Bone Grafts in Surgery of the Face

Bone Grafts in Surgery of the Face JOHN MARQUIS CONVERSE, M.D. * ROSS M. CAMPBELL, M.D. **

extent of osseous displacement, loss or maldevelopment, and the resultant deformity due to defects of the bones of the facial skeleton vary in degree and according to the region of the face affected. Depression of the frontal area and of the supra-orbital arches or loss of a segment of the frontal bone; flattening of the side of the face in the area of the zygoma; depression of the floor of the orbit which may be complicated by ptosis of the orbital contents; deformities of the nose, occasionally affecting associated structures and resulting in nasomaxillary deformity; mandibular deformities-any of these conditions may require restoration of normal contour by an implant or graft. Various types of grafts and implants have been employed for facial contour restoration: autogenous cartilage, preserved homogenous and heterogenous cartilage, foreign materials such as tantalum, the acrylics or polyethylene. Fresh autogenous cartilage tends to curl. Homogenous or heterogenous cartilage may initiate an inflammatory reaction violent enough to cause early rejection by the tissues; such grafts are progressively absorbed in a high proportion of cases (North, 1 Gibson and Davis, 2 Schofield3). Although the so-called inert foreign materials may be tolerated by the tissues for a variable period of time, when implanted in areas of functional stress, subjected to muscular movements or to trauma, they are often extruded because of tissue irritation around the implant; the rejected implant leaves behind it a bed of dense fibrou.s tissue, complicating further reconstructive procedures. In addition, all THE

From the Plastic Surgery Unit, Department of Surgery, N ew York University College of Medicine and the Third Surgical Division, Bellevue Hospital, and the Plastic Surgery Clinic, Manhattan Eye, Ear and Throat Hospital, New York City.

* Associate Professor of Clinical Surgery (Plastic Surgery), New York University College of Medicine; Visiting Surgeon, Bellevue Hospital; Surgeon-Director, Plastic Surgery Clinic, Manhattan Eye, Ear and Throat Hospital.

** Clinical Instructor in Surgery (Plastic Surgery), N ew York University College of Medicine; Assistant Visiting Surgeon, Bellevue Hospital; Assistant Attending Surgeon, Plastic Surgery Clinic, Manhattan Eye, Ear and Throat Hospital. 375

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of these implants, including cartilage, are subjected to the pull of the surrounding soft tissue scar in the course of healing and are apt to be twisted or rotated from their original position during the weeks following their implantation. Bone grafts, when placed in contact with living bone; cause no tissue reaction. They rapidly consolidate with the host bone :and incorporate into the bony framework of the face, so much so that in subsequent roentgenographic examination it is difficult to differentiate the bone graft from the bony framework. Bone grafting is contraindicated only if contact between the bone graft and living bone cannot be achieved. The purpose of this paper is to emphasize the use of bone grafts in preference to other implants in the repair of bone defects, for bone grafts become an integral part of the facial skeleton. HISTORY OF BONE TRANSPLANTATION

Interest in the regeneration of bone was aroused during the eighteenth century and bone transplantation was first attempted during the nineteenth century. The history of early observations and experimentation in this field has been told by Keith.4 Opinion regarding the growth and reproduction of bone was divided between those who, with Duhamel,5 Syme 6 and Ollier,1 regarded the periosteum as the chief osteogenic element of the human skeleton, the "maternal membrane of bone," to use Ollier's term, and those who, with Goodsif6 and Macewen,9 regarded the osteoblasts of the graft as the source of osteogenesis; for Macewen the periosteum was a mere "limiting membrane." Ollier had demonstrated the osteogenic power of detached fragments of periosteum in animals and concluded from observations made in experimental fractures that the periosteum is the chief agent in forming the callus, that the marrow plays a lesser role in the process, and that the bone itself is the least factor in callus formation. In 1878 Macewen removed the entire humeral diaphysis of a 3 year old boy in a case of osteomyelitis, restoring the shaft of the humerus with wedges devoid of periosteum, which he obtained in the course of tibial osteotomies performed on other patients; he reported this first recorded example of the clinical use of homogenous bone grafting in 1881. Macewen performed a series of operations on animals and published his results in 1912, thirty years after he had begun to use fragments of . bone as grafts. The contention of Macewen that the osteoblasts of a graft are the source of osteogenesis was criticized when it became apparent that new bone formation could not be considered the attribute of osteoblasts alone. Barth/o as early as 1893, concluded from carefully conducted experiments that all elements of transplanted bone die, and are slowly replaced from adjacent bone producing tissue. Galliell performed a series of experiments on dogs, using a wedge of bone from the radius replaced in its original site, to study autogenous grafts, boiling the wedge before replacing it, covering the wedge graft with tinfoil on one of its cut surfaces, and replacing the wedge taken from the dog's radius by one removed from a cat. He concluded that a bone graft merely supplies a medium for the invasion of bone cells from the host; Phemister12 called this process "creeping substitution." It appeared difficult, however, to explain the rapidity of reproduction of bone in large grafts if the source of the new bone was limited to host bone alone. If Macewen's homogenous osteotomy wedges had merely served as

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scaffolding for the living bone of the distant extremities of his patient's humerus, could the shaft of the bone have been reproduced in the short time which had elapsed? An answer to this question was given by Leriche and Policard:13 a graft can be the seat of osteogenesis only if it is in contact with pre-existing bony tissue furnishing a high local calcium supply, causing a metaplasia of the surrounding young connective tissue; osteoblasts are seen only after pre-osseous tissue appears in the graft. In addition, when one observes heterotopic ossification it would seem that survival of osteoblasts plays a minor role in regeneration, for bone appears in areas such as nerves and arteries where osteoblasts are not found. On the assumption that a bone graft serves merely as a framework to guide new bone originating from the host, Gallie and Robertson14 used boiled bone; in their experiments, however, they obtained a lower percentage of success than with autogenous bone grafts. Orell16 reported the use of "os purum," or bone from which the organic elements had been removed chemically. His findings seemed to indicate that slow revascularization and revitalization was due to the difficulty of resorbing and removing the coagulated cellular elements in the bony canals; it appeared also that the removal of the organic elements had eliminated the stimulus for osteogenesis. To explain the stimulus which results in the invasion of the framework of the bone graft by new cells, attempts were made to demonstrate an "organizing" substance in the graft, responsible for osteogenesis. After Robison's16 discovery of phosphatase in 1923, it was predicated by some that phosphatase was directly related to ossification. Huggins17 showed, in dogs, that bone forms from connective tissue in the presence of growing bladder epithelium which contains large quantities of phosphatase. The present generally accepted belief is that the role of alkaline phosphatase causes precipitation of calcium salts by the increase of phosphate ions. Levander18 succeeded in producing new bone in rabbits by the injection into muscle of alcoholic extract of normal bone or of callus. Annersten,19 also working with rabbits, obtained formation of cartilage and bone in 1 of every 13 cases by the intramuscular injection of an alcoholic extract of bone or of callus. Annersten also obtained formation of cartilage and bone in a proportion of 1 in 13 by injecting alcoholic extracts of tendon; when extracts of muscle were injected, the proportion was slightly less-l in 16. The results of Heinen's2o alcohol-injection experiments seem to throw doubts upon the importance of these findings; Heinen produced bone in rabbit muscle by the injection of alcohol alone. Despite the fact that the problem of osteogenesis is complicated by heterotopic ossification, there seem to be grounds for the belief that bone grafts which remain unadulterated by chemical or physical influence contain an enzyme-like bone-promoting substance for which Lacroix21 suggested the name "osteogenin." Lacroix demonstrated that a fragment of tibial bone, maintained for 13 days in alcohol and inserted beneath the kidney capsule of the rabbit, was undergoing resorption when examined three to seven months later, but that there was also an accompanying osteoblastic activity in a layer of newly formed bone. Upon repeating the experiment, using bone boiled for 10 minutes in water, the bone was found practically intact seven months later, with little osteoblastic activity and no new bone formation; it would thus seem that the capacity for osteogenic activity is destroyed by the process of boiling. Whether the stimulus for osteogenesis in such experiments originates from a growth-promoting substance or from survival of osteoblasts or by both of these factors remains questionable. That the ingrowing connective tissue cells of the host are induced to form bone . by contact with the substance of the transplanted tissue seems more probable. Rather than limiting the activity to the usual invasion of the transplant, the

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cells seem to acquire a potency to form bone; Urist and McLeanS! have termed this phenomenon, "bone formation by induction." There has been a tendency in recent years to attach little clinical importance to OIlier's original observations of the osteogenic properties of the periosteum. Baentzner,23 Bull,24 Levander,20 Pollock and Henderson26 denied any osteogenic power to transplanted adult periosteum. The question that also arose was whether periosteum was osteogenic only if bone particles were attached to its undersurface. The fact that osteoblasts in the deepest stratum of the periosteum of growing animals were osteogenic, was observed by OIlier as far back as 1858; his critics had alleged that he detached fragments of bony matter with the periosteum. He studied the periosteum and observed a gradual transition of structure from the superficial to the deep surface; the deepest stratum was more cellular, and oteoblasts were observed near the bone. Bonome27 contended that transplanted periosteum maintains its osteogenic properties even though, as he believed, the cells of the bone graft died. Levander concluded from his experiments that the deep or cambial layer of the periosteum is osteogenic in growing animals, but that in older animals it tends to disappear, thus reducing the osteogenic properties of the periosteum. Kolodny28 and Reiss29 had reached similar conclusions. Bisgard30 grafted periosteum alone, and periosteum and bone together, into the anterior chamber of the eyes of rabbits. New bone formation occurred in both implants but was more abundant in the grafts of periosteum and bone. Lacroix21 grafted adult tibial periosteum beneath the qapsule of the kidney in rabbits, and obtained new bone formation. He noted that the periosteal implant contained neither the cambial layer, characteristic of young periosteum, nor bone fragments, and that bone proliferation occurred only on the undersurface of the implant. This osteogenic potency of periosteum would seem to offer an explanation of the spontaneous regeneration of resected segments of bone observed by Byme,6 Ollier,7 White31 and subsequently by other surgeons (Kazanjian32). Byrne resected a segment of the radius of both right and left legs in a young dog; on the right side he also removed the periosteum; on the left, he preserved the membrane. Following sacrifice of the animal at the end of six weeks, examination showed that the missing part of the left radius had been replaced; on the right, where the periosteum had not been preserved, a gap still remained. Bertelsen33 reported that bone or cartilage was formed in 4 of 12 rabbits in which he had injected an alcoholic extract of periosteum intramuscularly. That bone-forming properties of adult periosteum can be activated before transplantation by fracture of the underlying cortex has recently been demonstrated by Urist and McLean. 22 Recent studies (Wilson;34 Reynolds and Oliver;86 Reynolds, Oliver and Ramsey36) seem to indicate that the major portion of the cells of the bone graft die. Barth,t° in 1893, had stated that the cellular elements of the bone graft die; in 1908,37 however, he admitted that fresh autogenous bone grafts were capable of active new bone formation. Axhausen,38 Mayer and Wehner,39 Haas,40 Brooks,u Phemister,12 Rhode,42 Mowlem,43 Abbott et a1.," Ham and Gordon,45 Urist and McLean,S! all expressed the opinion that osteogenic cells survive in fresh bone autografts. Ham and Gordon showed that cancellous chips form new bone when transplanted into muscle, but that no new bone forms around chips which had been frozen and thawed three times. According to their interpretation, this was due to the destruction of the osteoblasts. Campbe1l46 and his co-workers have shown that in onlay split-rib bone grafts, union of the cancellous portion of the graft to the host bed occurred in specimens which were removed two weeks after transplantation. They attributed this rapid union to the survival of os-

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teogenic cells in the graft. It is possible that the cells of the Haversian canals, endosteum or periosteum may survive in bone grafts, for it has been shown that when an explant of embryonic bony tissue is placed in tissue culture, the cells of the Haversian canals or of the endosteum are seen to grow; these facts were established by Fell,47 Gaillard48 and Judet and Delaunay.49 Heinen 50 successfully transplanted the outgrowth from tissue cultures of bone into the antQrior chamber of the eye. Pfeiffer 51 transplanted samples of autogenous bone marrow with attached bone spicules or endosteum into the anterior chamber of the eye in mice, and obtained new bone formation; only the reticular cells survived, and these were assumed to have the inate capacity to differentiate into osteoblasts. There would thus seem to be considerable circumstantial evidence in favor of osteogenic cell survival in fresh autogenous bone grafts. Growth on culture media has been limited to embryonic bone; an answer concerning the survival of osteoblasts awaits the successful culture of adult bone.

In reviewing the history of research concerned with the factors influencing osteogenesis and bone grafting, it is interesting to note that all the findings of early workers were at least correct in part. It has been shown that periosteum has osteogenic activity, as contended by Ollier; it is probable that osteoblasts survive under certain conditions, as Macewen maintained, and that the majority of bone graft cells die and are replaced by new cells, as originally observed by Barth. A number of conclusions which have practical clinical applications may be drawn from these studies. (1) The cells of the host are induced to form bone by contact with the substance of the transplanted tissue, which may contain an "organizer," or osteogenin, stimulating bone growth; it is therefore important to avoid physical or chemical injury of the bone graft, to preserve this property. In addition, the soft tissues surrounding the transplant must be healthy and well vascularized, and capable of generating new osteogenic cells and capillaries. (2) The survival of osteoblasts within the graft furnishes new centers of osteogenesis for its cellular repopulation. The graft, therefore, need not rely entirely upon metaplastic cells from the surrounding connective tissue nor upon cells from the host bone. Cancellous bone presents an extensive endosteal surface and numerous accompanying spaces which permit the extracellular fluid to permeate the graft, nourishing the cells until the ingrowth of capillaries assures the blood supply. Wide channels in the cancellous bone graft facilitate the penetration of new blood vessels and the accommodation of new bone. (3) Consolidation between grafted and host bone appears essential for permanent survival of the graft; immobilization of the graft against the host bone and the absence of dead space are necessary to prevent injury of the young connective tissue growing into the transplant. Cellular invasion from the host bone reaches its maximal activity only when the surface of contact is wide and the adjustment precise, even though it is not essential nor even possible in surgery of the face to achieve the cabinet worker's precision advocated by Albee. 52

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John Marquis Converse, Ross M. Campbell DEVELOPMENT OF THE BONE BANK

The possibility of using homogenous bone for grafting led to the preservation and storage of bone. Methods of preservation of tissues have been known since the work of Bert 53 and Carrel. 54 Inclan,55 Bush 56 and Wilson34 used refrigeration as a means of preservation; deep freeze storage is now commonly used for preserving large quantities of bone removed in the course of operations, from amputated limbs or from recently deceased cadavers. Kreuz et al. 57 prepared bone grafts by freeze-drying for indefinite preservation and greater ease in transportation. Bone heterografts from horses, calves and pigs have also been used to simplify the problem of a ready and adequate supply of available bone (Judet et al. 58 ). Even now, years after the first reports of the use of refrigerated bone, it is still difficult to make an accurate assessment of the relative merits of fresh autogenous and preserved homogenous bone. Early reports of the use of bone banks, and histologic studies of the comparative healing of autogenous and homogenous bone grafts, seemed to indicate a slower initial healing process and a lesser cellular activity in homografts; after a period varying from ten to twelve weeks, however, the microscopic picture of autografts and homografts presented a similar appearance (Wilson;34 Reynolds and Oliver35). More recent studies seem to indicate a higher percentage of growth in autogenous bone than in preserved homogenous bone. Haas reported that only autogenous bone showed evidences of healing following the transplantation of fractured bone into muscle. Mosiman,59 employing a number of different bone implants in the anterior chamber of the eyes of guinea pigs, used autogenous fragments from the fibula, and also acetone fixed, deep frozen, boiled and merthiolate preserved bone. Ninety-three per cent of the fresh autogenous bone grafts showed evidences of bone growth two weeks after implantation, whereas the implants of dead bone showed no growth. Bosworth et al.,60 in spinal fusion operations for tuberculosis, noted a nonconsolidation rate three times higher in cases grafted with refrigerated homogenous bone than in those which were autografted. Reynolds,61 in discussing these findings, stated that the use of homogenous bone had been discontinued in spinal fusion cases in his clinic, except those in which the removal of autogenous bone was not indicated. Campbell et al.,46 in experiments using split-rib grafts in dogs, found osteogenic activity only in fresh autogenous grafts. Ray et al. 62 found that fragments of embryonic bone which were frozen at -18 0 C. for twenty-four hours, and then transplanted to the anterior chamber of the eye of adult rats, showed endochondral ossification; all instances of autogenous adult cancellous and cortical bone treated similarly failed to survive. Kiehn et al.,63 studying the vascularization of experimental bone grafts by means of radioactive phosphorous, found that autogenous bone showed a higher degree of penetration of p32 than homogenous bone. Concomitant studies of the vascularization of bone fragments placed in an Algyre chamber showed a more rapid vascularization of autogenous bone. Roth, 64 following bone homografting, observed a rise in the number of circulating eosinophils, which also seems to occur following skin homografts (Rogers et al. 65). This phenomenon suggests the possibility of the failure of homografts on a basis of tissue incompatibility and immunity. In evaluating the respective merits of autogenous and homogenous bone, the advantages of the bone bank for reconstructive surgery of extensive defects of the extremities and of various orthopedic conditions is

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obvious, for a sufficient amount of bone is thus made available; in addition, secondary defects, and surgical shock due to removal of bone from donor areas, are avoided. The choice of autogenous or homogenous bone depends largely on the type of surgical repair. Bone grafting to bridge a gap between two ends of bone differs from the application of the onlay bone graft to restore contour deformity or to consolidate a nonunited fracture. In the latter instance, the wide bony surface of contact enables the success of grafts, even when such substances as boiled cadaver bone (Lloyd-Roberts66 ) or heterografts (Judet et al.58) are used. Judet and his co-workers, basing their opinion upon a series of 160 cases of heterografts in humans, feel that heterografts should be used only when a wide surface of contact can be obtained with the host bone. There is a rising opinion which favors the use of fresh autogenous bone grafts rather than other types of grafts. The substitution process in bone grafts is progressive but occurs with gradually subsiding impetus; the more rapid the fixation of the graft, the earlier its vascularization and cellular replacement. W atson-J ones, 67 in· expressing his preference for fresh autografts, stated that he favored a graft with bone cells which would "fight for him." A recent extensive survey of 3104 homografts by Frantz, Reynolds and Lipscomb 68 concludes that bank bone cannot entirely replace autogenous bone for grafting purposes, although in certain well-selected cases bank bone has its place; complications are fewer and the chances of success greater if frozen bank bone rather than merthiolate bank bone is used. BONE GRAFTS FOR FACIAL DEFECTS

As recently as 1916, when bone grafting of the mandible was referred to at all, it was merely mentioned for the sake of academic completeness when papers were presented at the Royal Society of Medicine (Cole and Bubb69 ). The use of bone for the repair of skeletal defects of the face became an accepted method for treating nonunited mandibular fractures during W orld War 1. A brief resume of the history of the use of bone grafts for facial defects includes the works of Delageniere,7° who employed osteoperiosteal grafts from the tibia; Lindemann,71 who employed the crest of the ilium and Gillies,72 who endorsed the method of Lindemann. Imbert and Real,73 Lebedinsky and Virenque,74 McWilliams,75 Ivy,76 Waldron and Risdon,77 Blair78 and others established bone grafting of the mandible as an accepted technique. Ivy 79 has published an excellent review of the history of bone graJting for restoration of defects of the mandible. Skull defects were repaired by bone grafts taken either from the outer table of the skull adjacent to the defect, from the tibia, or the ilium (Delageniere,70 Gulecke,80 Lexer,81 Grant and Norcross,82 Kazanjian and

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Converse83 ). Bone was also used as a nasal implant as early as 1911 by Carter 84 ; Mowlem43 considered this type of transplant most satisfactory for the treatment of saddle deformity of the nose. During W orld War II, bone grafts for surgery of the face were used extensively. Mowlem85 simplified the technique by using cancellous chiI'> bone grafts, a technique previously used by orthopedic surgeons for filling bone cavities. Bone transplants have been used for the repair of facial defects by Mclndoe,86 Ginestet,87 Ivy,88 New and Erich,89 Converse/o Gordon,91 Blocker and Weiss,92 MacComber et al.,93 Campbell,94 Dingman95 and Ragnell96 and many others. The ilium is now generally accepted as the donor site of choice for bone grafts for facial defects. "The IliUlll as a Donor Site

The portion of the iliac bone which serves as a donor site for bone grafts is composed of inner and outer tables including a layer of cancellous bone. The incision extends through the skin and periosteum to the crest of the ilium. Just prior to the incision, the skin is retracted upward by the assistant in order that the incision will lie lateral and below the crest instead of over the crest, following the removal of skin tension; the periosteum is then reflected and raised with a periosteal elevator. Depending on the amount of bone required for the operation, either a part of the crest, the full thickness of the crest, and/or the inner table are exposed. The periosteum covering the outer surface of the ala is also raised, if the full thickness of the ala is required. Bone removed from the inner aspect of the crest of the ilium is generally adequate for a nasal bone graft or a chin implant. Bone for a nasal implant can also be removed from between the inner and outer margins of the crest; after the removal of the graft, the margins of the crest are fractured and pressed together to obliterate the area from which the bone was removed. The inner table of the ilium can be removed along with some cancellous bone when a wider surface of bone is required; the periosteum is further elevated, raising the iliacus muscle with the periosteum and thus exposing a portion of the iliac fossa. By sectioning a portion of the crest vertically and splitting the crest horizontally between the vertical cuts, a section of the inner cortical table with its underlying cancellous bone attached may be separated and removed from the outer table of the bone. This technique does not disturb the continuity of the crest, thus leaving no visible deformity. It is preferable to expose the inner aspect of the ilium rather than the lateral aspect, for the periosteum is raised with greater ease over the smooth inner aspect, covered by the iliacus muscle, than over the lateral aspect, which is roughened for the insertion of the gluteal muscles. One can resort to the technique advocated by Robertson and Baron97 when a greater amount of bone is required; in this technique, the bone

Bone Grafts in Surgery of the Fooe is sectioned below the crest of the ilium, reflecting the crest upward, thus preserving the origin of the abdominal muscles. Cancellous bone is removed from the center of the bone after separation of the cortical surfaces, and the crest is then replaced in its original position; cancellous chips can be removed with a gouge. A similar technique may be employed in children; the epiphyseal cartilage which rims the crest must not be disturbed. The cartilaginous portion of the crest is incised along its junction with the bone and raised upward and medially; the cartilage is not separated from the muscles of the trunk by this method and the major part of the blood supply is preserved. We found, in our series of bone graft removals from the ilium, that when the full thickness of the ala is removed the patients experience more discomfort and difficulty in early ambulation than if the outer table of the ilium is prefilerved; this inconvenience may be the result of extensive stripping on the lateral surface of the ilium to obtain wide exposure, or the resultant weakening of the attachments of the gluteal musculature, particularly the gluteus medius and minimus, thys producibg the so-called "gluteus gait," a dragging type of persistent limp. In closing the wound, care should be exercised to obtain accurate apposition of the periosteal surface from which the abdominal and gluteal muscles arise. An unusual complication can occur as the result of removing the entire thickness of the anterior superior iliac spine. The attachment of the tensor fasciae femoris is recessed, and at the point where it normally crosses the greater trochanter the tendon slips
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The drain is placed in such a way that it may be removed the day following the operation without displacing the entire dressing. Drainage is not necessary if bone has been removed from the crest alone, as an adequate postoperative pressure dressing prevents hematoma. Early ambulation reduces the length of the period of discomfort and disability. Bone Grafts to Various Areas of the Face

Bony reconstruction of various areas of the face requires adequate exposure of the area in order to introduce the bone grafts. The surgical approach should not cause additional deforming scarring of the skin. When cutaneous scars are present which require excision and suture, the transplants can be introduced through the wound thus produced. In instances in which the wounds have healed satisfactorily and are scarcely noticeable, and in contour deformities from malunited fracture iwithout external scars and developmental malformations, other approaches may be used. Incisions for exposure may be placed in natural lskin folds, thus leaving inconspicuous scars. In certain defects of the maxilla, zygoma or mandible, the intra-oral approach is useful. An intranlJ.Sal incision avoids external scarring. Inadequate exposure because of the desire to minimize external scarring complicates the operative procedure and endangers the result of the operation. The frontal bone is exposed either through pre-existing scars, or through a coronal incision placed behind the hairline or through the eyebrow. A segment of the inner table of the ilium, with cancellous bone attached, is placed subperiosteally, bridging the defect. The cortical portion is placed against the frontal bone; the cancellous portion, more readily contoured, is placed externally. Small chips of cancellous bone are packed under this bone onlay, between it and the depressed bone or scar tissue over the dura (Fig. 94). Bone grafts to the nose, for the correction of saddle deformity, may be introduced through an external mid columellar incision or through an intranasal incision which follows the free margin of the alar cartilage. Careful elevation of the periosteum over the nasal bones is necessary to insure bony contact of the graft; this procedure may be difficult in malunited fractures, and additional rasping of the bone is necessary to adequately strip the periosteum, which is adherent in such cases. A graft of adequate shape is cut from the crest of the ilium. A small amount of the cortex of the crest is preserved to give the graft the degree of rigidity necessary in nasal implants. In flat noses with depression of the tip of the nose, the graft must extend downward into the tip beneath the area of junction of the alar cartilages; the tip and entire dorsum of the nose may be raised with a columellar strut based on the anterior nasal spine, thus supporting the dorsal bone graft (Fig. 95).

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When tightness of the overlying soft tissues interferes with the introduction of the bone graft, a smaller graft is employed; cancellous bone chips are then packed between the bone graft and the nasal bones until adequate contour is obtained.

Fig. 94. Reconstruction of the frontal bone by bone grafts. A, C, Aspect of patient !,\howing frontal bone depression following frontal sinus surgery. B, D, Result obtained by bone grafting.

Bone grafting the zygoma and adjacent area of the maxilla is best done under direct vision through the intra-oral approach (Converse99 ). This approach permits a subperiosteal view of the maxilla and zygoma from the edge of the pyriform aperture to the prominence of the zygoma. The infra-orbital nerve and vessels are avoided in these procedures. One or two grafts, mostly cancellous bone from the inner aspect of the crest of the ilium, are used for contour restoration (Fig. 96). Additional chips

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of cancellous bone are placed in the 1interstices, beneath and around the larger grafts. We have also employed a horizontal incision, following the natural skin folds which are found lateral to the outer canthus of the

Fig. 95. Correction of nasomaxillary depression by osteotomy of the maxilla and bone grafting. A, Nasomaxillary depression due to automobile accident when the patient was 3 years old. B, Result obtained by osteotomy and forward displacement of the maxilla. The nasal contour was improved by a bone graft.

-Fig. 96. Bone grafting for contour restoration after malunited fracture of the zygoma. A, Aspect of patient showing malunited depressed left zygoma. B, Restoration of contour by bone grafts introduced through the oral route.

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eye, but only in bone grafting for depression of the posterior lateral aspect of the zygoma. In nasomaxillary deformities with depression not only. of the nose but

Fig. 97. Nasomaxillary and chin deformities corrected by bone grafting. A, C, Aspect of patient with maldeveloped nasomaxillary area and chin. B, D, Result obtained by nasomaxillary, nasal and chin bone grafts.

also of the adjacent maxillary portion of the face, bone grafts are placed into the nose, as previously described, and over the maxilla around the edge of the pyriform aperture, the exposure being established subperi~ osteally through the intra~oral approach. Crescent~shaped pyramidal pieces of cancellous bone and additional bone chips are placed on each side to correct the maxillary depression (Fig. 97).

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Depressions of bone or defects of the floorofthe orbit are repaired by a portion of the inner aspect of the iliac crest of suitable thickness to restore the contour. -After an incision through the lower eyelid, the periosteum is elevated from the depressed orbital floor, the orbital contents raised to the level of the opposite eye, and the bone graft introduced (Converse and Smith100).In one case in which the maxilla and zygoma were resected for malignant disease, sparing the orbital contents, restoration of the floor of. the orbit and of the contour of the maxilla and zygoma was obtained by autogenous iliac bone grafts (Figs. 98 and 99) (Converse and Smith101 ). .

Fig. 98. Reconstruction of -the maxilla by bone grafts. A, Aspect of patient after resection of the left maxilla for carcinoma; ptosis of the left eyeball causing diplopia. B, Postoperative appearance after reconstruction by bone grafts. (From Converse, J. M. and Smith, B., Plast. & Recon. Surg. Vol. 5.)

We have used bone grafts to reconstruct various portions of the mandible. A segment of bone removed from the inner aspect of the iliac crest, comprising the cortical and cancellous bone, if fractured at two separate points to form the arch of the anterior portion of the body and symphysis of the jaw. The curve of the iliac crest is well suited to reproduce the contour of the lateral aspect of the body. The ramus and angle of the~ndible are restored by removing an angular piece of bone from the inner portion of the anterior-superior iliac spine and adjacent portions of the ilium. An important requirement in bone grafting for mandibular defects is adequate immobilization of the remaining segments by intermaxillary fixation and splints; additional fixation of grafts is obtained by wiring with fine stainless steel wire. Full-thickness defects of the mandible are approached by an external incision when the body of the mandible is

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to be grafted. The mandibular branch of the facial nerve is avoided if the· incision is made below the lower 9prder of the mandible, and if the dissection necessary to expose the .'bone is maintained deep to the platysma. The reconstruction of the ramus presents more of a problem because of the difficulty of exposure. A cleavage plane beneath the internal pterygoid and masseter muscles should be established, thus avoiding injury to the facial nerve, which is superficial to these structures.

Fig. 99. Roentgenogram showing reconstructed left maxilla and zygoma two and one-half years after bone grafting.

We have used bone grafts for chin contour r.estoration through an external incision made in the submentalfold (Fig. 100), and also through the intra-oral approach which we prefer for the insertion of small and moderate size grafts. After subperiosteal exposure of the mandible, a bone graft from the inner aspect of the crest of the ilium, comprising the inner cortical plate with its attached cancellous bone, is placed over the symphysis and small chips of cancellous bone are added between the graft and the cortical surface of the jaw (Fig. 101). In chin implants, as also in grafts over the zygoma or the frontal bone, a graft consisting of one layer of cortical bone, with its attached cancellous bone, permits bending the graft to the desired curve. Cuts are made in the cortex at suitable points with the tip of a bone-cutter, or with the edge of a rasp. The graft is then bent or partially fractured.

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Fig. 100. Deformity of the mandible corrected by osteotomy and bone transplantation. A, Aspect of the patient before treatment. B, Result obtained by osteotomy of the mandible; resection of bone from the right hemimandible which was transplanted to restore mandibular contour. A corrective nasal plastic operation was also performed.

,

Fig. 101. Bone grafting to the chin for microgenia and combined nasal plastic procedure. A, Aspect of patient showing deformed, deviated nose and microgenia. B, Aspect 'after nasal plastic operation and iliac bone grafting through the intraoral approach. (From Converse, J. M., Plast. & Recon. Surg., Vol. 6.)

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The cortical surface is placed toward the host bone and the cancellous bone toward the skin surface; cancellous chips are inserted between the host bone and the transplant. In all contour restoring bone grafts, a moderately firm pressure dressing is applied for a period of one week; in chin implants, elastoplast and adhesive are used. OBSERVATIONS AND CONCLUSIONS

Over a five year period from 1947 to 1952, we performed 189 bone grafting operations in 138 patients (Table 1). Of these bone grafts, 134 were autogenous bone and 46 were homogenous bone, preserved by deep freezing in a bone bank. In all these cases there were 12 failures. Of the 134 autografts, 6 were failures; of the 46 homografts there were also 6 failures. The failure rate in homografts was thus approximately three Table 1 ANALYSIS OF OPERATIONS IN FIVE YEAR PERIOD 1947-1952 (Number of patients bone grafted-138; Number of operations-189) OPERATIONS

AUTOGRAFTS

HOMOGRAFTS

FAILURES

Frontal bone ..................... Nose •............................ Malar bone ....................... Floor of orbit ..................... Maxilla .......................... Mandible and chin. .............

9 46 34 16 16 62

8 31 27 15 14 42

1 15 7 1 2 20

1 5 0 1 1 4

TOTAL ..........................

189

143

46

12

---

times higher than in autografts. Follow-up x-ray studies were obtained in 66 cases. Success in the other cases was determined by the consolidation of the graft with the underlying bone and maintenance of shape and size of the graft. The rapidity of consolidation can be evaluated in certain grafts, SUGh as the nose, mandible and chin, which are easily palpable .

•

Histological Examination of Bone Graft Biopsies

Biopsies of previously implanted bone grafts were obtained in 6 cases in which bone was added to a previous graft, or an overlying scar was repaired. These biopsies were obtained at periods of three to six months after bone grafting; the gross appearance of the grafts differs from that of the host bone, appearing more porous. The histological picture of the biopsied grafts (see Fig. 9) is similar to that described by Wilson;34 Reynolds, Oliver and Ramsay,36 and others. The microscopic studies indicate that with the ingrowth of capillaries, the graft is the seat of a dual process of destruction and reconstruction,

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of parallel osteoclastic and osteoblastic activity which extends over a varying period after transplantation. Active absorption of the dead trabeculae occurs simultaneously with an invasion of fibroblasts and bl00d vessels and of osteoid tissue, which appears to develop from the periphery of the transplant, penetrating int0 the interior of the graft (Fig. 102). Adjacent to the trabeculae, being absorbed by osteoclasts,

Fig. 102. Histological aspect of a 3 month old autogenous bone graft to restore chin contour. A, Photomicrograph showing in (B) an area of new bone formation with osteoblasts and in (C) an area of dead bone being resorbed. Osteoclasts are present. B, Drawing of area B in A illustrating new bone formation with osteoblasts. C, Drawing of area C in A showing dead bone with osteoc1asts.

are areas where numerous osteoblasts are present, and newly formed bone with osteocytes is replacing the dead bone by creeping substitution (Fig. 102); the graft thus seems to serve as a scaffolding for the new bone. A new cortex is formed on the surface of the transplanted cancellous bone graft as observed by Mowlem;48 this is clearly seen in roentgenograms eight to twelve weeks after transplantation (Fig. 103). Remineralization of the graft is a slow process, the graft appearing less dense on x-ray examination than the host bone in the early stages; it assumes its usual roentgenological picture following the deposition of calcium salts.

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Discussion of Failures

The analysis of the failures in this series (Table 1) shows that extraneous factors were responsible for a number of these. In one case of a frontal bone graft, the patient developed an extradural abscess due to probable residual infection following two previous unsuccessful reconstructive procedures elsewhere, employing a tantalum plate. A bone graft to restore the floor of the orbit became exposed, and was eliminated after the breakdown of heavily irradiated soft tissues. Two cases of

Fig. 103. Roentgenograms of nasal bone grafts. a, Nasal bone graft consolidated with nasal bones. Note the bony columellar strut fused with the dorsal graft. b, Nasal bone graft nonconsolidated with the nasal bones. There is evidence of decreased density in the graft. The columellar strut has not fused with the dorsal bone graft.

mandibular grafts failed, due to infection and suppuration, in attempts to repair the defects immediately following resection for carcinoma, combined with a radical dissection of the lymph nodes of the neck. An additional mandibular graft failure was due to infection and suppuration of a hematoma in a patient recently evacuated from a concentration camp and in poor physical condition. Progressive absorption occured in five nasal bone grafts and also in an onlay bone graft to the maxilla. One of these failures occurred in a case of subtotal reconstruction of the nose where the area of bony contact with host bone was inadequate; two failures occurred concomitantly in the same patient for unexplained reasons.

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In 2 cases of nasal bone grafts in which the graft was not consolidated with the bony framework, there were no signs of absorption. One such case has been observed over four years; it shows decreased density to the penetration of roentgen rays but its shape remains unchanged and it continues to give adequate contour support. Carter,t°2 McWilliams/o3 Mowlem 43 and Peer 104 stated that bone grafts of rib, iliac and septal bone retained their structure even though the grafts were not in contact with bone. These observations are puzzling, for no absorption occurred in any of the grafts in the present series which became firmly fixed to the host bone, and we presume that these nonconsolidated bone grafts will be absorbed ultimately; for this reason these 2 cases are listed as failures in our series. In bone grafts that were absorbed, the cancellous part was seen to disappear within two months, whereas the cortical persisted for a far longer period of time. The absorption of nonconsolidated cortical bone may extend over a period of years, as illustrated in the following case. A woman, aged 35 years, underwent a reconstructive bone grafting operation to restore the right hemimandible, resected 5 years previously for an adamantinoma. A bone homograft was used, the right side of a cadaver mandible, removed after an accidental death. The angle of the mandibular homograft was not similar to that of the mandible of the host. The graft was cut through at the angle in order to adapt the contour to the recipient site and the mandibular symphysis. The graft consolidated at the symphysis with the host bone; the ramus, however, failed to consolidate in the area of the angular section and fibrous union only occurred. The ramus of the graft persisted for 2 years; it became absorbed and disappeared in the third year.

It was noted in our series of bone grafts that after the graft had become consolidated to the host bone, no further changes in shape or size occurred; the graft was not progressively absorbed as are other types of implants. The original shape and size of the bone graft appeared to be maintained despite the extensive cellular repopulation within the graft. The impression of a slight diminution in size of the implant may be due to the subsidence of postoperative edema. When large quantities of bone chips are used, the postoperative dressing and gradual contraction of the healing tissues causes the chips to be pressed more closely together and a slight shrinkage of the entire bone mass occurs. Intra-oral Bone Grafting

Mowlem85 had noted that communication with the oral cavity need not be a barrier to the use of cancellous bone grafts. We obtained successful results in all 53 contour-restoring onlay bone grafts introduced through the intra-oral route. Exposure of the implanted bone occurred in 2 cases; one of these showed a purulent exudation through a small

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395

fistula for three weeks; the drainage eventually stopped spontaneously. In the other case, a mucopurulent discharge persisted one week, a small bone chip which cut through the mucosa was removed and the wound healed a few days later. We have had successful results in 3 cases of immediate reconstruction of the mandible (Marino et aU 05 ) in full-thickness defects communicating with the oral cavity following excision of benign or malignant tumors. In 2 additional cases of reconstruction following lengthy operations for careinoma, with concomitant block dissection of the lymph nodes of the neck in aged patients, failure occurred due to infection, suppuration and elimination of the graft. It is our feeling that in this type of patient, immediate reconstruction of full-thickness mandibular defects should be approached with caution. Autogenous Versus HOlllogenous Bone Grafts

In testing the degree of fixation of bone grafts to host bone, fresh autogenous onlay bone grafts, consisting mostly of cancellous bone, appeared attached in seven to ten days; homografts required a longer period. Adhesive strapping only was required to protect autogenous cancellous grafts after one week. When fresh autogenous bone grafts were employed, the consolidation period varied between four and six weeks in full-thickness defects of the mandible; when homografts were used a much longer period of time elapsed before consolidation occurred. In one graft of mandibular cadaver bone, immobilization by splinting was required for a period of four months before consolidation was completed. Six of 134 autogenous grafts failed as against 6 of 46 homografts. A factor to be considered in these figures is that a number of the homogenous bone grafts consisted of cortical bone, being the left-over cortical portion of iliac bone grafts, the cancellous portion having been used for fresh autogenous grafts; failures due to the use of homogenous bone may thus possibly be attributed to the fact that the homografts were mostly cortical bone. Cancellous Versus Cortical Bone Grafts·

There is considerable difference between the use of bone grafts in various portions of the anatomy. In facial bone grafts, rapid consolidation is necessary because prolonged immobilization is not as feasible in the face as, for example, in the extremities. The progressively subsiding impetus of osteogenesis requires rapid consolidation; this is best achieved by the use of autogenous cancellous grafts. The free surfaces of cancellous bone are more readily exposed to tissue fluid nourishment than cortical bone. The cellular elements of bone and the organic intercellular sub-

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stance in the early stages following transplantation are nourished by extracellular fluid before the ingrowth of new capillaries occurs, a process usually requiring a number of days. The nutrient fluids may penetrate the grafted bone in the manner described by Ham 106 as "nutrition beyond the capillaries." Although tissue fluids may circulate through the minute canaliculi of bone, it seems more probable that such tissue fluid serves as a means for diffusion of nutritional and waste substances. The high percentage of success obtained in this series may be attributed to the fact that the majority of the bone grafts were of the onlay type, placed under the periosteum with wide bony surface contact with the host bone. This condition was not present, however, in all cases. In nasal bone grafts the implant had contact with the host bone only at the upper portion of the graft. In a case of reconstruction of the maxilla (Figs. 98 and 99), bony contact between the grafts employed, and the host bone, could be established only in two small areas, one over the frontal process of the maxilla and the other at the anterior part of the zygomatic process of the temporal bone; successful consolidation of the bone grafts ensued. The surface of contact of the bone graft with the host bone is relatively small in full-thickness mandibular defects. In all such types of defects where a wide surface of contact with the host bone is not feasible, fresh autogenous bone is particularly indicated because of its higher osteogenic activity. Bank homogenous bone has pr(wed useful for small defects, such as a small chin implant. It seems illogical in such small defects to remove bone from the ilium, thus causing postoperative discomfort out of proportion to the defect to be repaired. Bank bone may be required during an operation when no previous plans for taking the graft had been anticipated, such as, for example, the addition of a bony implant in the course of a nasal plastic operation. Small chips of homogenous cancellous bank bone have been employed in the course of osteotomy of the ramus of the mandible to give additional osteogenic impetus and to promote the consolidation of the osteotomy line. Bank bone is also useful to supplement autogenous bone when an insufficient amount of bone has been removed. When stage procedures are necessary, excess autogenous bone may be stored for future use, thus £Lvoiding the repeated removal of iliac bone grafts. Relatively small quantities of bone are required in bone grafting of the facial area and it is generally possible to obtain enough bone from the patient's ilium. We have never encountered a patient with a facial deformity who objected to the removal of bone from the ilium. If homogenous cancellous bone were as satisfactory as autogenous bone the need for the removal of bone from the patient's ilium with the attendant discomfort would not exist. Until this fact is proved, however, fresh autogenous cancellous bone remains the material of choice.

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SUMMARY

1. This is a report of 189 bone grafts for the repair of facial defects. 2. A review of the history of bone transplantation is presented. 3. The development of the bone bank is discussed. 4. The use of iliac bone grafts is described and discussed in relation to bone grafting of various areas of the face. 5. Histological observations of biopsied bone grafts are included. 6. Failures of certain bone grafting operations are analyzed. 7. A discussion of the advantages of fresh autogenous versus bank homogenous bone grafts, and cancellous versus cortical bone grafts, is included. Acknowledglllents

We wish to thank Dr. Milton Helpern, who prepared and interpreted the histological sections, Dr. A. Cecil Taylor, who made the photomicrographs, Dr. J. L. Robin, who assisted in the bibliography and Dr. Harry H. Shapiro for his edi torial assistance.

REFERENCES 1. North, J. F.: The Use of Preserved Bovine Cartilage in Plastic Surgery. Plast. & Reconstruct. Surg. 11: 261, 1953. 2. Gibson, T. and Davis, W. B.: The Fate of Preserved Bovine Cartilage Implants in Man. Brit. J. Plast. Surg. 6: 4,1953. 3. Schofield, A. L.: A Preliminary Report on the Use of Preserved Homogenous Cartilage Implants. Brit. J. Plast. Surg. 6: 26,1953. 4. Keith, A.: Menders of the Maimed. London, H. Frowde, 1919. 5. Duhamel, H. L.: Quatrieme memoire sur les os. Dans lequel on se propo~e de rapporter de nouvelles preuves qui etablissent que les os croissent en grosseur par l'addition de couches osseuses qui tirent leur origine du perioste. Communication a l'Ac. Roy. des Sciences 56: 87,1743. 6. Syme, J. (quoted by Keith, A.): Menders of the Maimed. London, H. Frowde, 1919. 7. Ollier, L.: Traite experimental et clinique de la regeneration des os et de la production artificielle du tissu osseux. Paris, G. Masson et fils, 1867. 8. Goodsir, J. and Goodsir, H. D. S.: Anatomical and Pathological Observations. Edinburgh, M. Macphail, 1845. 9. Macewen, W.: The Growth of Bone. Glasgow, J. Mackhose, 1912. 10. Barth, A.: Ueber histologische Befunde nach Rnochenimplantationen. Arch. f. klin. Chir. 46: 409, 1893. 11. Gallie, W. E.: The History of a Bone Graft. J. Am. Orth. Surg.12: 201,1914. 12. Phemister, D. B.: The Fate of Transplanted Bone and Regenerative Power of Its Various Constituents. Surg., Gynec. & Obst. 19: 303,1914. 13. Leriche, R. and Policard, A.: Le perioste et son role dans la formation de l'os. Presse med. 26: 143, 1918. Fundamental principles in Pathology of Bone. Surg., Gynec. & Obst. 43: 308, 1926. Normal and Pathological Physiology of Bone. St. Louis, C. V. Mosby Co., 1928. 14. Gallie, W. E. and Robertson, D. E.: The Repair of Bone. Brit. J. Surg. 7: 211, 1919. 15. Orell, S.: Surgical Bone Grafting with Os Purum, Os Novum and Boiled Bone. J. Bone & Joint Surg. 19: 873, 1937.

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16. Robison, R.: Possible Significance of Hexosephosphoric Esters in Ossification. Biochem. J. 17: 286, 1923 . . 17. Huggins, C. B.: The Formation of Bone under the Influence of Epithelium of the Urinary Tract. Arch. Surg. 22: 377, 1931. 18. Levander, G.: A Study of Bone Regeneration. Surg., Gynec. & Obst. 67: 705,1938. An experimental Study of the Role of the Bone Marrow in Bone Regeneration. Acta chir. Scandinav. 8S: 545, 1940. Alcohol-soluble Osteogenetic Substance from Bone Marrow. Nature 167: 587,1946. 19. Annersten, S.: Experimentelle Untersuchungen ueber die Osteogenese und die Biochemie des Fractur Callus. Acta chir. Scandinav. 84 (Suppl.): 60,1940. 20. Heinen, J. H.: The Experimental Production of Ectopic Bone and Cartilage in the Muscles of Rabbits. J. Bone & Joint Surg. SlA: 765,1949. 21. Lacroix, P.: L'organisation des os. Liege, Belgium, Desoer, 1949. 22. Urist, M. R. and McLean, F. C.: Osteogenetic Potency and New Bene Formation by Induction in Transplants to the Anterior Chamber of the Eye. J. Bone & Joint Surg. S4A: 443, 1952. 23. Baentzner, W.: Ueber experimentelle freie Periostverpflanzung. Arch. f. klin. Chir. 118: 504, 1921. 24. Bull, C. R.: Experimentelle Studien ueber Knochentransplantation und Knochenregeneration. Norske Videnskaps-Akademi, Oslo; I. Matem.Naturo. Klasse No.9, 1928. 25. Levander, G.: Ueber die Knochenregeneratorische Fohigkeit des Periosts. Acta chir. Scandinav. 8S: 1, 1939. 26. Pollock, G. A. and Henderson, M. S.: Value of Periosteum in Bone Grafting Operation. Proc. Staff Meet., Mayo Clin. 16: 443, 1940. 27. Bonome, A.: Zur Histogenese der Knochenregeneration. Virchow's Arch. f. path. Anat. 100: 293, 1885. 28. Kolodny, A.: The Periosteal Blood Supply and the Healing of Fractures. Experimental Study. J. Bone & Joint Surg. 5: 698,1923. 29. Reiss, E.: Experimentelle Studien ueber die knochenbildende Kraft des Periostes. Arch. f. kline Chir. 129: 750 (1924). 30. Bisgard, J. D.: Ossification. The Influences of the Mineral Constituents of Bone. Arch. Surg. SS: 926, 1936. 31. White, C.: Communication to the Royal Society, 1769. 32. Kazanjian, V. H.: Spontaneous Regeneration of Bone Following Excision of Section of the Mandible. Am. J. Orth. & Oral. Surg., S2: 242, 1946.· 33. Bertelsen, A.: Experimental Investigations into Post Foetal Osteogenesis. Acta orthop. Scandinav. 15: 139, 1944. 34. Wilson, P. D.: Experiences with a Bone Bank. Ann. Flurg. 126: 932,1947. Follow-up Study of the Use of Refrigerated Homogenous Bone Transplants in Orthopedic Op.erations. J. Bone & Joint Surg. SSA: 307,1951. Experience with the Use of Refrigerated Homogenous Bone. J. Bone & Joint Surg. SSE: 30, 1951. 35. Reynolds, F. C. and Oliver, D. R.: Experimental Evaluation of Homogenous Bone Grafts. J. Bone & Joint Surg. S2A: 283 (1950). 36. Reynolds, F. C., Oliver, D. R. and Ramsey, R.: Clinical Evaluation of Merthiolate Bone Bank and Homogenous Bone Grafts. J. Bone & Joint Surg. SSA: 873, 1951. 37. Barth, A.: Ueber Osteoplastik. Arch. f. klin. Chir. 86: 859, 1908. 38. Axhausen, G.: Die histologischen und klinischen Gesetze der freien Osteo· plastik auf Grund von Tierversuchen. Arch. f. klin. Chir. 88: 23, 19081909. 39. Mayer, L. and Wehner, E.: An Experimental Study of Osteogenesis. Am. J. Orth. Surg. 12: 213, 1914. 40. Haas, S. L.: Spontaneous Healing Inherent in Transplanted Bone. J. Bone & Joint Surg. 4: 209, 1922.

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41. Brooks, B.: Studies in Bone Regeneration. Ann. Surg. 66: 625,1917. 42. Rhode, C.: Does Bone Form from Osteoblasts or from a Metaplasia of the Surrounding Connective Tissue? Surg., Gynec. & Obst. 41: 740, 1925. 43. Mowlem, R.: Bone and Cartilage Transplants: Their Use and Behaviour. Brit. J. Surg. 29: 182, 1941. 44. Abbott, L. C., Schottstaedt, E. R., Saunders, J. R. de C. M. and Bost, F. B.: The Evaluation of Cortical and Cancellous Bone as Grafting Material. J. Bone & Joint Surg. 29: 381, 1947. 45. Ham, A. and Gordon, S.: The Origin of Bone That Forms in Association with Cancellous Chips Transplanted into Muscle. Brit. J. Plast. Surg. 6: 154, 1952. 46. Campbell, C. J., Brower, T., Macfadden, D. C., Payne, E. B. and Doherty, J.: Experimental Study of the Fate of Bone Grafts. J. Bone & Joint Surg. 36A: 332, 1953. 47. Fell, H. B.: The Osteogenetic Capacity in vitro of Periosteum and Endosteum Isolated from the Limb Skeleton of Fowl Embryos and Young Chicks. J. Anat. 66: 157, 1932. 48. Gaillard, P. J.: Hormones Regulating Growth and Differentiation in Embryonic Explants. Paris, Hermann, 1942. 49. Judet, J. and Delaunay, D.: Personal communication, 1953. SO. Heinen, J. H.: The Differentiation of Bone and Cartilage from Tissue Cultures of Osteogenic Cells. Ph.D. thesis, Univ. of Chicago, 1940. 51. Pfeiffer, C. A.: Development of Bone from Transplanted Marrow in Mice. Anat. Rec. 102: 225, 1948. 52. Albee, F. H.: Bone Graft Surgery. Philadelphia, W. B. Saunders Co., 1915. 53. Bert, P.: Recherches experimentales de la vitalite propre des tissus animaux. Paris, 1866. 54. Carrel, A.: Preservation of Tissues and Its Application to Surgery. J.A.M.A. 69: 523, 1912. 55. lnclan, A.: Use of Preserved Bone Grafts in Orthopedic Surgery. J. Bone & Joint Surg. 24: 81, 1942. 56. Bush, L. F.: The Use of Homogenous Bone Grafts; A Preliminary Report on the Bone Bank. J. Bone & Joint Surg. 29: 620, 1947. 57. Kreuz, F. P., Hyatt, G. W., Turner, T. C. and Bassett, A. L.: The Preservation and Clinical Use of Freeze-Dried Bone. J. Bone & Joint Surg. 33: 863,1951. 58. Judet, R., Judet, J., Lagrange, J. and Dunoyer, J.: Communication sur les heterogreffes. Mem. Acad. chir., Paris, Dec. 3, 1952. 59. Mosiman, R. S.: A Study of Bone Growth. In Surgical Forum, Philadelphia, W. B. Saunders Co., 1951. 60. Bosworth, D. M., Wright, H. A., Fielding, J. W. and Goodrich, E. R.: A Study in the Use of Bank Bone for Spinal Fusion in Tuberculosis. J. Bone & Joint Surg. 36A: 329, 1953. 61. Reynolds, F. C.: Discussion of papers of Bosworth et al. J. Bone & Joint Surg. 36A: 344, 1953. 62. Ray, R. D., Degge, J., Gloyd, P. and Mooney, G.: Bone Regeneration. An Experimental Study of Bone Grafting Materials. J. Bone & Joint Surg. 34A: 638, 1952. 63. Kiehn, C. L~, Cebul, F., Berg, M., Gutentag, J. and Glover, D .. M.: A Study of the Vascularization of Experimental Bone Grafts by Means of Radioactive Phosphorus and the Transparent Chamber. Ann. Surg. 136: 404, 1952. 64. Roth, Hans: Die Konservierung von Knochengewebe fur Transplantationen. Julius Springer-Verlag, Wien (1952). 65. Rogers, B. 0., Converse, J. M., Taylor, A. C. and Campbell, R. M.: The Eosinophile in Skin Homografting. Proc. Soc. Exper. BioI. & Med. 82: 523, 1953. 66. Lloyd-Roberts, G. C.: Experiences with Boiled Cadaveric Bone. J. Bone & Joint Surg. 34B: 428,1952.

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67. Watson-Jones, R.: Quoted by Wilson in discussion of Campbell et al. 46 and Bosworth et al. 60 68. Frantz, C. H., Reynolds, F. C. and Lipscomb, P. R.: Report of the Committee t.o Study the Preservation of Bone. J. Bone & Joint Surg. 35A: 774, 1953. 69. Cole, P. P. and Bubb, C. H.: Bone Grafting in Ununited Fractures of the Mandible: With Special Reference to the Pedicled Graft. Brit. Med. J. 1: 67,1919. 70. Delageniere, H.: Les greffes periostiques prises au tibia. Bull. et memo Soc. chir. Paris 42: 1048, 1916. Methode generale et technique des greffes osteoperiostiques prises au tibia pour la reconstitution des os ou la reparation des pertes de substance osseuse d'apres 118 nouvelles observations personnelles. Bull. et memo Soc. chir. Paris (1917). 71. Lindemann, A.: Ueber die Beseitigung der traumatischen Defekte der Gesichtsknochen. Behandlung der Kieferschussverletzungen 4: 6, Wiesbaden, 1916. 72. Gillies, H. D.: Plastic Surgery of the Face. London, Oxford Univ. Press, 1920. 73. Imbert, L. and Real, P.: Le traitement chirurgical des pseudoarthroses des maxillaires. Marseilles med. 53: 193, 1916. 74. Lebedinsky, J. and Virenque, M.: Prothese et chir. maxillo-faciale. Bailliere, Paris, 1918. 75. McWilliams, C. A.: The Treatment of Bony Defects of the Lower Jaw. Ann. Surg. 65: 283, 1917. 76. Ivy, R. H.: War Injuries of the Face and Jaws. Surg., Gynec. & Obst. (Int. Abst. Surg.) 27: 101, 1918. 77. Waldron, C. W. and Risdon, E.: Mandibular Bone Grafts. Proc. Roy. Soc. Med. 12: 11, 1919. 78. Blair, V. P.: Some Observations on Our War Experiences with Face and Jaw Injuries. Mil. Surgeon 47: 379, 1920. 79. Ivy, R.: Bone Grafting for Restoration of Defects of the Mandible. ColI. Rev., Plast. & Recon. Surg., Int. Abst. 7: 333, 1951. 80. Gulecke, N. : Ueber das Schicksal bei Schaedel plastiken verpflan tzter Gewe be. Bruns Beitr. z. klin Chir. 107: 503, 1917. 81. Lexer, E.: Die gesamte Wiederherstellungschirurgie. Leipzig, J. A. Barth, 1931. 82. Grant, F. C. and Norcross, N. C.: Repair of Cranial Defects by Cranioplasty. Ann. Surg. 110: 488, 1939. 83. Kazanjian, V. H. and Converse, J. M.: Reconstruction after Radical Operation for Osteomyelitis of Frontal Bone. Arch. Otolaryn. 31: 94,1940. 84. Carter, W. W.: Transplantation of Bone for Correction of Depressed Deformities of the Nose with Report of Cases. Laryngoscope 21: 94,1911. 85. Mowlem, R.: Cancellous Chip Bone Grafts. Lancet 2: 746, 1944. 86. McIndoe, A. H.: Surgical and Dental Treatment of Fracture of Upper and Lower Jaws in Wartime. Proc. Roy. Soc. Med. 34: 267,1941. 87. Ginestet, G.: Des greffes d'os total dans Ie traitement des pseudoarthroses du maxillaire inferieur. Rev. de Stomatol. 42: 287, 1941. 88. Ivy, R. H.: The Repair of Bony and Contour Deformities of the Face. Am. J. Orthod. & Oral Surg. 30: 76 1944. 89. New, G. B. and Erich, J. B.: Bone Grafts to the Mandible. Am. J. Surg.63: 153, 1944. 90. Converse, J. M.: Early and Late Treatment of Gunshot Wounds of the Jaw in French Battle Casualties in North Africa and Italy. J. Oral Surg. 3: 112, 1945. 91. Gordon, S.: The Role of Cancellous Bone in Plastic Surgery. Surg. 20:)02, 1946. 92. Blocker, T. G. and Weiss, L. R.: Use of Cancellous Bone in the Repair of Defects about the Jaws. Ann. Surg. 123: 622, 1946.

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93. MacComber, W. B., Shepard, R. A. and Crofut, V. E.: Mandibular Bone Grafts. Plast. &.Recon. Surg. 3: 570, 1948. 94. Campbell, H. H.: Reconstruction of Left Maxilla. Plast. & Recon. Surg. 3: 66, 1948. 95. Dingman, R. 0.: The Use-o(Iliac Bone in the Repair of Facial and Cranial Defects. Plast. & Recon. Surg. 6: 179, 1950. 96. Ragnell, A.: A Simple Method of Reconstruction in Some Cases of Dish-Face Deformity. Plast. & Recon. Surg. 10: 227,1952. 97. Robertson, I. M. and Baron, J. N.: A Method of Treatment of Chronic Infective Osteitis. J. Bone & Joint Surg. 28: 19, 1946. 98. Oldfield, M. C.: Iliac Hernia after Bone Grafting. Lancet 1: 810, 1945. 99. Converse, J. M.: Restoration of Facial Contour by Bone Grafts Introduced Through the Oral Cavity. Plast. & Recon. Surg. 6: 295, 1950. 100. Converse, J. M. and Smith, B.: Reconstruction of the Floor of the Orbit by Bone Grafts. Arch. Ophth. 44: 1, 1950. 101. Converse, J. M. and Smith, B.: Case of Reconstruction of the Maxilla Following Resection for Carcinoma of the Antrum. Plast. & Recon. Surg. 5: 426, 1950. 102. Carter, W. W.: Value and Ultimate Fate of Bone and Cartilage Transplants in Correction of Nasal Deformities. Laryngoscope 33: 196, 1923. Ultimate Fate of Bone When Transplanted into Nose for Purpose of Correcting Deformity. Arch. Otol. 15: 563, 1932. 103. McWilliams, C. A.: The Periosteum in Bone Transplantations. Is Contact with Living Bone Necessary for the Life of Grafts and Will Transplanted Periosteum Produce New Bone? J.A.M.A. 62: 346, 1914. 104. Peer, L.: The Fate of Autogenous Human Bone Grafts. Brit. J. Plast. Surg. 3: 233, 1950-1951. 105. Marino, H., Turco, N. B. and Craviotto, M.: Immediate Reconstruction of the Lower Jaw Following Surgical Excision of Large Tumors. Plast. & Recon. Surg. 4: 36, 1949. 106. Ham, A. W.: Some Histophysiological Problems Peculiar to Calcified Tissues. J. Bone & Joint Surg. 34A: 701, 1952. 722 Park Avenue New York 21 (Dr. Converse)