Dr. Froum's Articles

Osseous Autografts
I. Clinical Responses to Bone Blend or Hip Marrow Grafts
by S. J. FROUM, R. THALER, I. W. SCOPP, S. S. STAHL
A PRIMARY GOAL of periodontal therapy is the restoration of lost periodontium destroyed by periodontal disease. Various graft materials1-17 have been used in the treatment of infrabony deformities. Currently, two such graft materials, autogenous iliac marrow-cancellous bone18-22 and osseous coagulum-bone blend,23-25 have been reported to give highly favorable results. Histological evidence in animal and human studies,26-29 using autogenous iliac marrow and cancellous bone suggested possible potentiation of regeneration and reattachment with the use of these materials. Animal30-32 and human studies 25, 33, 34 using autogenous intraoral graft material have supported clinical reports of regeneration of the periodontium.
The purpose of the present investigation was to clinically evaluate and compare regeneration following implantation of either osseous coagulum-bone blend obtained from intraoral sources or autogenous marrow-cancellous bone obtained from the posterior iliac crest.
MATERIALS AND METHODS
A total of 32 transplants were performed in 15 males, 23 to 64 years of age, each of whom consented to take part in this study. Twenty-five sites were treated with osseous coagulum-bone blend from intraoral sources, while seven sites were treated with frozen marrow-cancellous bone from the posterior iliac crest. Four patients received both marrow and bone blend implants in different sites.
All patients selected for this study were being treated for periodontitis at the New York Veterans Administration Hospital. These patients also suffered from a variety of other diseases (Chart I). Each patient had a complete medical work-up and where necessary, medical clearance was obtained. Pre-operative treatment, in all cases, consisted of oral hygiene instruction, adjustment for occlusal interferences, root planing, and curettage. Temporary splinting was employed where tooth mobility exceeded class II (Miller classification).35
Periodontic Section, Denial Service, New York Veterans Administration Hospital and the Department of Periodontics, College of Dentistry at the Brookdale Dental Center of New York, University, New York, New York.
After initial therapy, clinical and radiographic evaluations were used to determine whether surgery was necessary to eliminate the defect. An oral hygiene index (OHI-S)36 was utilized during initial treatment. Only when the index approached zero was surgery considered. Prior to surgery, periodontal conditions at the surgical site and other pertinent pre-surgical information were recorded on a specially prepared data sheet (Chart 11).

Surgical Procedures
In all cases, an inverse bevel lull thickness, mucoperiosteal flap was reflected. An effort was made to retain the marginal gingiva to ensure maximum soft tissue coverage of the graft material. Site preparation consisted of removal of chronically inflammed tissue from the osseous defects and root planing to remove root accretions. Following debridement, the donor material was prepared for insertion.
Intraoral donor sites used were tuberosities, edentulous ridges, and extraction sites. Graft material was removed with a rongeur. The spicules of cancellous and cortical bone, with a few drops of blood, were then placed in a sterile capsule, and triturated to obtain a bone blend as described originally by Diem et al.37
Autogenous marrow and cancellous bone was obtained by a punch biopsy from the posterior iliac crest by the Chief of Hematology at the New York Veterans Administration Hospital. The material was stored in Eagle's minimal essential medium in a nitrogen freezer at -79°C for two weeks, then cut into small pieces, and inserted into the defect.
Regardless of the graft material used, all defects were overfilled. Following the graft placement, all patients were put on antibiotic coverage for one week beginning with the day of surgery.
Reentries were performed seven to ten weeks after the initial surgery in 23 out of 25 cases of bone blend implantation. The two remaining cases were reentered at 16 and 22 weeks. Reentries were performed four to seven months after initial surgery in all seven cases of iliac crest implants.
Documentation of Responses
During initial therapy two sets of study models were constructed. An Omnivac stent was then fabricated from 0.10 mm thickness surgical tray material to serve as a fixed reference point.
At the site of the defect, the stents were grooved in an occlusal-apical direction with a no. 556 fissure bur. All measurements were recorded using a no. 50 endodontic silver point inserted into the notch and held by locking pliers with the beaks parallel to the occlusal surface (Fig. 1). A Boley gauge was used to measure the distance to the nearest O.1 mm. All measurements were performed by the same operator to eliminate interexaminer discrepancies. This technique of measurement using fixed distances was tested previously for variance of measurements over a period of time and no statistically significant differences were noted.
At the time of surgical exposure, another notch was cut into the stent which enabled the silver point to be positioned at the deepest point in the defect. The following measurements were recorded:
1. Base of stent to crest of the most coronal wall of defect (Fig. 2).
2. Base of slent to the deepest part of the defect (Fig. 3).
3. Base of stem to cementoenamel junction to cheek for sealing of the stent. In addition, roentgenograms and clinical photographs were taken of the surgical site immediately prior to and during periodontal surgery. Similar measurements, photographs, and roentgenograms were obtained at the time of reentry. At this time the tissues had to appear clinically healed as demonstrated by reduction in (1) pocket depth and (2) clinically evident inflammation.
CHART I. Patient Data

Chart II. Operative Data Chart

                                                 Prior to Implantation                            Prior to Re-entry

RESULTS
Response to Osseous Coagulum-Bone Blend
Osseous coagulum-bone blend was the implant material in 25 infrabony lesions in 14 patients. Among the 25 infrabony lesions were nine one-wall, six two-wall, eight three-wall wide (including one combination two. three-wall defect) and two furcation defects (Chart III). Fill in the one-wall lesions ranged from a loss of 0.8 mm to a gain of 5.3 mm with an average fill of 2.53 mm. Fill in the two-wall lesions ranged from 1.2 to 4.0 mm with an average fill of 3.0 mm. Fill in the three-wall wide lesions ranged from 2 to 6.4 mm with an average fill of 3.64 mm. Fill in the two furcation defects averaged 1.25 mm. Therefore, the total average increase in bone height with the osseous coagulum-bone blend graft material was 2.93 mm while the initial intraosseous depth averaged 4.0 mm. This represents a 73% fill of all defects (Figs. 4 and 5).
Response lo Hip Marrow
Iliac marrow and cancellous bone was utilized as a graft material in seven treatment sites in five patients. Among the seven infrabony lesions were five one-wall, one two-wall and one combination one, two-wall defect. Fill in the one-wall lesions ranged from 1.2 to 9.2 mm with an average fill of 4.3 mm. The fills in the combination one, two-wall defect and the two-wall defect were 5.6 and 3.4 mm. respectively. Therefore, the total average increase in bone height with the hip marrow graft material was 4.36 mm while the intraosseous depth averaged 7.18 mm. This represents a 60.7% average fill of all defects (Fig. 6). A comparison of the above reported repair trends demonstrated that the difference in percentage of fill obtained with the various bone graft materials used was
FIGURE 1. For standardization of measurements, a no. 50 endodontic silver point is inserted into a groove on the Qmnivac stent at the site of the defect. The beaks of the locking pliers unplaced parallel tlo the apical border of the stem.
FIGURE 2. Silver point measuring the distance between the base of the stem and the most coronal wall of the defect.
not statistically significant (t = 1.62. P < 0.05). However, our results suggest that average fill with marrow grafts was less than that obtained with osseous coagulum- bone blend. Furthermore, it is also obvious that marrow grafts were used in deeper defects. Because of these trends we subjected our results to further statistical analysis.
Comparison of Repair Responses in Intraosseous Defects Less or More Than 4 mm in Depth
Table I summarizes the repair trends considering average intraosseous fill in relation to the preoperative osseous depth.
In 15 cases using bone blend (defects less than 4.0 mm) we had an average fill of 2.3 mm, while average fill using marrow (defects less than 4.0 mm) was an identical 2.3 mm. In defects greater than 4.0 mm, the average fill using bone blend was 3.8 mm; using marrow it was 5.9 mm. The difference in osseous fill between marrow and bone blend was not statistically significant at the 0.05 level of confidence.
Table 2 lists the intraosseous depth remaining at the time of reentry. In cases where marrow was used the residual osseous depth ranged from 0 to 3.9 mm. In cases where bone blend was used, residual osseous depth ranged from 0 to 6.6 mm.
Table 3 summarizes the average reentry intraosseous depth in relation lo the preoperative osseous depth.
In cases where the initial intraosseous defect was less than 4.0 mm, the average residual osseous defect was 0.6 mm using marrow, compared to 0.3 mm using bone blend.
The average residual defect where the initial intraosseous depth exceeded 4.0 mm was 1.7 using marrow compared to 1.4 mm using bone blend.
Based on these trends, it appears that similar levels of osseous regeneration apparently took place regardless of graft material used.
FIGURE 3. The silver point is placed into the regrooved stem to measure the distance between the base of the stem and the deepest part of the defect.
Chart III.  Topography of Defect and Graft Material Used

FIGURE 4 A. Preoperative appearance of the osseous defect showing horizontal bone loss, prior lo placement of a bone blend graft. B. Appearance of the detect shown in A at reentry, nine weeks alter initial surgery. Note osseous crestal apposition of lesion.
DISCUSSION
Several comments should be made on the significance of our findings. Case report evidence has been used in reporting our results. Recognizing that different human periodontal defects are seldom identical, we wish to stress that our results represent trends rather than possible universal repair results. However, the results of the present study generally agree with the previous literature20-25 which demonstrates comparable results using either intraoral cancellous bone and marrow or iliac marrow and cancellous bone as an implant material. Theories attempting to explain the role of autogenous implants in regeneration of periodontal osseous defects suggest three possibilities:

1. Both intraoral and iliac autografts have inductive capabilities which induce osseous regeneration.30,32
2. Neither material has "inductive" abilities.
3. The degree of induction may vary with the site and the graft material used.
Although many investigators tend to support the third of the above possibilities.38 our clinical data suggest no significant difference in repair responses. Of further interest is pocket topography in our cases. We classified our defects as one-, two-, three-wall wide defects and a combination of these, following the classic terminology of describing osseous defects.39  Seldom, however, did we find a defect which was purely a "one" or "two" wall defect from its base to the most coronal aspect of the remaining osseous wall. Most defects presented as a "confluence" of bony architecture. Other researchers have mentioned this phenomenon.25 For example, a one-wall defect usually had three walls at
FIGURE 5A.  Preoperative appearance of the combination one. two-wall intraosseous defect prior to placement of a bone blend graft, B. Appearance of the one. two-wall intraosseous defect shown in A at reentry, eight weeks after initial surgery. Note the apparent fill and remodeling of the lesion.
FIGURE 6A. Preoperative appearance of the two-wall irttraosseous defect prior to placement of an iliac marrow and cancellous bone implant B. Appearance of two-wall intraosseous defect shown in A at reentry. 16 weeks after initial surgery. Again note the apparent fill and remodeling of the lesion.
Table 1.  Average Fill in Relation to Preoperative Osseous Depth in Two Procedures

its most apical part, two walls in the middle, and one wall at its most coronal portion. The implication of such classification in clinical research becomes apparent upon analysis of biometric data in studies dealing with osseous fill. If we take one of our cases, for example, we see how a reported complete fill could be deceiving. In this case (an osseous coagulum-bone blend graft) no residual defect apparently remained upon reentry. However, of the original 8.5 mm osseous defect, 4.9 mm filled with new bone while 3.6 mm were eliminated by resorption of the walls of the defect. Thus, in evaluating a successful "fill." one must separate the extent of the actual osseous fill from the remodeling with and/or without resorption of the original crestal architecture. We observed that the amount of new bone (fill) may depend on available osseous surfaces rather than number of osseous walls. In fact, as noted in our results, the difference in fill using osseous coagulum-bone blend in defects greater than 4.0 mm and defects less than 4.0 mm showed a statistically significant difference (t = 2.42, P < 0.05). Thus, the deeper the defect, the greater the fill.  In this manner, one, two, or three walls may be considered as a clinical expression of variations in available osseous surfaces. Therefore, a 10 mm defect of one- or two-wall configuration may give significant responses because it may present greater surface area than a wide, shallow three-wall defect. The possibility that treatment of any single surface
TABLE 2. Reentry Intraosseous Depth

* Percentage of case with <1mm defect remaining
TABLE 3. Average Fill in Relation to Pre-operative Osseous Depth in Two Procedures

may lead to considerable osseous remodeling also exists, Certainly our data show remodeling of the crest including resorption as a common phenomenon in the repair of infrabony lesions occurring within the first few weeks after surgery. It may, however, continue for many months29, 33 or years after surgery as part of the functional demands placed on the periodontium during the lifetime of the tooth. Finally a comment should he made concerning the timing of reentry procedures which in all but two cases of osseous coagulum-bone blend grafts, were performed seven to ten weeks post-operatively. Experimental histologic data in monkeys have demonstrated that bone responses following the use of osseous coagulum implants were completed by 90 days after graft surgery.32 Another study dealing with grafts of cancellous bone obtained from intraoral sources implanted into bifurcation defects showed evidence of new bone "connecting adjacent graft particles" as early as three weeks postoperatively.30 Using rabbits, Urist10 created defects in the rami of mandibles and filled these with deminerati/ ed bone. These grafts were "resorbed and refilled partially with new bone within four weeks.40 Other studies dealing with graft resorption, demonstrated a mean resorptive time of six weeks when autogenous cancellous bone was implanted intramuscularly in dogs.41 Since our study was aimed essentially at comparisons of repair potential rather then complete remodeling, and furthermore since human studies indicated that remodeling may not be complete until about five years after graft placement,34 we felt that the seven- to ten-week time interval chosen would give us adequate documentation for an analysis of repair potential following the use of different graft modalities.

SUMMARY
A clinical evaluation was undertaken to compare regeneration of osseous defects following implantation of either osseous coagulum-bone blend from intraoral sources or autogenous iliac marrow-cancellous bone. Thirty-two transplants were performed in 15 male patients. The intraosseous defects in which marrow was placed (initial average depth - 7.18 mm) filled 60.7% (average fill 4.36 mm). Defects in which osseous coagulum-bone blend was placed (initial average depth 4.0 mm) filled 73% (average fill 2.93 mm). The difference in results between the two materials was not statistically significant. Therefore, similar levels of osseous regeneration apparently took place regardless of graft material used.

ACKNOWLEDGMENTS

The authors wish to express their appreciation to Mr. T. Willers, Mr. R. Vollmer, and Mrs. C. Yarlett of the Medical Illustration Service of the Northpor: Veterans Administration Hospital for their assistance with the photography.

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