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Grafted periosteum is known to have potential for heterotopic bone formation by endochondral ossification. Although osteochondrogenic cells have been thought to originate from the osteogenic layer in grafted periosteum, no histological report has yet demonstrated this. The present study was designed to elucidate the origin of chondrogenesis preceding bone formation in grafted periosteum. Periostea harvested from young Japanese white rabbits' tibiae were grafted into suprahyoid muscles and examined radiographically and histologically at postoperative days 1, 7, 9, 14, 21, and 35. Normal periostea and tibial graft site were also examined. Surgical harvesting of the periosteum split and damaged its osteogenic layer but retained the fibrous layer intact. Most of the osteoblasts remained on the tibial bone surface, and only few cells of the osteogenic layer were present in grafted tissue. By the seventh day after grafting, the fibrous layer had thickened. The fibroblastic cells in the fibrous layer had significantly increased in number (P Ͻ 0.01) and were positively stained for proliferating cell nuclear antigen. These cells exhibited alkaline phosphatase activity at day 9. The differentiated chondrocytes had formed cartilage at postoperative day 14. Cells in the osteogenic layer appeared necrotic and subsequently disappeared. Following postoperative day 21, cartilage was replaced by trabecular bone. Bone formation was completed by 35 days. An X-ray analysis at this time also revealed new bone formation. These findings indicate that grafted periosteum forms bone by endochondral ossification and that the cells of the fibrous layer play essential roles in chondrogenesis that precedes such bone formation. Anat Rec 264: 348 -357, 2001.

Repair of bone defects remains a major concern in plastic and maxillofacial surgery. Based on modern concepts of tissue engineering, periosteum has gained attention as a suitable osteogenic material. We tested the hypothesis that surgically released and immediately repositioned periosteum would exhibit high osteogenic capacity upon grafting in a rat calvarial defect. Seven days after periosteum was released from the tibia and immediately repositioned, the "primed periosteum graft" (PPG; n = 15) was placed into a critical-sized defect of rat calvaria and the process of bone formation was evaluated histologically, immunohistologically, and radiographically at 7, 14, and 21 days after grafting. Findings were compared with a nonprimed periosteal graft (NPG; n = 15). Endochondral ossification was observed in both the PPG and NPG. The PPG showed higher expression of proliferative cell nuclear antigen, bone morphogenetic protein, and vascular endothelial growth factor than the NPG. Three-dimensional radiographic examination revealed significantly increased bone formation in the PPG than in the NPG (P < 0.01). These findings suggested that surgical stimulation of the periosteum enhanced the osteogenic potential of periosteal cells. This method may be suitable for the clinical repair of bone defects.

Periosteum covers the bone surface and displays the potential to initiate bone formation, after injury to the bone. Numerous studies have demonstrated that the periosteum plays major roles in the healing process after bone fracture. Some reports have described that in the healing of long bone fractures, the periosteum forms new bone by intramembranous and endochondral ossification. Other researchers insist that healing of defects in membrane bone shows bone formation by intramembranous ossification. However, previous studies have not been able to clarify differences in bone formation patterns. We hypothesized that differences in bone formation pattern are associated with the periosteal potential for cell differentiation. The present study grafted periosteum, harvested from the tibia and calvaria, into the suprahyoid muscle, with the aim of interrupting release of factors from bone matrix. Bone formation, after grafting periosteum, harvested from the tibia and calvaria, was examined histologically and radiographically. Grafted tibial periosteum formed a large area of new bone by intramembranous and endochondral ossification, while grafted calvarial periosteum displayed intramembranous ossification. Grafted tibial periosteum formed a larger area of bone than grafted calvarial periosteum. Patterns of cell differentiation thus differ between grafted periosteum, harvested from the tibia and calvaria.

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