Ann 0101 88 :1979
ROLE OF PERIOSTEUM ON THE FATE OF PEDICLE OSTEOCUTANEOUS GRAFTS lliNALDO
F.
CANALIS,
MD
TORRANCE, CALIFORNIA WILLIA...'\1
G.
HEMENWAY,
MD
PAUL
Los ANGELES, CALIFORNIA
H. WARD, MD
Los ANGELES, CALIFORNIA
Recent studies on the fate of pedicle osteocutaneous grafts have shown that they remain viable and may be actively involved in the mechanics of bone repair. This communication reports on a series of experiments aimed to clarify the role of periosteum in the survival of pedicle-assisted bone grafts. Osteocutaneous grafts were developed in dogs in such a manner as to isolate the implant from normal recipient bone. Free bone grafts were used as controls and a group of pedicle periosteal grafts were studied as potential sources of bone formation. Specimens were evaluated at regular intervals over a 40-week period. The pedicle bone grafts maintained their viability and developed vigorous osteoneogenesis. The process was progressive and eventually resulted in partial substitution of the original graft by new bone of periosteal origin. The free bone grafts were resorbed and no bone formation was obtained in pedicle periosteum specimens. The study provides clear evidence that under experimental conditions no bone contact is needed to maintain the viability of pedicle osteocutaneous grafts. It also shows that the periosteum has the leading role in the restructuring process of these grafts.
Recently the authors reported on a series of experiments aimed towards a clearer understanding of the fate of pedicle osteocutaneous grafts.' This study, together with the results of clinical experience," indicates that these grafts not only survive but participate actively in bone repair. The present communication discusses the results of a group of experiments devised to gain further insight into two aspects of this process remaining obscure: 1) the extent of recipient bone participation in structural repair and 2) the degree of periosteal involvement in this activity. In addition, the possibility of utilizing vascularized periosteum as a potential source of bone formation was also explored. METHODS AND MATERIALS Six adult mongrel dozs weighing between 20 and 25 kg were used. Sodium pentobarbital (600 mg/kg intravenously) and 1% lidocaine hydrochloride with epinephrine (1: 100,000, 10-12 cc subcutaneously) were employed as anesthesia. A forehead flap approximately 4 em wide was raised from the root of the ear to the lateral extent of the anterior wall of the frontal sinus. The forehead skin was incised at the midline and circumferentially around the upper
and lower limits of the sinus. The tissues between the skin and the periosteum covering the anterior wall of the sinus were carefully preserved and an oscillating saw was used to free the ipsilateral half of this wall from the surrounding bone. This waIl was maintained in continuity with the flap by its periosteal attachments (Fig. 1). Following this, the flap was tubed and rotated upwards. Its distal end was sutured to the fascia of the parietal muscle, taking care to immobilize the bone graft upon this structure. On the contralateral side a similar procedure was undertaken, but the distal end of the flap incorporated only the periosteum overlying the anterior frontal table. After tubing and rotating this flap, the periosteum was also sutured to the fascia of the ipsilateral parietal muscle. Finally, the remaining anterior table of the frontal sinus was removed and placed under the skin of the calvarium to be used as a control. Primary closure was accomplished by simple undermining and mobilization of the skin. Postoperatively each animal received benzathine penicillin G (600,000 units intramuscularly) and was allowed a normal diet. Animals were again anesthetized and the specimens removed at 8, 10, 24, 28, 36, and 40 weeks after the operation. Care was taken to include the distal portion of the flap and a generous portion of the parietal muscle underlying the implants. The size and general appearance of the grafts were recorded and the specimens were processed for light microscopy. Hematoxylin and eosin staining was used in all cases. In order to more objectively quantify the
From the Division of Head and Neck Surgery, Department of Surgery, UCLA School Medicine, Los Angeles, California and Harbor General Hospital, Torrance, California.
642
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
ot
OSTEOCUTANEOUS GRAFTS
643
Fig. 1. Forehead flap incorporating the ipsilateral anterior wall of the frontal sinus (G). Arrows mark limit of tubing to be done before rotation. degree of new bone formation in osteocutaneous grafts, equal magnification microphotographs (X60) of each specimen were obtained. Multiple measurements (10 to 12) of the ossification layer developing along the periosteal surface were taken from 5 x 7 prints. These were then averaged, converted into microns and used for comparison. RESULTS
All soft tissue pedicles healed without complications and, upon sectioning, their core showed abundant arterial and venous channels. The pedicle periosteum specimens were grossly unremarkable. Miscroscopically the periosteum could be identified as a fibrous layer of variable thickness devoid of any changes suggesting new bone formation. The pedicle osteocutanous grafts exhibited several interesting findings which are summarized in Table 1. In contrast with free bone grafts which underwent complete resorption, pedicleTABLE 1. RESULTS OF PEDICLE OSTEOCUTANEOUS GRAFTS ISOLATED FROM RECIPIENT BONE
Dog
1 2 3 4 5 6
Time (wks)
Original Graft Size" (mm)
8
23
10
25 23 24 24 24
24 28 36 40
Final Graft Size" (mm)
Osteoneogenesis"" (1-')
23 25 22 24 22 26
15 15 21 22 57 61
·Represents greater diameter. •• Approximate thickness of new bone layer.
Fig. 2. Eight-week specimen. Layer differentiation of spindle-shaped precursor cells (Sp) into osteoblasts (Ob) is clearly evident. The darker (basophilic) line between arrows rel?resents osteoneogenesis (H & E, XI60). Inserts show examples of mitotic activity seen in the periosteal periphery. (X300)
assisted implants retained their original size in most instances. One of the late specimens (40 weeks) showed a slight increase in diameter and thickness. Microscopically, the most striking features of these grafts were the persistence of viable osteocytes and the development of vigorous periosteal osteogenesis. The latter process appeared to be a progressive phenomenon which was most active in the 36- and 40-week specimens and was initially characterized by thickening of the periosteal layer to many times its normal size. Increase in the population of the spindle-shaped osteoprogenitor cells, gradual differentiation of these elements into distinct osteoblasts and profuse vascularization underlined this change (Fig. 2). As in any other form of osteogenesis, the osteoblasts were aligned along newly-deposited osteoid material, and as the process progressed, became incorporated into developing lacunae. Occasionally mitotic activity could be noted in the most peripheral areas (Fig. 2 insert). Early in the process, it became ap-
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
644
CANALIS ET At
Fig. 3. Eight-week specimen. A) Overall view demonstrating thickening (P) and a thin layer of new bone (arrow) overlying the X60). B) Detail of the area enclosed in rectangle. The lacunae of the osteocytes. Arrow points to newly-formed bone. p - Periosteum. (H
parent that newly-deposited bone, characteristically basophilic in aspect, tended to replace the bone graft. This finding, which was initially of modest proportions (Fig. 3), eventually became extremely prominent, and in late specimens, areas of new bone were noted to invade the graft throughout its thickness (Fig. 4). It must be emphasized that periosteal osteogenesis was limited to the surface directly vascularized by the
proximal periosteal graft (g) (H & E, graft are filled with & E, X120)
pedicle. The mucoperiosteal lining of the frontal sinus did not appear to undergo any change during the early phases and it frequently retained its normal pseudostratified ciliated epithelium which was left untouched during the surgical procedure. Eventually, the epithelium disappeared and the periosteum and advancing new bone virtually enveloped the graft by extending into this surface (Fig. 5A). Mature lamellar
Fig. 4. Twenty-four-week specimen demonstrating progression of the changes illustrated in Figure 3. A) Overall view. Area between arrows represents osteoneogenesis (H & E, X60). B) Detail of area enclosed within rectangle showing digitations of new bone invading the graft. Note early lacunar formation (arrows). P - Periosteum. (H & E, X140)
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
OSTEOCUTANEOUS GRAFTS
,
f
645
.....•
"
Fig 5 Thirty-six-week specimen. A) Overall view demonstrating diffuse subs~itu tion of the proximal table of the graft (g); P - Periosteum. (f.I &. E, X60) ..B) Detail of area enclosed within rectangle demonstrating advanced organization of penosteally generated bone. (H & E, X160)
bone with organized haversian canals was present in later specimens (Fig. 5B). Throughout these changes the bone graft, although exhibiting lacunae retaining morphologically n0fl!l~ osteocytes, did not appear t? participate actively in the reparative process. It seemed to provide the scaffold through which osteoneogenesis took place. DISCUSSION
The described experiment provided an excellent model to study the evolution of pedicle osteocutaneous grafts isolated from recipient bone. It must be stressed, however, that some conclusions may not be applicable to bone and bone grafts in general sin.ce. the model.u~ed is somewhat unique IS ItS charactenstics. It is a thin, (1.5 to 2.0 mm), predominantly cortical bone with very broad periosteal attachments, and is supplied by a profusely vascularized flap. In previous experiments,' it was felt that pedicle bone participated actively
in the repair process, but it was assumed that healing necessitated apposition of the graft to healthy recipient bone. This study provides clear evidence that restructuring depends almost entirely on a remarkably active process of periosteal osteogenesis which is, at least tempor-. arily, independent from t~e presen~e. of recipient bone. Such periosteal activity may depend on factors similar to those encountered by Judet and Patel" in the treatment of pseudarthrosis with muscle pedicle bone grafts. These investigators demonstrated that bridging of bony defects was drastically enhanced, even in the presence of infection, by using bone chips attached to vascularized periosteum. The vascular dependency of this process is demonstrate.d.in th~ describ~d experiments by the strikmg difference m bone production existing between the pedicle pole of the graft and its mucoperiosteal side. It is also corroborated by the investigators' previous work with tetracycline-labeled specimens, th~t showed intense fluorescence on the penosteal side of similar grafts.'
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
646
CANALIS ET AL
Periosteal activity increases through time and eventually results in replacement of the bone graft. This process of substitution was slow, since even after 40 weeks it remained incomplete, and it may be a function of the relatively small blood supply of these grafts. Another retarding factor may be related to the viability of the bone graft itself. In most instances of bone replacement, osteoclastic activity has to contend with devitalized bone which undoubtedly facilitates resorption. In this experiment, maintenance of the normal organization of bone may actually hinder the process of breakdown and substitution. Recently the possibility of stimulating periosteum to produce bone by maintaining its vascularization was demonstrated by Finley et al.' These investigators were able to reconstruct a portion of a dog's tibia by bridging it with costal periosteum vascularized by microanastomosis to the tibial artery and saphenous vein. Their subsequent attempts to bridge defects in the head and neck failed and it was assumed that lack of mechanical stress prevented bone formation. Our results do not support this thesis since, in the osteocutaneous grafts which were totally stress-free, the leading activity was periosteal osteogenesis. The various factors determining bone production by periosteal grafts are not completely understood. Among the causes of failure acting in our series, the age. animal species and status of the cambium layer are likely to be impor-
tant. Since allier's classic work," osteogenesis by periosteal grafts has been less successful in adult dogs than in any other experimental animal. Riess" has shown that in dogs younger than eight months, with an intact cambium layer, bone production may be obtained consistently, the opposite being true for older animals. A factor common to many experiments in which bone formation is obtained, is the presence of sectioned or fractured bone. For several decades the presence of an osteogenic factor liberated by devitalized bone has been implicated in osteogenesis," This "inductor substance" could be responsible for the process leading to callous formation, bone resurfacing, and for the development of bone under abnormal conditions. The existence of such substance has a histological basis in the demonstration of primitive connective tissue cells changing into osteoblasts while still distant from areas of active new bone formation." Additional indirect evidence is found in the many instances of ectopic ossification" and in the osteogenic process of the grafts described here. The results discussed open several areas of investigation that may clarify certain aspects of bone graft behavior and perhaps result in the availability of new clinical methods. The possibility of producing bone from a malleable soft tissue source could offer a solution to many reconstructive problems of the head and neck and merits further study.
REFERENCES ioste desgreffes osseuses. Gaz Med (Paris) 14: The fate of osteocutanous grafts in mandibulo- 212-233, 1859 facial restoration. Laryngoscope 87 :895-908, 6. Riess E: Experimentelle Studien uber 1977 dies knochenbielden de Kraft des Periostes. 2. Ward PH, Canalis RF, Fee W, et al: Arch Klin Chir 129:750-756, 1924 Composite hyoid sternohyoid muscle graft in 7. Young R"V: Cell proliferation and spehumans. Arch Otolaryngol 103:531-534, 1977 cialization during endochondral osteogenesis 3. [udet R, Patel A: Muscle pedicle bone in young rats. J Cell BioI 14:357-361, 1962 grafting of long bones by osteoperiosteal de8. Bloom W Bloom MD McLean FC: cortication. Clin Orthop 87:74-80, 1972 Calcification and' ossification: Medullary bone 4. Finley JM, Acland RD, Wood MB: Re- changes in the reproductive cycle of female vascularized periosteal grafts. A new method pigeons. Anat Rec 81:443-450, 1941 to p~oduce functional new bone without bone 9. Heinen JH [r, Dabbs GH, Mason HA: The experimental production of ectopic cartigrafting. Plast Reconstr Surg 61:1-6, 1978 5. OIlier L: De la production artificielle lage and bone in the muscles of rabbits. J des os au moyen de la transplantation du perBone Joint Surg (Am) 31:765-771, 1949 1. Canalis RF, Saffouri M, Mirra J, et al:
ACKNOWLEDGMENTS -
The authors wish to thank Dr. Juan Lechago for his valuable help
in the preparation and interpretation of the histological material and to Ms. Tatiana Astroza for her assistance in the preparation of this manuscript.
REPRINTS - Rinaldo F. Canalis, MD, Division of Head and Neck Surgery, Harbor General Hospital, 1000 West Carson St., Torrance, CA 90509.
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
ROLE OF PERIOSTEUM ON THE FATE OF PEDICLE OSTEOCUTANEOUS GRAFTS lliNALDO
F.
CANALIS,
MD
TORRANCE, CALIFORNIA WILLIA...'\1
G.
HEMENWAY,
MD
PAUL
Los ANGELES, CALIFORNIA
H. WARD, MD
Los ANGELES, CALIFORNIA
Recent studies on the fate of pedicle osteocutaneous grafts have shown that they remain viable and may be actively involved in the mechanics of bone repair. This communication reports on a series of experiments aimed to clarify the role of periosteum in the survival of pedicle-assisted bone grafts. Osteocutaneous grafts were developed in dogs in such a manner as to isolate the implant from normal recipient bone. Free bone grafts were used as controls and a group of pedicle periosteal grafts were studied as potential sources of bone formation. Specimens were evaluated at regular intervals over a 40-week period. The pedicle bone grafts maintained their viability and developed vigorous osteoneogenesis. The process was progressive and eventually resulted in partial substitution of the original graft by new bone of periosteal origin. The free bone grafts were resorbed and no bone formation was obtained in pedicle periosteum specimens. The study provides clear evidence that under experimental conditions no bone contact is needed to maintain the viability of pedicle osteocutaneous grafts. It also shows that the periosteum has the leading role in the restructuring process of these grafts.
Recently the authors reported on a series of experiments aimed towards a clearer understanding of the fate of pedicle osteocutaneous grafts.' This study, together with the results of clinical experience," indicates that these grafts not only survive but participate actively in bone repair. The present communication discusses the results of a group of experiments devised to gain further insight into two aspects of this process remaining obscure: 1) the extent of recipient bone participation in structural repair and 2) the degree of periosteal involvement in this activity. In addition, the possibility of utilizing vascularized periosteum as a potential source of bone formation was also explored. METHODS AND MATERIALS Six adult mongrel dozs weighing between 20 and 25 kg were used. Sodium pentobarbital (600 mg/kg intravenously) and 1% lidocaine hydrochloride with epinephrine (1: 100,000, 10-12 cc subcutaneously) were employed as anesthesia. A forehead flap approximately 4 em wide was raised from the root of the ear to the lateral extent of the anterior wall of the frontal sinus. The forehead skin was incised at the midline and circumferentially around the upper
and lower limits of the sinus. The tissues between the skin and the periosteum covering the anterior wall of the sinus were carefully preserved and an oscillating saw was used to free the ipsilateral half of this wall from the surrounding bone. This waIl was maintained in continuity with the flap by its periosteal attachments (Fig. 1). Following this, the flap was tubed and rotated upwards. Its distal end was sutured to the fascia of the parietal muscle, taking care to immobilize the bone graft upon this structure. On the contralateral side a similar procedure was undertaken, but the distal end of the flap incorporated only the periosteum overlying the anterior frontal table. After tubing and rotating this flap, the periosteum was also sutured to the fascia of the ipsilateral parietal muscle. Finally, the remaining anterior table of the frontal sinus was removed and placed under the skin of the calvarium to be used as a control. Primary closure was accomplished by simple undermining and mobilization of the skin. Postoperatively each animal received benzathine penicillin G (600,000 units intramuscularly) and was allowed a normal diet. Animals were again anesthetized and the specimens removed at 8, 10, 24, 28, 36, and 40 weeks after the operation. Care was taken to include the distal portion of the flap and a generous portion of the parietal muscle underlying the implants. The size and general appearance of the grafts were recorded and the specimens were processed for light microscopy. Hematoxylin and eosin staining was used in all cases. In order to more objectively quantify the
From the Division of Head and Neck Surgery, Department of Surgery, UCLA School Medicine, Los Angeles, California and Harbor General Hospital, Torrance, California.
642
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
ot
OSTEOCUTANEOUS GRAFTS
643
Fig. 1. Forehead flap incorporating the ipsilateral anterior wall of the frontal sinus (G). Arrows mark limit of tubing to be done before rotation. degree of new bone formation in osteocutaneous grafts, equal magnification microphotographs (X60) of each specimen were obtained. Multiple measurements (10 to 12) of the ossification layer developing along the periosteal surface were taken from 5 x 7 prints. These were then averaged, converted into microns and used for comparison. RESULTS
All soft tissue pedicles healed without complications and, upon sectioning, their core showed abundant arterial and venous channels. The pedicle periosteum specimens were grossly unremarkable. Miscroscopically the periosteum could be identified as a fibrous layer of variable thickness devoid of any changes suggesting new bone formation. The pedicle osteocutanous grafts exhibited several interesting findings which are summarized in Table 1. In contrast with free bone grafts which underwent complete resorption, pedicleTABLE 1. RESULTS OF PEDICLE OSTEOCUTANEOUS GRAFTS ISOLATED FROM RECIPIENT BONE
Dog
1 2 3 4 5 6
Time (wks)
Original Graft Size" (mm)
8
23
10
25 23 24 24 24
24 28 36 40
Final Graft Size" (mm)
Osteoneogenesis"" (1-')
23 25 22 24 22 26
15 15 21 22 57 61
·Represents greater diameter. •• Approximate thickness of new bone layer.
Fig. 2. Eight-week specimen. Layer differentiation of spindle-shaped precursor cells (Sp) into osteoblasts (Ob) is clearly evident. The darker (basophilic) line between arrows rel?resents osteoneogenesis (H & E, XI60). Inserts show examples of mitotic activity seen in the periosteal periphery. (X300)
assisted implants retained their original size in most instances. One of the late specimens (40 weeks) showed a slight increase in diameter and thickness. Microscopically, the most striking features of these grafts were the persistence of viable osteocytes and the development of vigorous periosteal osteogenesis. The latter process appeared to be a progressive phenomenon which was most active in the 36- and 40-week specimens and was initially characterized by thickening of the periosteal layer to many times its normal size. Increase in the population of the spindle-shaped osteoprogenitor cells, gradual differentiation of these elements into distinct osteoblasts and profuse vascularization underlined this change (Fig. 2). As in any other form of osteogenesis, the osteoblasts were aligned along newly-deposited osteoid material, and as the process progressed, became incorporated into developing lacunae. Occasionally mitotic activity could be noted in the most peripheral areas (Fig. 2 insert). Early in the process, it became ap-
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
644
CANALIS ET At
Fig. 3. Eight-week specimen. A) Overall view demonstrating thickening (P) and a thin layer of new bone (arrow) overlying the X60). B) Detail of the area enclosed in rectangle. The lacunae of the osteocytes. Arrow points to newly-formed bone. p - Periosteum. (H
parent that newly-deposited bone, characteristically basophilic in aspect, tended to replace the bone graft. This finding, which was initially of modest proportions (Fig. 3), eventually became extremely prominent, and in late specimens, areas of new bone were noted to invade the graft throughout its thickness (Fig. 4). It must be emphasized that periosteal osteogenesis was limited to the surface directly vascularized by the
proximal periosteal graft (g) (H & E, graft are filled with & E, X120)
pedicle. The mucoperiosteal lining of the frontal sinus did not appear to undergo any change during the early phases and it frequently retained its normal pseudostratified ciliated epithelium which was left untouched during the surgical procedure. Eventually, the epithelium disappeared and the periosteum and advancing new bone virtually enveloped the graft by extending into this surface (Fig. 5A). Mature lamellar
Fig. 4. Twenty-four-week specimen demonstrating progression of the changes illustrated in Figure 3. A) Overall view. Area between arrows represents osteoneogenesis (H & E, X60). B) Detail of area enclosed within rectangle showing digitations of new bone invading the graft. Note early lacunar formation (arrows). P - Periosteum. (H & E, X140)
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
OSTEOCUTANEOUS GRAFTS
,
f
645
.....•
"
Fig 5 Thirty-six-week specimen. A) Overall view demonstrating diffuse subs~itu tion of the proximal table of the graft (g); P - Periosteum. (f.I &. E, X60) ..B) Detail of area enclosed within rectangle demonstrating advanced organization of penosteally generated bone. (H & E, X160)
bone with organized haversian canals was present in later specimens (Fig. 5B). Throughout these changes the bone graft, although exhibiting lacunae retaining morphologically n0fl!l~ osteocytes, did not appear t? participate actively in the reparative process. It seemed to provide the scaffold through which osteoneogenesis took place. DISCUSSION
The described experiment provided an excellent model to study the evolution of pedicle osteocutaneous grafts isolated from recipient bone. It must be stressed, however, that some conclusions may not be applicable to bone and bone grafts in general sin.ce. the model.u~ed is somewhat unique IS ItS charactenstics. It is a thin, (1.5 to 2.0 mm), predominantly cortical bone with very broad periosteal attachments, and is supplied by a profusely vascularized flap. In previous experiments,' it was felt that pedicle bone participated actively
in the repair process, but it was assumed that healing necessitated apposition of the graft to healthy recipient bone. This study provides clear evidence that restructuring depends almost entirely on a remarkably active process of periosteal osteogenesis which is, at least tempor-. arily, independent from t~e presen~e. of recipient bone. Such periosteal activity may depend on factors similar to those encountered by Judet and Patel" in the treatment of pseudarthrosis with muscle pedicle bone grafts. These investigators demonstrated that bridging of bony defects was drastically enhanced, even in the presence of infection, by using bone chips attached to vascularized periosteum. The vascular dependency of this process is demonstrate.d.in th~ describ~d experiments by the strikmg difference m bone production existing between the pedicle pole of the graft and its mucoperiosteal side. It is also corroborated by the investigators' previous work with tetracycline-labeled specimens, th~t showed intense fluorescence on the penosteal side of similar grafts.'
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
646
CANALIS ET AL
Periosteal activity increases through time and eventually results in replacement of the bone graft. This process of substitution was slow, since even after 40 weeks it remained incomplete, and it may be a function of the relatively small blood supply of these grafts. Another retarding factor may be related to the viability of the bone graft itself. In most instances of bone replacement, osteoclastic activity has to contend with devitalized bone which undoubtedly facilitates resorption. In this experiment, maintenance of the normal organization of bone may actually hinder the process of breakdown and substitution. Recently the possibility of stimulating periosteum to produce bone by maintaining its vascularization was demonstrated by Finley et al.' These investigators were able to reconstruct a portion of a dog's tibia by bridging it with costal periosteum vascularized by microanastomosis to the tibial artery and saphenous vein. Their subsequent attempts to bridge defects in the head and neck failed and it was assumed that lack of mechanical stress prevented bone formation. Our results do not support this thesis since, in the osteocutaneous grafts which were totally stress-free, the leading activity was periosteal osteogenesis. The various factors determining bone production by periosteal grafts are not completely understood. Among the causes of failure acting in our series, the age. animal species and status of the cambium layer are likely to be impor-
tant. Since allier's classic work," osteogenesis by periosteal grafts has been less successful in adult dogs than in any other experimental animal. Riess" has shown that in dogs younger than eight months, with an intact cambium layer, bone production may be obtained consistently, the opposite being true for older animals. A factor common to many experiments in which bone formation is obtained, is the presence of sectioned or fractured bone. For several decades the presence of an osteogenic factor liberated by devitalized bone has been implicated in osteogenesis," This "inductor substance" could be responsible for the process leading to callous formation, bone resurfacing, and for the development of bone under abnormal conditions. The existence of such substance has a histological basis in the demonstration of primitive connective tissue cells changing into osteoblasts while still distant from areas of active new bone formation." Additional indirect evidence is found in the many instances of ectopic ossification" and in the osteogenic process of the grafts described here. The results discussed open several areas of investigation that may clarify certain aspects of bone graft behavior and perhaps result in the availability of new clinical methods. The possibility of producing bone from a malleable soft tissue source could offer a solution to many reconstructive problems of the head and neck and merits further study.
REFERENCES ioste desgreffes osseuses. Gaz Med (Paris) 14: The fate of osteocutanous grafts in mandibulo- 212-233, 1859 facial restoration. Laryngoscope 87 :895-908, 6. Riess E: Experimentelle Studien uber 1977 dies knochenbielden de Kraft des Periostes. 2. Ward PH, Canalis RF, Fee W, et al: Arch Klin Chir 129:750-756, 1924 Composite hyoid sternohyoid muscle graft in 7. Young R"V: Cell proliferation and spehumans. Arch Otolaryngol 103:531-534, 1977 cialization during endochondral osteogenesis 3. [udet R, Patel A: Muscle pedicle bone in young rats. J Cell BioI 14:357-361, 1962 grafting of long bones by osteoperiosteal de8. Bloom W Bloom MD McLean FC: cortication. Clin Orthop 87:74-80, 1972 Calcification and' ossification: Medullary bone 4. Finley JM, Acland RD, Wood MB: Re- changes in the reproductive cycle of female vascularized periosteal grafts. A new method pigeons. Anat Rec 81:443-450, 1941 to p~oduce functional new bone without bone 9. Heinen JH [r, Dabbs GH, Mason HA: The experimental production of ectopic cartigrafting. Plast Reconstr Surg 61:1-6, 1978 5. OIlier L: De la production artificielle lage and bone in the muscles of rabbits. J des os au moyen de la transplantation du perBone Joint Surg (Am) 31:765-771, 1949 1. Canalis RF, Saffouri M, Mirra J, et al:
ACKNOWLEDGMENTS -
The authors wish to thank Dr. Juan Lechago for his valuable help
in the preparation and interpretation of the histological material and to Ms. Tatiana Astroza for her assistance in the preparation of this manuscript.
REPRINTS - Rinaldo F. Canalis, MD, Division of Head and Neck Surgery, Harbor General Hospital, 1000 West Carson St., Torrance, CA 90509.
Downloaded from aor.sagepub.com at MICHIGAN STATE UNIV LIBRARIES on June 14, 2015
