteum a n d ' b o n e regeneration could not be ESP transplantation, will also be described, as mono-layer found, only the electric callus (EC) formation within the titransplantation of the ESP was not enough to maintain tanium mesh was found. proper mandibular function.
Mandibular Reconstruction Ushtg Electrically Stimulated Periostertm
J. Cranio-Max.-Fac. Surg. 18 (I 990)
9
~
t Fig.1 a Five weeks after transplantation. Slight radiopacities were detected in the titanium tray. Fig.1
Fig.1 b Ten weeks after transplantation. Features of calcification were evident.
Fig.1 e One year after transplantation. Definite bone formation is clearly seen in the mesh tray.
Radiographs after transplantation.
Case Report A 12-year-old girl diagnosed as having Ewing's sarcoma located in tile anterior part of the mandible underwent anterior segmental mandibulectomy, and the space was retained with an AO plate. As the AO plate became partially exposed three months after operation, ESP grafting for mandibular reconstruction was planned. Following highdose M T X rescue therapy, seven months after the segmental mandibulectomy, electrical stimulation of the tibial periosteum with 20 microamperes was begun. Five weeks after continuous electrical stimulation of the tibial periosteum, the periosteum was raised and transplanted into a titanium mesh tray that was inserted into the mandibular defect following removal of the AO plate. The titanium mesh tray was used as a space maintainer and container. One year after the operation, definite bone formation could be demonstrated in the transplant region by X-ray examination (Fig. 1 c). Technique for Electrical Stimulation of the Periosteum The left tibiM periosteum of the patient was electrically stimulated for 5 weeks. The cathodic electrodes were inserted into the tibial bone through the skin under radiographic control with epidural anaesthesia, and anodes were put on the skin (Figs. 2 and 3 a). The cathodes were made of Kirschner wire of 2 mm diameter. The top 20 mm of each had a screw thread for insertion into the bone. The remainder was coated with Teflon (Fig. 4 a). The electrode of an electrocardiograph was ~ e d as the anode (Fig. 2), and had to be repositioned every t h r e e days to protect against bulla formation. The cathodes inserted into the tibial bone for the electric stimulation of the periosteum were arranged in two rows,
Fig.2 Complete view of electric stimulation for tibial periosteum (left leg). The cathodes were inserted into the tibial bone and fixed by resin. The electrode of an electrocardiogram was used as an anode. The anodes were applied to the adjacent skin near the cathodes. The power pack was bandaged to the tibia.
10
J. Cranio-Max.-Fac. 8urg. 18 (I990)
Akibide Kamegai et al.
FIg.4a The electrode for cathode. The top 2 cm was inserted into the tibial bone to touch the periosteum. The middle 7 cm was covered by Teflon for insulation.
J i ,-..:
,-=
FIg.3a Photograph of cathodes inserted into the tibia.
D~
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t~
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FET
Fig.3 b No marked radiopaque area was found around the electrodes in the five-week ESP of the tibial shaft.
I
30
Flg.4 b The circuit chart. Each circuit provided the electric power to each electrode. The current should be always kept at 20 microamps.
Kn
6.2V
I "
--
Fig.3c The elevation of the ESP for transplantation.
1.5 cm apart, and cathodes in each row were spaced 1 cm apart. Each row contained 10 cathodes, giving a total of 20 (Figs. 3 a and b). The electrodes thus defined an area having the same length and width as the mandibular bon6 defect as measured on X-ray and by visual inspection. After insertion of the 20 electrodes as cathodes, they were fixed to each other with r~sin, and the lead wires of the cathodes were connected to cathodes (Fig. 2). After commencing the electrical stimulation, antibiotics were admini-
200
K~
_
+
Output
stered for 5"days prophylactically. The other procedures were disinfection of the skin around the cathodes with 1% 2-ethoxy-6,9-diaminoacridinium-hydrochloride paste, monitoring of the current and its maintenance at 20 mic"roamperes, and replacement of the anode every three days. The patient could live normally except that hard work was avoided. The power source was positioned outside the tibia and output was adjusted to 20 microamperes in vivo by a
Mandibular Reconstruction Using Electrically Stimulated Periosteum
J. Cranio-Max.-Fac. Surg. 18 (1990)
11
rheostat, for protection against decreasing power due to depolarization (Fig. 4b). As the current must always be kept at 20 microamperes, it was measured with an ammeter and adjusted by rheostat every three days. ESP Transplantation
The 3 • 12cm ESP was elevated (Fig. 3c) following skin incisign finder general anaesthesia and immediately transplanted into the mandibular defect after segmental mandibulectomy in the anterior region. From the follow-up study, it is clear that double or triple overlapped layers of the ESP should be used to obtain a thick and solid mandible for proper function. A titanium mesh tray was used as a space maintainer and container of the transplanted ESP. The lingual half of the tray was cut off.
i'
Fig.5 Histopathology of transplanted ESP. The ESP was conposed of a cell-rich layer and newly formed bone with osteoblasts.
Maintenance after ESP Transplantation
Intermaxillary fixation was not used. Drainage or continuous suction may sometimes be necessary for protection against infection, but any device used should be removed three days after the operation. Antibiotics should also be administered in the usual way. Just after the patient has recovered from anaesthesia and has had a bowel movement, talking and self feeding are encouraged. Because continuous electric stimulation causes the ESP to differentiate into an EC (Kamegai, 1986; Kamegai and Shibata, 1988), and because mastication produces 0.5 mV to 5 mV of piezoelectricity (Cochran et al., 1967), the piezoelectricity alone should provide reasonable electric power for bone remodelling. Hard physical work must be prohibited for at least three months, i.e., until the tibial periosteum has regenerated, to protect against pathological fracture. Histopathology of Transplanted ESP A small piece of ESP from the transplant was obtained for histopathological examination with HE staining. The transplanted ESP was composed of a thickened outer layer of periosteum, and underlying proliferated, undifferentiated mesenchymal cells, osteoblasts differentiated from proliferated undifferentiated mesenchymal cells, and osteoid (Fig. 5). X-ray Examination and Clinical Findings after the ESP Transplantation Two weeks after transplantation, radio-opacity could hardly be seen in the transplanted ESP in the mandible. By five weeks after ESP grafting, however, radio-opacities were detected'in small limited areas (Fig. I a). And by ten weeks, features of calcification were evident on X-ray (Fig. 1 b). One year after the ESP transplantation, evidence of definite bone formation was clearly seen in the mesh tray (Fig. I c), but incorporation of the newly formed bone into the mandibular bone could not be seen on the X-ray film (Fig. I c). Although slight movement of the titanium mesh tray was palpable just after the ESP transplantation, a solid mandible had formed clinically one year after the ESP transplantation.
Discussion
Periosteum has the power to change into bone tissue when it is electrically stimulated. Recently, the following reports have appeared, describing experimental bone induction by electrical stimulation. Sasaki and Inoue (1988) reported that new bone tissue was found in 40 out of 44 rats (90.9 %) when rat tibial periosteum, electrically stimulated for 6 days by 8 to 10 microamps of direct current, was grafted into the rat axillary muscle. Kamegai (1986) and Kamegai and Shibata (1988) stated that the defective palatal bone region of Maccaca monkeys was filled with newly formed bone tissue one month after transplantation of periosteum that had been electrically stimulated with 20 microamps of direct current for 2 weeks; however, no bone formation was detected in the non-ESP-transplanted region. We expected that osteogenesis of ESP would be strong enough to form bone tissue even in a defective bone region after segmental resection, and that ESP would be a useful bone source for use in children. These were the reasons why ESP grafting was planned for this child. The tibia is supposed to be the best source for producing ESP, because it is long and wide, and can provide enough ESP for defective bone in any region. As the region of the cruris anterior has thin connective tissue beneath tile skin, the ESP can easily be elevated and removed surgically. Tile lower third of tile tibia should be avoided as a source of ESP, however, because it is too slender to form enough ESP. The patient complained that the left leg felt heavy .and no'tmal physical exercise was difficult. Nonetheless, five weeks of electric stinmlation of tile periosteum should be used to ensure a sufficient amount of ESP for use in tile recipient bed. Histopathologi~ily, three phases have been noted in the progression of'ESP to EC (Kanmgai et al., 1988): 1) tile first phase exhibits proliferation of undifferentiated mesenchymal cells from the inner or cambium layer, 2) tile second phase shows the change of undifferentiated me.,enchymal cells into osteoblasts, and then osteoid tissue formation, and 3) the third phase displays bone tissue formation from the osteoid structure. The ESP thus has strong osteogenic potential and tile EC is the final stage of tile ESP, that is, a very highly calcified ESP.
12
1. Cranio-Max.-Fac. Surg. 18 (1990)
The caihodes made from Kirschner wires were carfully inserted and reconfirmed radiologically to be in the correct position to stimulate the tibial periosteum. The number of cathodes had to be determined by the length and width of the bone defect, because each cathode (electrode) may make an ESP or EC of only about 1 or 2 cm in diameter (Zengo et al., 1976). In the present case, segmental resection of.the mandible resulted in a bone defect measuring 11 e~n • 2.5 cm; therefore 20 electrodes arranged in 2 rows were inserted. Any site for the electrodes is acceptable, except-for the growing area near the epiphysis in order to prevent inhibition of growth of the tibia. The anodes are applied to the skin adjacent to the cathodes, and their position must be changed at least every three days. Otherwise the anode will induce a bulla on the skin just beneath the point of application if it remains on the same skin site too long. The current was measured and readjusted at least every two or three days to maintain 20 microamps, in vivo, continuously since depolarization decreases the current (Brighton et al., 1975). Yasuda et al. (1955) reported that a reasonable out-put for EC formation was within the range from 1 microamp, to 100 microamps, of direct current; below 1 microamp, no bone forms, over 100 microamps. cartilaginous callus appeurs, and more than 1000 microamps, causes bone destruction. Direct current electrical stimulation has been in clinical use for the treatment of nonunions and pseudarthroses of the long bones (Lavin et al., 1977; Brighton et al., 1981), and animal studies have suggested its potential for increasing healing rates of a mandibular fracture (Zengo et al., 1976; Masureik and Eriksson, 1977; Shandler et al., 1979). The application of 3 to 5 microamps, produced bone growth in the vicinity of mandibular drill holes in dogs (Zengo et al., 1976). Slot osteotomies in the dog mandible healed faster following stimulation with 12 microamps. (Shandler et al., 1979). Mobility in jaw fractures in 40 patients has been reported to be reduced, as judged from clinical examination and periodontometer measurement, following treatment with 10 to 20 microamps. (Masureik and Eriksson, 1977). The ESP is stripped from the tibia by chisel using ordinary hand pressure. The outside layer of the ESP is chiefly composed of osteoprogenitor cells that have marked osteogenic propensity (Kamegai, 1986; Kamegai and Shibata, 1988; Sasaki and Inoue, 1988) like the inner layer of the periosteum (Burman and Umansky, 1930; Haldeman, 1933); therefore the outer surface of the ESP should be removed as gently as possible. The titanium mesh tray was used as both a space maintainer and container, because the ESP itself is not calcified enough to maintain the shape o f the mandibular arch. The titanium mesh tray can be removed when definable bone formation is identified radiologically. From our follow-up study both with X-rays and clinical observation of this case, it appears that the procedure could be improved by the use of double or triple overlapping layers of ESP in order to produce a thicker and more solid mandible for psoper function. Conclusions From the present case, ESP transplantation certainly formed identifiable bone as judged by X-ray examination. ESP grafting seems to be a useful method for mandibular
Akihide Kamegai et al. reconstruction in the y o u n g patient who does not have 9enough donor bone for transplantation. References Adekeye, F~0., K. Nigeria: Reconstruction of mandibular defects by autogenous bone grafts: a review of 37 cases. J. Oral Surg. 36 (1978) 125 Basset, C. A. L, IL J. Pawluk, tL 0. Becker: Effect of electric current on bone in vivo. Nature 204 (1964) 652 Bear, S. ~, ILK. Green, W. W. Wentz: Stainless steel wire mesh - an aid in difficult oral surgery problems. J. Oral Surg. 29 (1971) 27 Bear, S. E., F. Chairsell, L Cuttino, IL L Ewing: Experimental use of stainless steel wire mesh in mandibular defects. J. Oral Surg. 31 (1973) 348 Boyne, P. J.: The restoration of resected mandibles in children without the use of bone grafts. Head Neck Surg. 6 (1983) 626 Bradley, P. F.: A two-stage procedure for reimplantation of autogenous freeze-treated mandibular bone. J. Oral Maxillofac. Surg. 40 (1982) 278 Brighton, C. T., A. Steven, B. J. Black, N. Itada, Z. B. Friedenberg: Cathodic oxygen consumption and electrically induced osteogenesis. Clin. Orthopaed. Rel. Res. 107 (1975) 277 Brighton, C. T., Z. B. Friedenberg, L M. Zemsky, P. R. Pollis: Direct current stimulation of nonunion and congenital pseudoarthrosis. J. Bone Joint Surg. 57 A (1975) 368 Brighton, C. T., J. Black, Z. B. Friedenberg, J. L Esterhall, L J. Day, J. F. Connolly: A multicenter study of the treatment of nonunion with constant direct current. J. Bone Joint Surg. 63 A (1981) 2 Burnmn, M. S., M. Umansky: An experimental study of free periosteal transplants, wrapped around tendon. J. Bone Joint Surg. 12 (1930) 579 Cochran, G. V. B., R. J. Pawluk, C. A. L. Bassett: Stress generated electric potentials in the mandible and teeth. Arch. Oral Biol. 12 (1967) 917 Crockford, D. A., J. M. Converse: The ilium as a source of bone grafts in children. Plast. Reconstr. Surg. S0 (1972) 270 Cuono, C. B., S. Ariyan: Immediate reconstruction of a mandibular defect with a regional osteomusculocutaneous flap. Plast. Reconstr. Surg. 65 (1980) 477 Friedenberg, 7_, B., M. C. Harlow, C. T. Brighton: Healing of nonunion of the medial malleolus by means of direct current. A case report. J. Trauma 11 (1971) 883 Green, M. F., J. R. Gibson, J. R. Bryson, E. Thomson: A one-stage correction of mandibular defects using a split sternum pectoralis major osteo-musculocutaneous transfer. British J. plast. Surg. 34 (1981) 11 Harben, G. W., D. A. Corgill: Chrome cobalt mesh mandibular prosthesis. J. Oral Surg. 27 (1969) 5 Haldenmn, K. 0.: The influence of periosteum on the survival of bone grafts. J. Bone Joint Surg. 15 (1933) 302 Kamegai, A.: An experimental study on boneless bone grafting for the maxillary bone defect region using the electrically stimulated periosteum. Jpn. J. Oral Maxillofac. Surg. 32 (1986) 2220 Kamegai, A,, K. Sbibata: Knochenlose Knochentransplantation d~ch elektrisch stimuliertes Periost. VorKiufiger Bericht und klinische Anwendung. Dtsch. Zahn~irztl. Z. 43 (1988) 26 Kamegai, A,, Y. Muranmts~6 Y. Matuoka, K. Sbibata, S. lnoue: Autoradiographic study for calcium detection on the process of electric callus formation. JJBERS 2 (1988) 73 Lavine, L S.,,~ Lustrin, M. H. Shamos: Experimental model for studying the effect of electric current on bone in vivo. Nature 224 (1969) 1112 Lavi,m, L S., I. Lustrin, M. H. Sbamos, IL A. Ri~mldi, A. tL Liboff: Electric enhancement of bone healing. Science 17S (1972) 1118 9Lavine, L S., I. Lustrin, M. H. Shamos: Treatment of congenital pseudoarthrosis of the tibia with constant direct current. Clin. Orthop. 124 (1977) 69 Masureik, C., C. Eriksson: Preliminary clinical evaluation of the effect of small electrical currents on the healing of jaw fractures. Clin. Orthop. 24 (1977) 84
Mandibular Reconstruction Using Electrically Stimulated Periosteum Minkin, C.,'B. R. Poultotb W. H. Hoover:The effect of direct current on bone. Clin. Orthop. 57 (1968) 303 Nagamitte, T., H. Yakata, T. Nakajima: Secondary reconstruction of the mandible with an aluminum oxide prosthesis. J. Oral Maxillofac. Surg. 45 (1987) 173 New, G. B., J. B. Erich: Bone grafts to the mandible. Am. J. Surg. 63 (1944) 155 O'Connor, B. T., H. M. Cbarlton, J. D. Currey, D. R. S. Kirby, C. Woods: Effects of electric current on bone in vivo. Nature 222 (1969) 162 Persson, G., P. tk Lundgren, S. Stenstroem: Mandibular reconstruction with bone grafts. Int. J. Oral Surg. 7 (1978) 512 Sasaki, H., S. lno~te: Electrically stimulated periosteal grafting in the rat. J. Jpn. Orthop. Assoc. 62 (1988) 57 Sbandler, H. S., S. Weinsteht, L. E. Nathan: Facilitated healing of osseous lesions in the canine mandible after electrical stimulation. J. Oral Surg. 37 (1979) 782 Siemssen, S. 0., B. Kirkby, T. P. F. O'Connor: Immediate reconstruction of a resected segment of lower jaw, using a compound flap of clavicle and sternomastoid muscle. Hast. Reconstr. Surg. 61 (1978) 724
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Snyder, C. C., J. M. Bateman, G. D. Warden: Mandibulo-facial restoration with live osteocutaneous flaps. Hast. Reconstr. Surg. 45 (1970) 14 Vuillemin, T., J. Raveb, F. Sutter: Mandibular reconstruction with the Thorp condylar prosthesis after hemimandibulectomy. J. Cranio-Max.-Fac. Surg. 17 (1989) 78 Yasuda, L, K. Nogucbi, T. Sara: Dynamic callus and electric callus. J. Bone Joint Surg. 37 A (1955) 1292 Zengo, tL N., C. A. 1_, Bassett, G. Prountzos, IL J. Pawluk, A. Pilla: In vivo effects of direct current in the mandible. J. Dent. Res. 55 (1976) 383
A. Kamegai, DDS, PbD Department of Oral and Maxillofacial Surgery Asahi UniversitySchool of Dentistry 18S 1- 1 Hozumi Hozumi-cbo Motosu-gun Gift Japan