A comparative analysis of the microarchitecture of cortical membranous and cortical endochondral onlay bone grafts in the craniofacial skeleton

Previous work in this laboratory established that an onlay bone graft's survival is determined primarily by its relative cortical and cancellous composition rather than its embryologic origin. A volumetric analysis of external bone graft resorption, however, does not explain the internal microarchitectural changes that may be occurring as these grafts become incorporated. To expand the knowledge of bone graft dynamics beyond volumetric parameters, a better understanding of the internal processes of bone graft remodeling is needed. In this comparative study of cortical onlay bone graft microarchitecture, the authors propose to show that cortical onlay bone grafts undergo measurable internal microarchitectural changes as they become incorporated into the surrounding craniofacial skeleton. In addition, the authors propose to further demonstrate similarities between the internal microarchitecture of cortical onlay bone grafts of different embryologic origin over time. Twenty-five adult New Zealand White rabbits were used for this study. They were divided into two groups of eight animals and one group of nine. The groups were killed at 3, 8, and 16 weeks. Cortical membranous and endochondral bone grafts were placed subperiosteally onto each rabbit's cranium. In addition, five ungrafted cortical endochondral and membranous bone specimens were used as controls. Microcomputed tomography (MCT) scanning and histomorphometric analysis were performed on all of the specimens to obtain detailed information regarding the microarchitecture of the cortical bone grafts. The parameters of bone volume fraction, bone surface area to volume, mean trabecular number, and anisotropy were used to give quantitative information about a bone's micro-organization. The results showed that there is no statistically significant difference between the cortical endochondral and the cortical membranous bone grafts for bone volume fraction, bone surface to volume, mean trabecular number, and anisotropy measurements for all time points. There were, however, statistically significant differences when comparing the control and 3-week groups to the 16-week group for all parameters. The advanced MCT technology and histomorphometric techniques proved to be effective in providing a qualitative and quantitative ultrastructural comparison of cortical endochondral and membranous onlay bone grafts over time. In this study, a statistically significant change in the internal microarchitecture of cortical onlay bone grafts of different embryologic origins was seen as they were remodeled and resorbed at all time points. Specifically, the onlay cortical bone grafts developed a less dense, more trabecular, and less organized internal ultrastructure. In addition, no difference in the three-dimensional ultrastructure of cortical endochondral and membranous bone was found. These results challenge some of the currently accepted theories of bone-graft dynamics and may eventually lead to a change in the way clinicians approach bone-graft selection for craniofacial surgery.     

Growth potential in suture bone inlay grafts: a comparison of vascularized and free calvarial bone grafts

The present study investigates transsutural growth in vascularized and free calvarial bone grafts and notes the effects of such growth on craniofacial development. The temporalis myoosseous flap served as a model of vascularized graft. In ten 8-week-old dogs, a standardized skeletal defect, including a segment of the zygomatico-maxillary suture, was created. The defect was reconstructed with a vascularized graft in half the animals and a corresponding free graft in the remaining animals. Growth was assessed by means of serial cephalometric radiography and direct osteometry. Vascularized bone grafts demonstrated persistent transsutural growth following transplantation. Growth at the recipient site was preserved, resulting in less restriction of vertical maxillary development.     

Elastic properties of external cortical bone in the craniofacial skeleton of the rhesus monkey

Knowledge of elastic properties and of their variation in the cortical bone of the craniofacial skeleton is indispensable for creating accurate finite-element models to explore the biomechanics and adaptation of the skull in primates. In this study, we measured elastic properties of the external cortex of the rhesus monkey craniofacial skeleton, using an ultrasonic technique. Twenty-eight cylindrical cortical specimens were removed from each of six craniofacial skeletons of adult Macaca mulatta. Thickness, density, and a set of longitudinal and transverse ultrasonic velocities were measured on each specimen to allow calculation of the elastic properties in three dimensions, according to equations derived from Newton's second law and Hooke's law. The axes of maximum stiffness were determined by fitting longitudinal velocities measured along the perimeter of each cortical specimen to a sinusoidal function. Results showed significant differences in elastic properties between different functional areas of the rhesus cranium, and that many sites have a consistent orientation of maximum stiffness among specimens. Overall, the cortical bones of the rhesus monkey skull can be modeled as orthotropic in many regions, and as transversely isotropic in some regions, e.g., the supraorbital region. There are differences from human crania, suggesting that structural differences in skeletal form relate to differences in cortical material properties across species. These differences also suggest that we require more comparative data on elastic properties in primate craniofacial skeletons to explore effectively the functional significance of these differences, especially when these differences are elucidated through modeling approaches, such as finite-element modeling.     

Distraction osteogenesis of the craniofacial skeleton

Distraction osteogenesis is becoming the treatment of choice for the surgical correction of hypoplasias of the craniofacial skeleton. Its principle is based on the studies of Ilizarov, who showed that osteogenesis can be induced if bone is expanded (distracted) along its long axis at the rate of 1 mm per day. This process induces new bone formation along the vector of pull without requiring the use of a bone graft. The technique also provides the added benefit of expanding the overlying soft tissues, which are frequently deficient in these patients. This article reviews the authors' 11-year clinical and research experience with mandibular distraction osteogenesis. It highlights the indications and contraindications of the technique and emphasizes the critical role that basic science research has played in its evolution.     

Distraction osteogenesis of the craniofacial skeleton

In summary, distraction osteogenesis is a safe and effective means of achieving bone lengthening. These techniques were originally applied to the long bones of the extremities; over the past 10 years they have been effectively applied to the bones of the craniofacial skeleton. The new bone regenerate that is observed after distraction osteogenesis is stable, and relapse rates after skeletal advancement are believed to be lower than with conventional osteotomy and bone graft techniques. There is considerable variability in distraction protocols employed in clinical practice, including differences in the types of devices used and in the rate, rhythm, latency, and period of consolidation for distraction osteogenesis. The greatest application for distraction osteogenesis in the craniofacial skeleton has been with mandible lengthening, for which there is presently a 10-year clinical experience. Midfacial advancement is a newer application of distraction osteogenesis, for which clinical experience has been accrued over the past 5 years. This latter experience indicates that distraction osteogenesis is a viable treatment option for lengthening of the hypoplastic mandible and midface. These techniques have advantages over conventional means of bone graft and rigid fixation because of the quality of the bone regenerate, the decrease in the long-term relapse rate of the advanced bone segments in both the mandible and the midface, and the simultaneous soft-tissue elongation that accompanies the distraction process. Distraction osteogenesis is particularly applicable to the correction of severe deformities of the mandible and midface in children with developmental hypoplasia and syndromic craniosynostosis. However, growth is an added variable in this patient population. The amount of overcorrection in lengthening of the hypoplastic bone required to compensate for continued growth discrepancy of the adjacent facial bones is difficult to predict. Therefore, the families of these patients should be informed that many children will require repeated operations at a later age as they reach skeletal maturity.     

Temporal fossa bone grafts: a new technique in craniofacial surgery

The calvarium has become an increasingly popular bone-graft donor site. Previously described harvesting techniques are often difficult to perform and may produce unsatisfactory bone fragments. However, full-thickness bone grafts taken from the region of the temporal fossa, beneath the temporaiis muscle, have proven to be of high quality and technically easy to obtain. In our experience with eight patients, temporal fossa bone grafts were used primarily around the orbit, including reconstruction of the orbital floor, frontal bone, and zygoma. The procedure begins with a hemicoronal or bicoronal incision; the temporalis muscle is reflected, and an underlying bone plate up to 4 X 6 cm is removed. The resulting bone graft is consistently 3 to 4 mm in thickness. The cranial defect is packed with bone debris, and the muscle is replaced. This technique has proven to be safe, technically simple, consistently productive of high-quality bone grafts, and within discernible donor-site deformity.     

Blood supply of the upper craniofacial skeleton: the search for composite calvarial bone flaps

This study investigated the blood supply of the upper craniofacial skeleton by injection studies. The major supply to the calvaria is provided by the middle meningeal artery and its branches. This vessel is difficult for the plastic surgeon to exploit in composite bone-flap design. The majority of the outer surface of the craniofacial skeleton is supplied by tiny perforators from the overlying periosteum. The vascular interconnections within the periosteum are poorly developed. For this reason, the galea and the overlying vascular network (derived from the superficial temporal, occipital, supraorbital, and supratrochlear vessels) should be left broadly attached to the bone when transferring a vascularized calvarial bone flap. Dissection of the scalp away from this vascular network should be carried out just below the hair follicles. By observing these principles, vascularized calvarial bone can be transferred on the superficial temporal, deep temporal, supraorbital, supratrochlear, or occipital vessels. Details of the use of each are discussed.     

Effect of isolation of periosteum and dura on the healing of rabbit calvarial inlay bone grafts

Little is understood about the role of the recipient site in the revascularization and incorporation of autogenous inlay bone grafts in the craniofacial skeleton. Clinical experience demonstrates that secondary complex cranial vault reconstruction performed with scarred avascular dura or poor soft-tissue coverage may undergo significant resorption, thus compromising the aesthetic outcome. This study was designed to determine the effect of isolating autogenous orthotopic inlay calvarial bone grafts from the surrounding dura and/or periosteum on graft revascularization, healing, and volume maintenance in the adult rabbit. Adult rabbits were randomized into four groups (n = 10 per group); in each rabbit, the authors created a circular, 15-mm in diameter, full-thickness cranial defect followed by reconstruction with an autogenous calvarial bone graft, which was replaced orthotopically and held with microplate fixation. Silicone sheeting (0.5 mm thickness) was used to isolate the dura (group II), the periosteum (group II), or both dura and periosteum (group IV) from the graft interface. No silicone was placed in group I. Animals were killed 10 weeks postoperatively, and calvaria were harvested to assess graft surface area, morphology, quantitative histology, fluorochrome staining, and revascularization. Grafts isolated from both the dura and periosteum exhibited significant decreases in total bone (cortical and trabecular) surface area, blood vessel count, and interface healing compared with nonisolated control grafts. Isolation of either the dura or periosteum significantly (p < 0.05) decreased blood vessel count but had no significant effect on interface healing. Isolation of the dura alone was associated with a significant (p < 0.05) decrease in graft cross-sectional surface area and dural cortical thickness compared with nonisolated control grafts, but this effect was not observed when the periosteum alone was isolated. Quantitative histology performed 10 weeks after surgery indicated that graft isolation was associated with increased marrow fibrosis and necrosis compared with nonisolated controls; it also demonstrated evidence of increased activity in bone remodeling (osteoblast and osteocyte count, new trabecular bone, and surface resorption). Triple fluorochrome staining suggested increased bone turnover in the nonisolated grafts compared with isolated grafts at 1 and 5 weeks postoperatively. This study demonstrates that isolating a rabbit calvarial inlay autogenous bone graft from the dura and/or periosteum results in significantly (p < 0.05) decreased revascularization, interface healing, and cross-sectional areas of amount of mature bone compared with nonisolated control grafts 10 weeks after surgery. At this time point, histologic examination demonstrates a paradoxical increase in bone remodeling in isolated bone grafts compared with controls. It is possible that the inhibition of revascularization results in a delayed onset of the remodeling phase of graft incorporation. However, in the model studied, it is not known whether the quantitative histologic and morphometric parameters measured in these isolated grafts exhibit a "catch-up" phenomenon at time points beyond 10 weeks after surgery. The results of this study emphasize the importance of a healthy recipient site in the healing and incorporation of calvarial bone grafts but stress the need for further investigation at later time points.     

New biomaterials and methods for craniofacial bone defect: chondroid bone grafts in maxillary alveolar clefts

The purpose of this study was to evaluate autogenous osteogenic marrow within chondroid bone grafts in simulated alveolar defects of mice in order to determine the ability of the graft material to effectively close the cleft from an osseous standpoint and to observe the effect of the grafting procedure. Critical-sized defects were made in the premaxillary bones of male mice using a surgical trephine and a low-speed dental engine as a model of the maxillary alveolar cleft for testing bone-inductive agents. Premaxillary trephine defects were not repaired by fibrous tissue or bone formation 30 days after operation. This nonhealing bony wound of the premaxilla in mice may be useful as a model for studying the effect of bone-inductive agents on the healing of alveolar clefts. Distraction osteogenesis is a recently advanced principle of bone lengthening in which a long bone separated by osteotomy is subjected to slow progressive distraction using an external fixation device. The osteotomy site was surrounded by an external callus consisting of hyaline cartilage. The callus contained a lot of chondroid bone. The transplant bone within chondroid bone was characterized by bone formation and remodeling 30 days after transplantation. Throughout the experiment, our findings demonstrated, for the first time, that the transplant bone that contains chondroid bone may be used clinically in relation to craniofacial bone defects to improve the treatment of bone grafts.     

The craniofacial skeleton in anencephalic human fetuses. III. Facial skeleton.

A sample of 12 anencephalic fetuses with gestational ages ranging from 26 to 40 weeks and exhibiting varying degrees of severity of the dorsal cranial defect was compared to three normal fetuses of comparable gestational ages with regard to the morphology and positional relationships of the maxillofacial skeletal complex. Gross dissection, alizarin red S staining, radiographs, cephalometric tracings, and histologic techniques were utilized. It was found that some facial bones were severely affected in morphology, size, spatial and angular relationships. The manner in which these were altered suggests that their morphogenesis is an adaptation to the primary defect of the neurocranium.     

The role of rigid skeletal fixation in bone-graft augmentation of the craniofacial skeleton

The type of fixation (rigid skeletal vs. wire) was assessed against embryologic origin (membranous vs. endochondral) and recipient site (depository vs. resorptive) as variables affecting inlay and onlay bone-graft survival in 20 mature dogs. Wet weight and volume measurements were made at operation and at sacrifice (16 weeks). The results were as follows: (1) Rigid skeletal fixation increased bone-graft volume survival over wire fixation (p less than 0.05). (2) Fixation (i.e., rigid skeletal) and embryologic origin (i.e., membranous) were equal determinants of bone-graft volume survival (p less than 0.001); the recipient site was not significant for onlay bone graft survival. (3) Embryologic origin was the only significant determinant of weight survival (p less than 0.001). (4) Inlay bone grafts demonstrated greater weight and volume survival than onlay bone grafts (p less than 0.05). (5) Histologic and microradiographic studies demonstrated bony union of bone grafts fixed with rigid skeletal fixation, while fibrous union predominated in bone grafts fixed with wire technique.     

Patterns of covariation in the hominoid craniofacial skeleton: implications for paleoanthropological models

Living species are often used as analogues for fossil ones. When this is done, the implicit assumption is made that hominids and living hominoids vary in the same way. This paper addresses the validity of this assumption by comparing patterns of facial variation among humans and African apes. In particular, it addresses three major questions that underlie approaches to reconstructing hominid relationships. First, is phenotypic variation similar between closely related species? Second, if it is dissimilar, why? Third, is it feasible to use analogue species for modeling purposes? Measurements are obtained from 542 crania of adult apes and humans. Care is taken to choose homologous data, and account for differences in population size and structure. Variance/covariance and correlation matrices among the species are compared using common principal component (CPC) analysis, random skewers methods and matrix correlations. Morphological distances (D(2)) are calculated between population means, and between randomized pairs of individuals within each population, to evaluate intraspecific variation. Morphological distances are also calculated between randomized pairs of individuals using the variation patterns of analogue populations, in order to evaluate the efficacy of such substitutions. Results show that while the hominoids share a similar pattern of facial variation overall, the patterns do diverge. This difference generally corresponds to the phylogenetic relationships among these species, suggesting that patterns of variation may have diverged through time in the large bodied hominoids. Because interpretation of relationships in the fossil record is confounded by a lack of understanding of how variation changes through time, exploration of such patterns of divergence can provide important clues to understanding human evolution. Additionally, neglecting to account for this divergence when using living analogues as variation "yardsticks" can give rise to interpretations of the fossil record that are more speciose than is warranted.     

Mechanical structure and function of the craniofacial skeleton of the domestic dog.

Masticatory habit is a major factor determining the morphology of the craniofacial skeleton. The craniofacial skeleton essentially comprises a series of bony stress-bearing bridges forming a structural framework. The structural framework of the skull of dog has been described as a rigid trestle-like structure; it can be illustrated by mechanically removing nonresistant areas of bone. It is then found that a framework is produced which is partially rigid (cranium) and partly flexible (rostrum). It is postulated that the flexibility of the rostrum acts to absorb shock and it is suggested that the primate postorbital bar is developed in response to craniofacial morphology which increases compressive bite forces.     

Nasal reconstruction with full-thickness cranial bone grafts and rigid internal skeleton fixation through a coronal incision

The use of iliac and rib bone as onlay grafts to the nasal dorsum often fails because endochondral grafts resorb unpredictably. Membranous cranial bone grafts are less likely to resorb, especially when used with rigid internal fixation techniques. However, when split, they are often too thin and can be difficult to contour. Full-thickness cranial bone grafts were used to achieve nasal augmentation in 26 patients with end-stage nasal skeleton deficiency. All procedures were carried out using only a coronal incision. Grafts were harvested through a craniotomy, carved meticulously, and secured rigidly with miniplates or bicortical screws. Donor sites were reconstructed with split cranial grafts, leaving an intact cranial vault. No graft was lost to infection, and there was no significant donor-site morbidity. In carefully selected patients this method of full-thickness cranial bone graft reconstruction yields good results.     

Age-related changes of the craniofacial skeleton: an anthropometric and histologic analysis.

With the development of increasingly sophisticated methods for the alteration of bony facial form consequent to age, it is imperative that the surgeon have a fundamental knowledge of the age-related changes the skeleton may undergo. To understand these changes better, a detailed anthropometric and histomorphic analysis of the craniofacial skeleton as a function of age was undertaken. The study consisted of a detailed craniometric analysis of 160 skulls selected randomly from a Caucasian population of skeletal remains totaling 1500 specimens. Additionally, a histologic analysis of the supraorbital ridge in a separate preserved cadaver population was performed. Although the results showed individual variation as expected, definite changes in craniofacial morphology were observed. These included (1) appreciable reduction of facial height, most marked in the maxilla and mandible, and strongly correlated with loss of teeth, (2) modest increase in facial width, (3) modest increase in facial depth, except in those regions associated with tooth loss, and (4) general coarsening of bony prominences. Histomorphic analysis demonstrated increasing porosity with age, more marked in the female population. Although these changes represent population trends, in any given patient, any or all of them may be present to varying degrees. Surgeons should be aware of these possibilities and consider selective alterations of the skeletal foundation, either separately or in concert with the overlying soft-tissue envelope, in order to optimize the results of surgery for the aging face.     

The craniofacial skeleton in anencephalic human fetuses. II. Calvarium.

A detailed study of the calvarium of twelve anencephalic and four normal human fetuses 26 to 40 weeks gestational age using gross dissection, alizarin red S staining, silver nitrate radiography and histology revealed dramatic alterations in the presence, form, location and relationship of the individual bones. In the larger dorsal cranial defects the interparietal portions of the occipital bone were relocated anteriorly to approximate the frontal bone. The occipital components were rotated anterolaterally and inferiorly with lack of fusion of the chondrocranium posterior to the foramen magnum. The squamae of the frontal bone were collapsed horizontally and reduced in size to lie peripheral to the anterior cranial fossa forming most of the orbital roofs. In anencephaly the bones derived from the chondrocranium were not as severely affected morphologically as those derived from the neurocranium. The sutures were narrow and smooth instead of wide and serrated as in the normally developing calvarium. In general the degree of maldevelopment was proportional to the extent of the dorsal cranial defect in anencephaly.     

The craniofacial skeleton in anencephalic human fetuses. I. Cranial floor

Twelve anencephalic and four normal fetuses 26 to 40 weeks gestational age were compared by anatomic, radiographic and histologic methods in order to gain information concerning morphogenesis. In the anencephalics, alterations located within the body of the sphenoid bone led to a reduced cranial floor angle and a more vertical clivus. The reduced lateral extension of the lesser and greater wings of the sphenoid constricted the anterior and middle cranial fossae respectively. The posterior cranial fossa tended to have an increased transverse dimension related to the supraoccipital and exoccipital bone orientation. The increased anterior and inferior position of the lateral end of the petrous temporal ridge was positively correlated with the degree of dorsal schisis in the anencephalics. Alterations in the size, form, or duration of the neural functional matrix are suggested as the cause of changes in the cranial floor.