Cancellous-marrow bone grafts in irradiated tissue Robert D. Marciani, Lexington, Ky. VETERANS COLLEGE
ADMINISTRATION
D.M.D.,’
and John N. Trodahl, D.D.S.,*+
HOSPITAL
AND
UNIVERSITY
OF KENTUCKY
OF DENTISTRY
Discontinuity defects of the mandible have been successfully treated by means of cancellous-marrow grafting techniques, This method of reconstruction has not been widely reported in the repair of defects in mandibles that have been exposed to radiation therapy. In the two cases presented in this article, the patients were previously treated for oral squamous-cell carcinoma by irradiation and partial mandibulectomy. Later, cancellous-marrow grafts were implanted. One patient received 3,000 rads of Cobalt-60 and had the body of the right mandible resected. The subsequent grafting procedure was successful in this patient. The second patient received 6,000 rads of Cobalt-60 and underwent resection of the mandible anterior to the molar region. The subsequent graft failed in this case.
B
one grafts restoring discontinuity defects of the mandible challenge the skills of the oral and maxillofacial surgeon. The challenge is heightened when the graft is placed in irradiated tissue. Bone grafts are most successful when the recipient site is well vascularized, soft tissue is plentiful, and the surgical site is free of infection. Previously irradiated graft sites are often compromised both in available blood supply and in tissue integrity. In bone, absorption of large amounts of radiation may cause the death of osteoeytes, vascular disturbances, destruction of marrow, and reduction or complete loss of bone vitality. In 1926, Ewing1 interpreted the significance of the behavior of bones under external irradiation. He reported .that moderate and severe radiation reduces the vitality and growth capacity of bone cells and compromises their bone-forming
*Staff Oral Surgeon, Veterans Administration Hospital, Lexington, Ky. ; and Associate Professor, Department of Oral Surgery, University of Kentucky College of Dentistry, Lexington, Ky. **Chief, Dental Service, Veterans Administration Hospital, Lexington, Ky.; and Professor, Department of Oral Pathology, University of Kentucky College of Dentistry, Lexington, Ky.
431
432
Marciani
Oral Surg. October, 1976
and Trodahl
Fig. 1. Case 1. Preoperative mandibular body.
view
of lower
face. Loss of soft-tissue
contour
in the right
function. This effect, however, is slowly overcome if the devitalized bone remains free from infection. GowgielZ experimentally studied osteoradionecrosis of the jaws in the Macaca rhesus monkey. In his study, a 7,500-rad dose of orthovoltage to the mandible produced a fatty and acellular marrow. Artery and arteriole walls in the body of the mandible were thickened. These vascular changes uniformly involved the arterioles, whereas medium-sized and large arteries were only occasionally involved. Capillaries and veins were not affected. A sterile necrosis was found under an intact gingiva in some animals. Histologically, the periosteum had a normal appearance. In one case, periosteal bone formation was responsible for the complete regeneration of a large portion of sequestrating mandible. Gowgiel’s study indicated that the intact osteoradionecrotic mandible contained sufficient regenerative powers to overcome the deleterious effects of lower levels of irradiation if the osteoradionecrotic process could be arrested. Over-all, however, the effect of irradiation favored bone resorption rather than bone production. Graft recipient sites may be further compromised by the surgical procedure associated with the irradiation treatment. Soft tissue may be in short supply or displaced by sear contracture. Securing enough tissue to adequately develop a graft bed may not be possible. The character of the bone used for the graft is also a factor. Iliac crest and rib have been common donor sites for mandibular grafts. Traumatic defects of the mandible have been successfully restored with cancellous-marrow bone. The technique popularized by Boyne3 has advantages over the solid one-piece autografts. He has described several : (1) The particulate graft of marrow and cancellous bone is more easily obtained by making only a small opening at the iliac crest rather than taking a large portion of the ilium or a rib in order to effect the desired surgical result. (2) Complete healing of the grafted defects with viable
Catlcellous-marrow
Volume 42 Numher 4
bone grafts
Fig. 2. Case 1. Surgical splints inserted preoperatively. to
the
right.
Upper
and
lower
splints
are
keyed
to
in irradiated
tissue
433
Note the deviation of the mandible reestablish ridge alignment.
appears to be more rapid than when the solid one-piece autograft is used. (3) The duration of intcrmaxillary fixation can be greatly reduced because of the rapid spanning and osseous regeneration of the defect by new bone. In addition, support of the host bone fragments is provided by the metal implant itself. (4) Restoration of bony architecture and contour is more easily accomplished because the basic form of the regenerated bone is dictated by the metal implani itself. Boync further wrote, “In certain surgical situations, however, with large communications between the oral cavity and the skin areas in which intra-oral dehiscence is anticipated or present at the time of surgery, it is considered more prudent not to utilize the metal-type implant, but to utilize the solid one-piect autograft to effect the restoration. Intra-oral dehiscence over a metal implant may lead to total loss of the graft contained within the metal framework.” The use of this method of reconstruction has not been widely reported in the literature for managing defects in previously irradiated mandibles. The purpose of this article is to present two cases of cancellous-marrow mandibular bone grafts implanted in previously irradiated tissue. bone
CASE REPORTS CASE
1
A 54.year-old white man with a chief complaint of inability to chew was examined in the Dental Service, Veterans Administration Hospital, Lexington, Ky. Eighteen months earlier he had 1)ecn treated for squamous cell carcinoma of the right lateral tongue. Preopcrntivrly, the patient received 3,000 rads of Cobalt-60 irradiation to the tongue, mandible, and right neck, over a period of 17 days. An operation including a right hemiglossectomy, a right partial mnndibulectomy, and right radical neck dissection was performed approximat,ely 6 \ve&s after completion of the radiation therapy. He had an uneventful postoperative course, and subsequent follow-up examinations did not reveal recurrent tumor. The surgical defect srverely limited masticatory function, however, and the patient desired correction if possible. He was admitted to the hospital for work-up. Significant past medical history included tension headaches, hypertension, possible myo-
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3976
cardial infarction, and chronic prostatitis. The patient drank and smoked excessively prior to diagnosis of the malignancy. He was allergic to penicillin. Review of systems was negative, except for frequent headaches and his chief complaint. Physical examination confirmed the history of previous irradiation and operation. There was an obvious deformity of the right mandible. A discontinuity defect was npparcwt from the right, angle to the right parasymphysis region (Fig. 1). The remaining mandible was deviated to the right. The skin overlying the neck and right mandible was supple and nondiscolored, and facial hair was present. Well-healed wars in thcl right side of the nwk indicabd a radical nwk dissection. There was slight tcndrnwss to palpation in the right carotid region, and no cervical lymphadenopathy. Oral examination and indirwt laryngoscopy \vc’re negative for new or wcurrent tumor. Salivary flow was diminished. There was no mucositis. ‘Phr, patient was edentulous. The discontinuity defect of the right mandible was covered 1)s soft tissue intraorally. A prominent band of scar tissue was present in the floor of the mouth on thcl right side. The tongue had a decreased range of motion. The alveolar ridges were poorly aligned (Fig. 2). There was anesthesia and a motor deficit in the right lower lip. Thr findings of the remainder of the physical examination were unremarkable. Routine laboratory findings were within normal limits. A chest radiograph showed no active disease. The ~~lectro~:irrliogr;tm showed left ventricular hypertrophy and, possibly, an old anteroaeptal infarction. The problem list included: (1) discontinuity defect of right mandible with deviation and masticatory difficulties, (2) mild hypertension, (3) chronic prostatitis, (4) tension headaches, (5) status post-squamous cell carcinoma of right posterior tongue. A treatment plan to restore mandibular cont,inuity was devised that included an autogenous eancellous-marrow bone graft to the right mandible supported in position by a titanium mesh basket. The patient was taken to the operating room, administewd general anesthesia via a nasal endotraeheal tube, and prepared and draped in the usual manner. Prefabricated maxillary and mandibular acrylic denturr splints were positionrd with right and left circumzygomatit wires wiws in the left body and left parato secure the maxillary appliance, and circummandibular symphysis wgion to stabilize the mandibular dentow splint. The> wlationship of maxillary alveolar ridgcr to mandibular alveolar ridge, dctcrmined preoperatively, involved a repositioning of the nnmdil~le to the left. Bringing the prcfnl)ricatc~d splints into owlusion ac~~on~plial~ctl thcl rtralignmcwt, and intwmaxillary \\ircs were placed for fixation. C:rn~rllous-rrlarrolv born was obtained from thcb right hip. A skin incision was outlinctl in the right nrck in the scar of thr previous radical neck dissrction. The incision was approximately 10 cm. in length extending from the submental region curving inferiorly to thr 101rw right aspwt of the nwk and then superiorly to the mastoid region. The incision was carried through skin and sul~cutnnrous tissucl. superiorly along the The carotid artery was palpated and protected. A flap ~vas tleveloprd length of the incision in :I plane just below the platysmn rnusch~. The depth of t,hc neck dissection was determined by identifying thcx intnrnrdiate tenllon of the digastric muscle. The flap was retracted superiorly to expose thP proximal and distal segments of the right mandible. Extensive scarring was cneounterctl in all awas of the diswction. The periosteum along the lower I)order of the anterior mandible was inrisrd ant1 rrflwtcd, thcwl~y exposing the parasymphysis region. A 1~~1 was created for the bone graft l)y Iliswcting thrx scar tissue between the proximal and distal segments of thr m:~ndil)lc. The proxinml scgmmt of the mandible was located in a position superior snd anterior to its original position. Thr prriosteum ovwlying this segment was reflected, tlreret,y exposing the, ramus and coronoid process. The proximal fragment was then easily repositioned infrriorly and posteriorly and a roronoidectomy was performed. The proximal and distal segments werp aligned with the use of an acrylic stunt that, had been prefabricated on thr basis of cephalometric tracings of the left mandible (Fig. 3). The titanium mesh basket was trimmed to proper siztx and contour to allow closure of the mound without tension. The bone margins were freshened with a pear-shaped hur. Rleeding was elicited from the distal segment but not from the proximal portion. The mesh ~vas fixed to thr, mandible at each end with titanium screws. The basket was packed with canccllous-marrow hone from the donor sit,e (Fig. 4). The posterior inferior aspect of the proximal segment was reduced to improve the configuration of the angle. The, wound wns closed in layers. The titanium mesh was completely covered by the tissues of the created bed. Neither mesh, anterior
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Fig. 3. Case 1. Proximal and distal fragments exposed. Angle of the mandible is on the left. Fig. 4. Case 1. Titanium mesh basket attached to mandible fragments. Basket has been packed with cancellous-marrow bone.
bone, nor posterior bone was visible after the deep closure. Dead space was carefully obliterated. Drains were not placed. After superficial closure, a pressure bandage was applied. The patient tolerated the operation and the general anesthetic well. Five days postoperatively a slight swelling was evident at the inferior margin of the neck wound. When the sutures were removed on the eighth postoperative day, the wound was noted to be breaking down at the most inexudate was ferior port,ion of the incision and in the submental region. A serosanguineous expressed at these sites. Exploration of the drainage areas indicated breakdown of the wound to some extent under the flap, and dead space was noted at a position inferior t,o the mesh and bone graft. The dead space was obliterated with lh-inch iodoform gauze. Aerobic and anaerobic cultures of the exudate were subjeet,ed to microbiological review. No growth was reported. The drainage sites were irrigated and packed daily with iodoform gauze for approximately 1 month. The dead space under the flap gradually became smaller and finally closed completely. Intermaxillary fixation was maintained for 6 weeks. Circummandibular and circumzygomatic fixations were removed during the eighth postoperative week. There was firm union at the graft site. The oral mucosa was int,act and no mesh was visible in the mouth or extraorally. Eighteen months after graft placement, t,he mrsh was weI1 toleratcXd by the tisPml and there was no evidence of tissue breakdown. Postoperaively, the paient used the splints as interim denures until a permanent prosthesis could be constructed. The prosthodontist extended the mandibular denture only to the parasymphysis area on the surgical side. Loss of sensation and function of the right lower lip caused entrapment of the lip between the denures. The patient wore both a maxillary and a mandibular prosthesis primarily for cosmetic reasons (Figs. 5 and 6). He reported improved masticatory efficiency, however, with just the mandibular denture. CASE 2
A 63-year-old white man was presented to the Tumor Board at the Veterans Administration Hospital, Lexington, Ky., in August, 1974, for evaluation of a sever? facial deformity. In 1965,, a squamous cell carcinoma of the floor of the mouth on the right side was treated by surgical resection. In 1967, the lesion recurred and was treated with radiotherapy (6,000 rads in 6 weeks with the use of a 6-by-g-cm. field to the floor of the mouth on the right side). Jn February, 1972, t,he patient was treated elsewhere for squamous ccl1 carcinoma involving the anterior floor
436
Mamia~wi md Trodahl
Fig. 5. Case 1. Postoperative tissue support enhanced.
Oral Surg. October, 1976
view of lower face. Right, mandibular
E’ig. 6. Case 1. Frontal postoperative view. Note paralysis dible is undercontoured compared to left side.
of right
contour
improved.
Soft-
lower lip. Right
man-
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Cancellous-marrow
Fig. ‘/. Case 2. Preoperative
bone grafts in irradiated
view of facial
tissue
437
deformity.
of the mouth and mandible. Resection of the anterior door of the mouth, partial mandibulectomy, and bilateral suprahyoid neck dissection were performed at that time, An attempt at immediate reconstruction with a titanium mesh prosthesis failed and the prosthesis was removed in May, 1972. Subsequently, a split-thickness skin graft was placed over the anterior mandibular mucobuccal fold and the lower lip. In August, 1973, the patient presented for admission at the Veterans Administration Hospital, Lexington. His chief complaint was his facial deformity and constant drooling (Fig. 7). Because he was unable to care for himself, admission as an intermediate-care patient was suggested by the social service. The patient was subsequently presented to the Tumor Board three times for evaluation of his facial deformity. The oral surgery section evaluated the patient and judged him to be a poor candidate for further reconstructive surgery. This opinion was prompted by: (1) the previous 6,000 rads of cobalt irradiation to the area, (2) failure of the original titanium mesh implant, (3) poor graft bed in the anterior floor of the mouth, and (4) patient’s unreliable social and psychiatric history. The Oral Surgery Service recommended that no further reconstruction be attempted. Further psychiatric evaluation of the patient strongly implied that rehabilitation and social adjustment were largely dependent on improvement of facial cosmetics and mandibular function. Despite the likelihood of graft failure, the Tumor Board recommended that another attempt be made to improve the appearance and function of the patient. He was transferred to the Oral Surgery Service for the reconstructive procedure. The patient’s medical history indicated that he had had no operations other than his mandibular surgery, that he was free of major illnesses, but that he did have psychiatric problems. He had no complaints other than his drooling and inability to masticate food properly. He had smoked two packs of cigarettes per day for 50 years and had used ethanol frequently for many years. Physical findings included absence of the anterior mandible bilaterally back to the molar region. The proximal mandibular remnants were displaced superiorly, touching the maxillary tuberosities (Fig. 8). There was an inadequate lip seal, and saliva ran freely from the mouth. A well-healed skin graft covered the inner lower lip and extended to
438
Mamimi
Oral Burg. October, 1976
and l’rodahl
Pig. maxillary
8. Case 2. Displaced tuberosities.
Fig. restored.
9. Case 2. Titanium
right
and left
mesh basket
mandibular
in place.
proximal
The anterior
fragments
mandible
contacting
the
and body region
the anterior floor of the mouth. There was a small bone-exposing ulceration in the mucosa overlying the left proximal fragment. No new or recurrent tumor was apparent, and there was no cervical lymphadenopathy. Multiple spider nevi were found on the skin. Routine laboratory studies were negative. The electrocardiogram and routine chest radiographs were unremarkable. The patient’s problem list included: (1) facial deformity, (2) depression, (3) ethanolism, (4) status post-squamous cell carcinoma of the anterior floor of the mouth. A treatment plan to restore facial contour was developed. A cancellous-marrow graft supported by a titanium mesh basket would be used to reposition the displaced proximal fragments and improve the anterior facial contour. The patient was taken to the operating room, intubated nasally, and prepared and draped in the usual manner. Cancellous-marrow bone was obtained from the left iliac crest. An incision was made from 1 cm. below the right ear lobe anteriorly across the midline to the mandibular
Volume 42 Number 4
20. Case 2. Six weeks postoperatively. visible.
Fig.
graft
Callcellolls-?,zarrow
belle grafts in irradiated
Titanium
mesh eroding
through
tissue
439
lip. Necrotic
angle area of the opposite side. Sharp dissection carried the incision through the fibers of the platysma muscle, and a flap was developed superiorly deep to that muscle, with coincident identification of landmark anatomy. The proximal fragments of the mandible were identified and an incision was made through the periosteum in the inferior border of each angle. The pterygomasseteric sling was reflected off the bone and the temporalis insertion was freed from the anterior border of the asernding ramus. Coronoidectomies were accomplished bilaterally and t,he proximal fragments were moved inferiorly. The titanium mesh basket splint was fitted to the proximal fragments (Fig. 9). This metallic replacement was undercontoured in order to facilitate softtissue closure without tension. Once contoured, the mesh was fixed to the re mnining mandible with titanium screws and packed with cancellous-marrow bone from the donor site. The wound was closed in la.yers. Periosteum was available to cover the mesh only in the proximal portions of the graft. Anteriorly, the mesh was covered by fibrous scar tissue. Hemovac drains were placed bilaterally through separate stab incisions made below the incision line. Oral examination indicated a small mucosal tear in the left ramus. A 4-O chromic suture was placed in order to close the tear. The patient tolerated the operation and the general nnrsthetic well. Two weeks postoperatively, a 2-cm. area of exposed graft and mesh developed intraorally. Extraorally, the wound appeared to be well healed. The intraoral wound dehiscence was treated with daily irrigations. Six weeks postoperatively, however, the skin in the mental region broke down (Fig. 10) and the titanium mesh was also visible extraorally. Treating the intraoral and extraoral wounds with irrigation and iodoform gauze packing was to no avail and both dehiscences became steadily larger. Eight weeks postoperatively, the exposed portion of the graft was removed, along with the necrotic marrow. Additional portions of mesh and marrow were periodically removed during the next few weeks, and the anterior section of the graft was completely lost. Treatment was then directed toward the healing of tissues t,hat overlay the remaining proximal portions of the mesh and graft.
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and Trodnhl
Oral 8ury. October, 1976
prowdwe, Three months after the gmft a suspicious-looking PrythemRtou~ :uea of the right tonsillar pillar was detected. The lesion measured approximately 13 mm. An incisional biopsy spceimcn WIS taken, and a diagnosis of infiltrating, moderately differentiated squamous cell carcinoma was returned. The Tumor Hoard recommended surgical excision of the lesion. Definitive operation did not totnlly remove the tumor, however, and the lesion was subse. quently treated with 7,000 rads of cobalt irradiation by means of bilateral opposing tields. Fifteen months :tfter the graft operation, the patient was free of tumor. The interim course of irradiation therapy further complicated healing of soft tissue at, the graft site. All of the titanium mesh was removed. The proximal fragments of the mandible returned to their pro opomtivn malposrd position. The patient has ~~ontjnueti to drool.
DISCUSSION Studies of osteoradionecrosis of the jaws and the effects of irradiation on bone growth and repair clearly indicate an unfavorable environment for successful bone grafting in irradiated tissue. Bone resorption appears to predominate over hone formation, thus creating an environment that is conductive to infection and sequestration. In addition, heavily irradiated skin and oral mucosa have an increased fragility and susceptibility to tlehiscencc! and repair of all soft, tissues is inhibited. The use of rib grafts arltl block iliar: crest grafts to restore defcct,s in previously irradiated mandibles has the disadvantage of inherent nonviability of the graft material. A grafting technique that relics less on the recipient tissues for reconstitution would appear to have an improved chance of success. The titanium mesh cancellous-marrow system offers the advant.agca of greater viability, as previously outlined by Boync. Also, rrc,orlstmr.tioll of large mandibular defects can he effeetcd with the use of a relatively small amount of graft material. The restored defect is composed primarily of richly cellular, viable bone with a minimum of noncontributive calcified matrix. Thcrcfore, the graft is less dependent on adjacent tissue for bone production. Successful reconstruction of the previously irradiated resected mandible depends on a number of factors : (I ) the dosage level of irradiation delivered to the tissues, (2) the response to irradiation of the individual patient’s tissue, (3) the character of the soft-tissue surgical tlcfcct, (4) the size of the hard-tissue surgical defect, and ( fi) anatomic relationships of the discontinuous mandibular segments with each other and the maxilla. Our cases provide examples of those variables. The patient in Cast: 1 reccivccl 3,000 ratls of cobalt irradiation. There was considerable scarring in the floor of the mouth, b.ut ample soft tissue to cover the graft. The hard-tissue resection left the mandibular angle and the parasymphysis intact,. The remaining InandiIAc was freely movable. Ridge alignment could be easily achieved prcopcrativcly by manipulation of the remaining mandible without significant forw. The interarch relationship was acceptable. The skin of the neck was supple and showed little evidence of the earlier irradiation. Hair growth was plentiful and there was no pigmentation. In Case 2, the tissues had received considerably more irradiation. The viability of the remaining soft, t.issuc was sc~ercly compromised. Much of the floor of the anterior mouth and remaining lip were covered by split-thickness skin. The entire anterior mandible had been previously resected. (Cancellous-marrow grafts
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Numl,er 4
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tissue
441
in nonirradiated tissue have been reported to have their highest failure rate in the anterior mandible.‘) The proximal fragments of the mandible mere scarred into a superior-anterior position. There was a small mucosal tear preoperatively that exposed the underlying bone to the oral environment. The oral mucosa was inflamed. The skin in the submental and submandibular areas was dry and hairless. The recipient tissue in this case was severely compromised in every respect, so that there was little chance of success. Our experience in Case 2 also underlines the importance of continued vigilance for detecting new or recurrent tumor. Careful preoperative examination had obviated any stigmata apparent at that time. Three months later, however, a suspicious-looking erythematous area was noticed and a third primary carcinoma was documented. SUMMARY
Two cases of mandibular cancellous-marrow bone grafts in irradiated tissue have been reported. The advantages and disadvantages of the titanium mesh system have been reviewed, and factors that contribute to graft failure have been discussed. REFERENCES
1. Ewing, J.: Radiation Osteitis, Acta Radiol. 6: 399-412, 1926. 2. Gowgiel, J. M.: Experimental Radio-Osteonecrosis of the Jaws, J. Dent. Res. 39: 176-196, 1960. 3. Iioynr, P. J. : Transplantation, Implantation and Grafts, chapter in Goldman, H. M., et al. : Current Therapy in Dentistry, St. Louis, 1970, The C. V. Mosby Company, vol. 4, pp. 320. 326. 4. Connole P. W.: Mandibular Cancellous Bone Grafts: Discussion of 25 Cases, J. Oral Surg. 32: 745-754, 1974. Reprint requests to : Dr. Robert D. Marciani Department of Oral Surgery University of Kentucky College of Dentistry Lexington, Ky. 40506