Histologic and microradiologic comparison of block and particulate cancellous bone and marrow grafts in reconstructed mandibles being considered for dental implant placement

J Oral Maxillofac 54:15-20, 1996

Surg

Histologic and Microradiologic Comparison of Block and Particulate Cancellous Bone and Marrow Grafts in Reconstructed Mandibles Being Considered for Dental Implant Placement TATSUO MASAYUKI

SHIROTA, DDS, PHD,* KOHSUKE OHNO, DDS, PHD,t MOTOHASHI, DDS,$ AND KEN-ICHI MICHI, DDS, PHD§

Purpose: Patterns of healing were investigated in mandibles reconstructed with three different techniques to assess their readiness for implant placement. Patients and Methods: The subjects were 10 patients who had undergone mandibular reconstruction with either nonvascularized iliac block bone grafts (group 1; 3 patients), particulate cancellous bone and marrow (PCBM) grafts (group 2; 3 patients) for mandibular discontinuity, or PCBM grafts for mandibular marginal defects (group 3; 4 patients). Six (groups 2 and 3) or 12 months (group 1) after mandibular reconstruction, bone biopsy specimens were obtained for histologic examination with a trephine bur. As controls, bone specimens were obtained from ungrafted mandibles of patients undergoing dental implant placement. Undecalcified specimens were embedded in polyester resin and examined by routine light microscopy and microradiography. Results: The morphology of the specimens from group 1 was similar to that of group 2, but not to that of the control subjects. However, the morphology of specimens from group 3 was generally similar to that of control subjects. Conclusion: These results suggest that mandibular reconstruction with PCBM grafts allows the placement of dental implants sooner than reconstruction with block bone grafts.

required for anchorage of craniofacial prostheses and is particularly advantageous in situations where large mandibular hard and soft tissue defects were reconstructed with tissue from various donor sites. However, some clinical problems with this approach are well known. For example, there is a risk of infection in the early phase of integration, because the graft cannot be sufficiently protected by antibiotic agents.7 Furthermore, there is a risk of delayed healing with possible fibrous encapsulation of the implants.8,9 Thus, proper timing of implant placement after mandibular reconstruction is essential for success. In general, mandibular reconstruction and implant placement are separated by a 6- to 12-month healing period.3.4.7 There are several basic approaches for reconstruction of the resected mandible with autogenous bone grafts. These approaches include nonvascularized block bone grafts, particulate cancellous bone and mar-

Many clinical successes have shown that placement of dental implants after bone grafting for reconstruction of mandibular defects has become an important component of functional oral rehabilitation after extensive tumor resection.‘.’ The procedure is commonly Received from the School of Dentistry, Showa University, Tokyo, Japan. * Lecturer, First Department of Oral and Maxillofacial Surgery. t Associate Professor, First Department of Oral and Maxillofacial Surgery. $ Postgraduate student. 9 Professor and Chairman, First Department of Oral and Maxillofacial Surgery. Address correspondence and reprint requests to Dr Shirota: First Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, 2-l-l Kitasenzoku Ohta-ku, Tokyo, 145, Japan. 0 1996 American

Association

of Oral and Maxillofacial

Surgeons

0278-2391/96/5401-0004$3.00/O

15

16

MANDIBULAR

Table Case No.

1.

Patient

RECONSTRUCTION

Profiles

Sex (M/F)

Age W

Pathology

Radiation (Gy)

Defect

1

F

70

see

40.0

Block

2

F

62

see

54.0

Block

3

F

73

see

-

Block

4

M

62

see

5

M

56

see

50.0

PCBM

6

F

53

see

24.0

PCBM

7

M

44

see

40.0

PCBM

8

M

49

see

40.0

PCBM

9

F

51

see

40.0

PCBM

10

M

36

Ameloblastoma

Bone-Graft

PCBM

u

PCBM

Abbreviations: SCC, squamous cell carcinoma; Block, block bone graft; PCBM, particulate cancellous bone marrow.

row (PCBM) grafts, and revascularized bone grafts.2~‘~‘3 No technique is universally successful; each has its own physiologic and technical advantages and disadvantages. Although healing after bone grafts has been extensively investigated in experimental models,‘4-‘6 in man the histologic processes involved in healing are not yet clear, and consequently a scientific basis for determining the timing of implantation does not exist. Therefore, we undertook the histologic evaluation of mandibles that had been reconstructed with autogenous iliac bone grafts and for which implant placement was being considered. Patients

and Methods

Ten patients, 5 men and 5 women ranging in age from 36 to 71 years, served as subjects in this study. All patients had undergone surgical resection of the mandible for malignant or benign tumors. In six patients, malignant tumors had been treated with preoperative irradiation. Patient data and extent of the mandibular defects are summarized in Table 1. None of the patients had any sign of tumor recurrence at the time of this study. The surgical defects had been secondarily reconstructed with autogenous bone grafts. The patients were divided into three groups according to the method

of mandibular reconstruction. Group 1 consisted of three patients (patients l-3) who had had a mandibular discontinuity repaired with nonvascularized iliac block bone grafts. Group 2 consisted of three patients (patients 4-6) who had undergone PCBM grafts for reconstrnction of a mandibular discontinuity. Group 3 consisted of four patients (patients 7- 10) who had received PCBM grafts for defects resulting from marginal mandibular resection. The volume of grafted bone required had been estimated by clinical and radiographic examinations and harvested from the iliac crest. Our surgical procedure for the PCBM graft has been described previously.‘7 Briefly, a corticocancellous bone block was divided into two components; PCBM and the ipsilateral cortex, which was used as a crib. After being perforated with bur holes to promote vascular ingrowth, the crib was rigidly fixed to the mandibular segment with a titanium plate, after which the PCBM was densely packed into the defect. All patients who had undergone mandibular reconstruction healed uneventfully. Six months (groups 2 and 3) or 12 months (group 1) after bone transplantation, biopsies of the grafted bone tissue were performed for histologic examination. Samples were taken from the reconstructed sites in the center of the graft with

17

IIROTA ET AL

FIGURE 2. Bone from a control patient. The degree of new bone formation is minimal. Most bone marrow cavities are filled with adipose tissue (toluidine blue stain, original magnification x20).

FIGURE 1. A, Trephine bur used for bone biopsy. B, Biopsy core from a reconstructed mandible.

a 3.0-mm trephine bur (Figs lA, B; Asahi Optical Corporation, Tokyo, Japan). As controls, eight bone specimens were taken from the ungrafted mandibles of four other patients (two men and two women, ages 20 to 60 years) during dental implant placement (control group). Specimens were fixed in 10% neutral formalin, dehydrated, and embedded in polyester resin. Sections 100 pm thick were cut along the long axis of the specimens with an EXAKT cutting machine (EXAKT, Nordstedt, Hamburg, Germany) and ground in an EXAKT grinding machine to 50 prn.18 Prepared sections were placed in direct contact with a high resolution spectroscopic platetype 624-O (Eastman Kodak, Rochester, NY). Microradiography was performed at 15 kV and 19 mA using a machine for contact microradiography (Softex Microradiography CMR Tokugata, Softex, Japan). After contact microradiography, the sections were reground to 15 pm, stained with 1% toluidine blue, and inspected under a microscope (Nikon, Tokyo, Japan).

within the bone did not exhibit any obvious changes. The degree of new bone formation was minimal, and only a few osteoclasts were noted. Most bone marrow cavities were filled with loose connective tissue or adipose tissue (Fig 2). Microradiographic

Findings

Radiolucency was nearly uniform. The crest side of the sample displayed minimal vascular enlargement and a small amount of resorption of the bone lamellae. The inner side had fewer bone lamellae than the crestal side, and a small amount of resorption of the bone surfaces was also seen (Fig 3). GROUP 1: RECONSTRUCTION OF MANDIBULAR DISCONTINUITY WITH ILIAC BONEBLOCKGRAFT

Histologic Findings

Newly formed trabecular bone grew along the surface of the grafted bone and was characterized by the presence of devitalized bone tissue containing empty lacunae. The new bone trabeculae contained numerous

No gross differences in bone healing were observed between specimens from patients who had and had not received preoperative radiotherapy. Examination of biopsy specimens revealed four basic histologic patterns, depending on the type of mandibular bone from which the specimen was taken. CONTROLGROUP:UNGRAFTEDMANDIBULAR BONE TISSUE

Histologic Findings

The biopsy specimens contained numerous mature bone lamellae lined by endosteal cells; blood vessels

FIGURE 3. Microradiograph of bone from a control patient showing nearly uniform radiolucency.

18

MANDIBULAR

FIGURE 4. Bone from a patient in group 1. New bone trabeculae have grown along the grafted bone (toluidine blue stain, original magnification X50).

large lacunae and abundant, strongly stained, osteoid tissue lined by developing osteoblasts. Osteoclasts were noted in some places. The bone marrow consisted of loose connective tissue and blood vessels (Fig 4).

FIGURE 6. Bone biopsy taken from a patient in group 2. New bone has formed on the surface of the grafted bone lamellae (toluidine blue stain, original magnification X50).

dant osteoid tissue with developing osteoblasts. Osteoclasts were seen at some sites. The bone marrow consisted of loose connective tissue and blood vessels. Hemopoetic cells were also noted (Fig 6). Microradiographic

Microradiographic

Findings

Radiolucency of new bone formed around the grafted bone lamellae was greater than that of the grafted bone lamellae itself. The crest side of the samples displayed moderate to excessive enlargement of the vascular canals. The inner side contained a threedimensional network of bone tissue, and the bone marrow cavity had redeveloped (Fig 5). GROUP 2: RECONSTRUCTION OF MANDIBULAR DISCONTINUITY WITH PCBM GRAFT

Histologic

Findings

The bone that had formed on the surface of the grafted bone lamellae was by mature in character and contained distinct osteocytes. The newly formed bone on the surface of the mature bone had numerous large lacunae, and abun-

FIGURE 5. Microradiograph of bone from a patient in group 1. Radiolucency of the new bone is greater than that of the grafted bone.

RECONSTRUCTION

Findings

Radiolucency of the new bone on the surface of grafted bone lamellae was similar to that of the grafted bone. The crestal side of the samples displayed moderate to excessive enlargement of the vascular canals. The inner side contained a three-dimensional network of bone tissue, as was seen in specimens of group 1 (Fig 7). GROUP 3: RECONSTRUCTION OF MARGINAL DEFECT OF THE MANDIBLE WITH PCBM GRAM

Histologic

Findings

The specimens contained numerous mature bone lamellae. New bone formation on the surface of the la-

FIGURE 7. Microradiograph of the same area as in Figure 6. Radiolucency of the new bone is similar to that of the grafted bone. (original magnification X50).

SHIROTA

ET AL

mellar bone was minimal. Most of the lamellar bone was lined by endosteal cells, as was seen in the control specimens. A few osteoclasts were noted. Most of the bone marrow consisted of loose connective tissue and blood vessels. Hemopoetic cells were also seen in some sites (Fig 8). Microradiographic

Findings

Radiolucency of various bone tissues was nearly uniform. Some highly radiolucent concentric lamellae were seen. The crest side of the sample displayed a minimal to moderate degree of vascular enlargement and slight resorption of bone lamellae. On the inner side, the bone marrow cavity had reformed (Fig 9). Discussion In the present study different types of bone grafts were characterized by different patterns of graft incorporation and remodeling. On the basis of histologic and microradiographic findings, the stage of healing in group 2 was similar to that in group 1, although bone biopsies after mandibular reconstruction of group 2 were performed 6 months before those of group 1. Therefore, healing after reconstruction of mandibular discontinuity with PCBM grafts occurs significantly earlier than that with block bone grafts. Such a degree of osteogenetic activity after a PCBM graft may reflect the transplantation of sufficient numbers of endosteal osteoblasts and marrow mesenchymal cells capable of bone induction.‘5.‘9 Biopsy specimens of both groups contained numerous grafted bone trabeculae that were surrounded by newly formed immature bone. Bone resorption was also seen in some places, and the bone marrow cavity was filled with loose connective tissue and reestablished blood vessels. The findings in groups 1 and 2

FIGURE 9. Microradiograph of the same area as in Figure 8. Radiolucency of the various bone tissues are nearly uniform (original magnification X50).

differed greatly from those in the control group and indicate that both groups 1 and 2 were in the middle stage of their postgraft remodeling process. It was evident that bone formation and vascularization was in an active stage. These conditions are associated with a small risk of contamination, fibrous encapsulation, and other events that could contribute to failure. The morphology of specimens from group 3 was generally similar to that of the control group, although bone biopsies were performed 6 months after bone grafting. The degree of healing in group 3 was equivalent to the end stage of the remodeling process after bone grafting, in part because the PCBM graft had been placed into a smaller defect. These results suggest the possibility of earlier placement of implants into the graft in group 3 than in other groups. Variations in individual patient characteristics, amount of overlying soft tissue, presence of internal fixation and immobilization, graft materials, and size of the mandibular defects do not permit definitive conclusions to be drawn. However, the findings of this study suggest that PCBM demonstrates greater osteogenic activity after bone grafting. Although further longitudinal studies are needed to evaluate implant prognosis, mandibular reconstruction with PCBM grafts might allow placement of dental implants more than 6 months earlier than with block bone grafts. References

FIGURE 8. Bone biopsy taken from a patient in group 3. A, Most of the lamellar bone is lined by endosteal cells, as in the control specimens (toluidine blue stain, original magnification x50).

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