Material and methods

Seven mature male foxhounds 1 to 2 years of age, weighing between 55 and 65 lbs, were used for this study. The Institutional Animal Care and Use Committee at Baylor College of Dentistry (Dallas, Tex) approved the care of the animals and the experimental protocols. Foxhounds are an established model for investigating peri-implant osseous dynamics; their larger mandibles provide sufficient space between MSIs for loading.

MSIs (IMTEC, Ardmore, Okla) with 2 material surface preparations were used. The MSIs were self-drilling and made of titanium alloy, 6 mm long and 1.8 mm in diameter. SLA-type surfaces and conventional machined surfaces were compared. These MSIs were used to reduce the possibility of contacting the lingual cortical plate during placement.

Each animal had 6 MSIs placed in the interradicular areas of the mandibular first and second molars. Two immediately loaded MSIs and 1 unloaded MSI were placed on each side. The SLA-surfaced MSIs were randomly allocated to 1 side; 3 machine surfaced MSIs were placed in the same positions on the opposite side.

Prior to MSI placement, alginate impressions were poured in die stone, and radiographic stents were fabricated from the models. On the day of placement, all animals were sedated with ketamine (2.2 mg/kg intramuscularly) and rompin (0.22 mg/kg intramuscularly) and given prophylaxis with ultrasonic scaling instrumentation. The stents were placed, and periapical radiographs were taken bilaterally to determine MSI placement locations. The animals were intubated and maintained with 1% isoflurane with oxygen at 1 L per minute. Gingival tissue around the surgical sites was irrigated and lavaged with 0.2% chlorhexidine irrigant before administration of local anesthesia (2% lidocaine with 1:100,000 epinephrine) via local infiltration. Radiographic stents were replaced and used as guides to ensure the accuracy of MSI placement. All 42 MSIs were placed in buccal alveolar bone perpendicular to the cortical plate or parallel to the occlusal plane ( Fig 1 , A ). The placement sites included the bifurcations of the first and second molars. Height and anteroposterior location of placement were measured on periapical radiographs. Unloaded MSIs were placed 4 mm apical to their loaded counterparts when no anatomic limitations were present. Placement sites were marked and prepared with a 1.5-mm tissue punch, and pilot holes were drilled by using a 1.1-mm surgical drill under copious irrigation. The MSIs were manually placed and tightened with a torque tester (Cedar Sugisaki Division, Northbrook, Ill). Placement torque was recorded for each MSI.

A, Radiographic image confirming the intraradicular placement of MSIs in the posterior mandible; B, MSIs placed in the posterior mandible were loaded immediately with 200 g.

The MSIs were loaded with nickel-titanium 200-g coil springs tied through the islets on the heads of the implants with 0.010-in stainless steel ligature wire ( Fig 1 , B ). The activation forces of the coil springs were measured with a Correx Gram Force Gauge (Long Island Indicator Service, Hauppauge, NY). Postoperative peri-implant sites were irrigated with 0.2% chlorhexidine; periapical radiographs taken bilaterally were used to ensure proper MSI positioning. Both analgesics (torbugesic, 0.2 mg/kg [2 mg/mL with 1 mL per animal] and antibiotics (penicillin G, 60,000 units/kg) were administered. Inspections of appliance condition and prophylaxes with a tooth brush and 0.2% chlorhexidine irrigant were performed weekly.

Nine weeks after MSI placement, the animals were killed with 2 mL of Beuthanasia-D given intracardiac and perfused with 1 to 2 L of normal saline solution followed by 1 L of 70% ethanol. The mandibles were resected en bloc and stored in 70% ethanol before analysis.

Each bone-implant sample was retrieved with a 10-mm diameter trephine bur (ACE Dental Implant System, Brockton, Mass) under copious irrigation. The bur was modified to ensure that the bone-implant specimen fitted into the 9.8-mm inner diameter of the cylindrical specimen carriers used for scanning. The samples were trephined parallel to the long axis of the implant to ensure that all 3 layers of the bone (buccal cortical, medullary, lingual cortical) remained intact and undamaged during the retrieval process. The samples were stored in 70% ethanol.

A maximum of 3 bone-implant specimens were placed in cylindrical sample holders with 70% ethanol and evaluated by using μCT (μCT 35, Scanco Medical, Basserdorf, Switzerland) with an isotropic resolution of 6 μm. X-ray energy levels were set to 70 kVp, current to 114 μA, and integration time to 800 ms. A 0.5-mm aluminum filter and a high resolution setting of 1000 projections per 180° were used to ensure the highest quality scans with minimal metal implant artifacts.

A volume of interest (VOI) for each specimen was defined with the implant positioned in the center. The apical limit of the VOI was set to 10 slices (0.06 mm) coronally from the MSI tip; the coronal limit of the VOI was visually defined as the slice at which bone was observed to completely surround and contact the MSI. Because of the varying depths that each MSI was embedded in bone, the total number of slices in the VOI ranged from 936 to 1199, with an average total scanning time of 3.2 hours per specimen.

After scanning, a threshold (1 gray-scale “brightness” number, above which all voxels [ie, volumetric 3D pixels] are considered bone, and 1 gray-scale number below which all voxels are considered nonbone ) was determined based on multiple specimens to distinguish the MSI from mineralized bone and background. Based on comparisons with the original gray-scale images, threshold values that produced the best representation of the MSI, mineralized bone, and background images were selected. Three-dimensional images of the bone-implant specimens were reconstructed from the defined threshold parameters ( Fig 2 ). From the reconstructed 3D images, cortical and noncortical bone regions were identified; 2 Scanco Medical proprietary programming scripts with different parameters for bone-implant contacts were processed for each specimen.

Three-dimensional images of a bone-implant specimen constructed from the defined threshold values: A , cortical and noncortical regions identified through evaluation of individual axial segments; B , different materials, such as titanium alloy MSI and mineralized bone can be separated, allowing for better examination of individual components; C , titanium alloy MSI ( green ) with peri-bone-to-implant contact ( red ); D , 3D image of peri-bone-to-implant contact with MSI and supporting bone removed.

For each specimen, separate ratios of bone volume to total volume (BV/TV) were calculated for both cortical and noncortical bone regions. BV/TV measures the relative amount of bone per unit of volume; for example, a BV/TV ratio of 0.5 indicates 50% bone and 50% space, or nonbone. Although the cortical area included only cortical bone, the noncortical regions included mostly trabecular bone and limited amounts of cortical bone. The analyses pertained to 2 layers of bone, 6 to 24 μm and 24 to 42 μm, from the MSI surface ( Fig 3 ). Each layer was 18 μm thick and included three 6-μm voxels. The 24-to-42 μm layer was used because μCT segments beyond 24 μm from the MSI surface have been previously validated based on hisotologic sections of cortical (r = 0.65; P <0.05) and trabecular bone (r = 0.92; P <0.05). BV/TV ratios of bone 0 to 6 μm from the MSI were excluded in this study based on the assumption that the voxel immediately adjacent to the MSI was subject to metallic artifacts.

A , BV/TV measurements of the 2 evaluated zones reconstructed 3 dimensionally, 24-to-42 μm layer ( red ) and 6-to-24 μm layer ( purple ); B , schematic description of the 2 zones, 3 voxels in dimension, with 24 μm from the MSI surface as the midpoint. The voxel immediately adjacent to the MSI ( white ) was excluded from the study.

Results

The overall success rate for the study was 92.9%, with 3 of the 42 MSIs showing evidence of failure. There were 1 total failure and 2 partial clinical failures (slight mobility but stable enough for clinical use). The total failure pertained to an unloaded machine-surfaced MSI; the 2 partial failures were both loaded machine-surfaced MSIs, one with less than 1 mm of mobility, and the other with 1 mm of mobility. The partial failures were analyzed along with the remaining intact specimens. Clinically, the external surfaces of cortical bone for both partially failed implants had considerable amounts of remodeling, resulting in large bony concavities around the MSI. The loss of bone and consequent exposure of previously submerged threads might have compromised their stability.

The relative amounts of cortical bone in the 6-to-24 μm and 24-to-42 μm layers ranged from 39%-56% and 88%-100%, respectively. The amounts of noncortical bone in the 6-to-24 μm layers ranged between 15% and 36%; noncortical bone in the 24-to-42 μm layers ranged between 46% and 84%.

For both the cortical and noncortical regions, BV/TV decreased linearly and significantly ( P <0.05) between the coronal and apical aspects of bone ( Fig 4 ). The cortical and noncortical regions around the SLA-surfaced MSIs showed significantly greater amounts of bone at their most coronal aspects than did the machined MSIs ( Table I , Fig 5 ). Differences at the most coronal aspects ranged from 3.5% to 6.4% in the cortical regions and from 9% to 9.1% in the noncortical regions. The SLA-surfaced MSIs also showed significantly ( P <0.05) greater decreases in BV/TV than did the machined MSIs. Although the cortical regions showed few or no differences in the amount of bone in the apical aspects, the machine-surfaced MSI showed more bone than the SLA-surfaced MSIs in the noncortical regions.

Three-dimensional reconstruction of bone layers 6 to 24 μm from the MSI surface for A , loaded machine-surfaced MSIs and B , loaded SLA-surfaced MSIs.

BV/TV ratios of loaded SLA-surfaced and machine-surfaced miniscrew implants as a function of relative slice height for A , cortical region, 6-to-24 μm layer; B , cortical region, 24-to-42 μm layer; C , noncortical region, 6-to-24 μm layer; D , noncortical region, 24-to-42 μm layer.

The cortical regions around the loaded MSIs showed greater amounts of bone than did the unloaded MSIs ( Fig 6 ). The differences at the most coronal aspect were statistically significant only for the 24-to-42 μm layer in the noncortical region ( Table II ; Fig 7 ). However, all loaded MSIs showed significantly greater decreases in BV/TV between the most coronal and apical aspects than did the unloaded MSIs, with differences ranging from a low of 1.8% (for the 6-24 μm layer in the cortical region) to 9.6% (for the 24-42 μm layer in the noncortical region).

Three-dimensional reconstruction of bone layers 6 to 24 μm from the MSI surface for A , unloaded MSI and B , loaded MSI, with equal numbers of SLA-surfaced and machine-surfaced MSIs in each group.

Table II

BV/TV ratios for layers of bone 6 to 24 μm and 24 to 42 μm from the surface of unloaded and loaded miniscrew implants

	Unloaded				Loaded				Difference
	Constant	SE	Linear	SE	Constant	SE	Linear	SE	Constant	SE	Linear	SE
Cortical
6-24 μm	5.16e-1	1.24e-2	–8.55e-4	5.63e-5	5.43e-1	1.14e-2	–1.52e-3	4.46e-5	2.63e-2	1.78e-2	–6.69e-4 ∗	7.21e-5
24-48 μm	9.74e-1	8.87e-3	–8.20e-4	5.28e-5	9.90e-1	6.87e-3	–9.97e-4	3.93e-5	1.64e-2	1.13e-2	–1.76e-4 ∗	6.50e-5
Noncortical
6-24 μm	2.92e-1	2.79e-2	–9.18e-4	5.16e-5	3.14e-1	1.95e-2	–1.28e-3	3.47e-5	2.20e-2	3.41e-2	–3.60e-4 ∗	6.33e-5
24-42 μm	7.28e-1	4.27e-2	–2.04e-3	7.31e-5	8.24e-1	2.42e-2	–3.00e-3	4.84e-5	9.55e-2 ∗	4.58e-2	–9.56e-4 ∗	8.85e-5

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