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Table 2 Summary of the characteristics and main results of pre-clinical animal studies

From: The bone lid technique in lateral sinus lift: a systematic review and meta-analysis

Refs.

Animal model

Sample size (no. animals)

Test side- bone lid biomaterial(s)

Control side Biomaterial(s)

Killing (weeks)

Bone cutting instruments

Bone lid fixation

Assessment method(s)

Main findings

Perini et al. [31]

Sheep

8

β-TCP

β-TCP + polylactic membrane

16

Round bur

Cyanoacrylate-based surgical glue

Histological analysis

Histomorphometric analysis

Histological analysis: new bone surrounding and partially interpenetrating the biomaterial’s particles, in continuity with the lateral and medial walls of the sinus and with the repositioned bone plate. The bone window appeared connected by new formed bone with the edge of the antrostomy and the center of the elevated area. No remnants of cyanoacrylate

Histomorphometric analysis: higher bone regeneration and bone interpenetration into the graft in the close-to-window region in test than in control group (bone regeneration: 22.1 ± 12.6%; vs 7.5 ± 4.5%; P = 0.028 and bone interpenetrated: 66.1 ± 14.7% vs 44.2 ± 15.1%; P = 0.046, respectively). Higher amount of soft tissue in the middle of the elevated space in the control than in the test site (37.5 ± 10.1% vs 29.7 ± 4.9%; P = 0.046)

In other areas, no differences between the two groups in terms of new bone % and graft %. More bone regenerated at the edges of the antrostomy in the test sites compared with the control ones, not statistically significant

Complications: loss of biomaterial in one sinus of the test group (associated with sinusitis) and one sinus of the control group; loss of one repositioned bone lid (probably during histological processing)

Omori et al. [29]

Rabbit

18

Collagened cortico-cancellous porcine bone

Collagened cortico-cancellous porcine bone + collagen membrane

2,4,8

Sonic instrument

Cyanoacrylate-based surgical glue

Histological analysis

Histomorphometric analysis

Histological analysis: at 2 weeks, small amounts of new bone, originating from the bony sinus walls, in both groups. New bone density increased proportionally to the healing period, both in test and control group. Small residual defects around the margin of the repositioned bone plate in the test sites, and in the center of the antrostomy in the control ones. Surgical glue remnants still present after 8 weeks. Xenograft resorption increased with the healing period

Histomorphometric analysis: 2 weeks: both in test and control groups, small amount of new bone (2.5 ± 2.4% vs 1.6 ± 1.0%, P < 0.05), predominantly proximal to the bony walls (4.0 ± 3.8% vs 3.1 ± 2.3%). No bone adjacent to the sinus mucosa and in the middle area. New bone % at the edge of the antrostomy were 6.4 ± 12.5% (test) and 3.2 ± 1.7% (control). No bone regenerated in the central region of the control site

4 weeks: new bone increased to 7.9 ± 6.5% and 8.5 ± 9.7% (P < 0.05), respectively, in the test and control site with highest amounts near the bone walls (11.0 ± 9.5% vs 10.0 ± 9.5%). At the edge of the antrostomy new bone % increased both in test and control groups (24.7 ± 16.8% vs 18.1% ± 11.6%)

8 weeks: new bone values were 22.7 ± 13.6% and 23.9 ± 14.4% (P < 0.05), respectively, at the test and control site with lower amount in the sub-mucosa region. New bone at the edge of the antrostomy: 33.9 ± 19.3% (test) and 37.4 ± 19.2% (control)

Complications: 3 sinus membrane perforation in the control group repaired with collagen membranes (two at 2 weeks and one at 4 weeks, still visible at the histological analysis). Loss of biomaterial in one sinus of the 2 weeks control group

Moon et al. [17]

Rabbit

16

β-TCP

β-TCP + collagen membrane

1, 2, 4, 8

Piezosurgery (saw)

None

Histological analysis

Histomorphometric analysis

Histological analysis: new bone thickness and density as well as new bone around β-TCP particles increased following the healing periods. Higher and faster bone regeneration in the test sites. No signs of inflammation. TRAP staining revealed an increasing number or osteoclast from 1 to 4 weeks, which decreased at 8 weeks in all groups

Histomorphometric analysis: control group: new bone % increased at 1, 2,4 and 8 weeks (0.6 ± 0.10%; 6.35 ± 1.25%; 13.02 ± 1.76% and 21.74 ± 2.40%) with significant difference between each timepoint and the previous one (P < 0.05). Test group: new bone significantly increased between each timepoint and the former (0.58 ± 0.21%; 11.15 ± 1.48%; 19.81 ± 2.22% and 31.28 ± 3.51%, respectively, at 1, 2, 4, and 8 weeks) (P < 0.05). Lamellar bone/ new woven bone ratio significantly higher in the test group at 4 and 8 weeks. β-TCP resorption significantly higher in test group at 8 weeks

Complications: None

Sohn et al. [19]

Rabbit

20

None

DBBM + collagen membrane

1, 2, 4, 6, 8

Piezosurgery (saw)

Mini-screws

Histological analysis

Immunohistochemical analysis

Histological analysis: Test group: new woven bone along the repositioned bone window at 1 week. New bone expanding from the repositioned bone window to the center of the elevated area at 2 weeks. At 4,6 and 8 weeks, new bone thickness, maturation, and density progressively increased

Control group: no new bone around the biomaterial at 1 week. At 2 weeks new bone mainly along the elevated sinus mucosa. At 4 weeks, presence of osteocytes and new bone bound to the biomaterial particles. At 6 weeks, presence of more mature and abundant new bone and particles surrounded by dense and mature new bone

Immunohistochemical analysis: test group: positive cells for PCNA presence along the floor of the replaceable bone window and the elevated sinus membrane from 1 to 4 weeks. Weak expression of positive cells for PCNA on the new bone surface. Strong expression of type I collagen in new bone on the floor of the repositioned bone window and weak expression of type I collagen in the surrounding soft tissue. Osteocalcin expression mainly found on the new bone along the floor of the repositioned bone window after 1 week. Control group: few PCNA-positive cells found at the new bone surface under the elevated sinus membrane. At 2 weeks, more PCNA-positive cells were observed in the biomaterial particles and presence of osteoblasts on the new bone surface. Weaker expression of PCNA-positive cells at 4, 6 and 8 weeks. Strong expression of type I collagen on osteoblasts and new bone surface after 2 weeks. Osteocalcin was observed on the surface of new bone around the biomaterial particles, but not along the collagen membrane at 1 week

Complications: none

Sohn et al. [18]

Rabbit

20

None

DBBM + collagen membrane

1, 2, 4, 6, 8

Piezosurgery (saw)

Mini-screws

Histological analysis

Histomorphometric analysis

Histological analysis: Test group: initial new bone formation under the elevated sinus membrane and the floor of the replaced bone window after 1 week. Active bone regeneration with presence of osteoblasts and osteoclasts at 4 weeks. New bone thickness and density constantly increased, up to 8 weeks. Control group: no new bone around the biomaterial nor under the collagen membrane at 1 week. Bone regeneration started from the 2nd week and constantly increased till the 8th week. Higher and faster bone regeneration along the elevated sinus membrane than around the graft

TRAP staining: in both test and control group, osteoclasts number increased from 1 to 4 weeks, and decreased at 6 and 8 weeks, compared with the 4 weeks timepoint. No statistically significant differences

Histomorphometric analysis: test group: bone regeneration 1.52 ± 0.79%; 11.33 ± 2.28%; 43.09 ± 5.23%; 55.62 ± 4.81% and 65.96 ± 2.99%, respectively, at 1, 2, 4, 6 and 8 weeks, with significant difference between each timepoint (P < 0.001). Control group: newly formed bone: 0.55 ± 0.29%; 3.54 ± 1.02%; 14.36 ± 2.71%; 21.94 ± 1.89% and 23.26 ± 2.07% respectively at 1, 2, 4, 6 and 8 weeks, with no significant differences only between 6 and 8 weeks. Significantly faster regeneration and denser new bone in the test group compared with the control one

Complications: None

  1. β-TCP β-tricalcium phosphate, DBBM deproteinized bovine-derived bone mineral, PCNA proliferating cell nuclear antigen