To evaluate how aging and estrogen deficiency influence the success rate of Sandblasted Titanium (Ti/SA) implants, the osteointegration of Ti/SA rods was studied in the cortical and trabecular bone of 5 young, 5 aged and 5 ovariectomized (OVX) sheep.
The characterization of the host bone by transiliac biopsies of the iliac crest showed a progressive rarefaction of trabecular bone in aged and OVX animals when compared to young ones. A significant reduction, both in cortical and trabecular bone, of the osteointegration rate of Ti/SA rods in the presence of estrogen deficiency compared to young animals was observed, while only a minor reduction was observed in aged animals. These results were confirmed by the pushout test in cortical bone.
Bone quality affected the biological response of bone to Ti/SA implants in both trabecular and cortical bone; consequently, strategies to maximize the bone osteogenic properties of osteoporotic patients should be adopted.
DreinhoferK.E., FeronJ.M., HerreraA., HubeR., JohnellO., LidgrenL., MilesK., PanarellaL., SimpsonH., WallaceW.A.Orthopaedic surgeons and fragility fractures. A survey by the Bone and Joint Decade and the International Osteoporosis Foundation.J Bone Joint Surg (Br)2004; 86-B: 958–61.
2.
Nicoli AldiniN., FiniM., GiavaresiG., MartiniL., DubiniB., Ponzi BossiM.G., RustichelliF., KrajewskiA., RavaglioliA., MazzocchiM., GiardinoR.Osteointegration of bioactive glass-coaterd and uncoated zirconia in osteopenic bone. An in vivo experimental study.J Biomed Mater Res A2004; 68: 264–72.
3.
LinderL., ObrantK., BovinG.Osseointegration of metallic implants. II. Transmission electron microscopy in the rabbit.Acta Orthop Scand1989; 60: 135–9.
MarieP.J.Cellular and molecular alterations of osteoblasts in human disorders of bone formation.Histol Histopathol1999; 14: 525–38.
6.
AugatP., SimonU., LiedertA., ClaesL.Mechanics and mechano-biology of fracture healing in normal and osteoporotic bone.Osteoporos Int2005; 16(suppl): S36–43.
7.
BarriosC., BrostrumL.A., StarkA., WalheimG.Healing complications after internal fixation of trochanteric hip fractures. The prognostic value of osteoporosis.J Orthop Trauma1993; 7: 438–42.
8.
BlomqvistJ.E., AlberiusP., IsaksonS., LindeA., HanssonB.G.Factors in implant osteointegration failure after bone grafting. An osteometric and endocrinologic matched analysis.Int J Oral Maxillofac Surg1996; 2581: 63–8.
9.
FiniM., GiavaresiG., TorricelliP., KrajewskiA., RavaglioliA., Mattioli BelmonteM., BiaginiG., GiardinoR.Biocompatibility and osteointegration in osteoporotic bone. A preliminary in vitro and in vivo study.J Bone Joint Surg (Br)2001; 83-B: 139–43.
10.
FiniM., Nicoli AldiniN., GandolfiM.G., Mattioli BelmonteM., GiavaresiG., ZucchiniC., De BenedittisA., AmatiS., RavaglioliA., KrajewskiA., RoccaM., GuzzardellaG.A., BiaginiG., GiardinoR.Biomaterials for orthopedic surgery in osteoporotic bone: a comparative study in osteoporotic rats.Int J Artif Organs1997; 20: 291–7.
11.
KuboT., ShigaT., HashimotoJ., YoshiokaM., HonjoH., UrabeM., KitajimaI., SembaI., HirasawaY.Osteoporosis influences the late period of fracture healing in a rat model prepared by ovariectomy and low calcium diet.J Steroid Biochem Mol Biol1999; 68: 197–202.
12.
LillC.A., GerlachU.V., EckhardtC., GoldhahnJ., SchneiderE.Bone changes due to glucocorticoid application in an ovariectomized anmal model for fracture treatment in osteoporosis.Osteoporos Int2002; 13: 407–14.
13.
MeyerRAJr, TsahakisP.J., MartinD.F., BanksD.M., HarrowM.E., KiebzakG.M.Age and ovariectomy impair both the normalization of mechanical properties and the accretion of mineral by the fracture callus in rats.J Orthop Res2001; 19: 428–35.
14.
Namkung-MatthaiH., AppleyardR., JansenJ., Hao LinJ., MaastrichtS., SwainM., MasonR.S., MurrellG.A., DiwanA.D., DiamondT.Osteoporosis influences the early period of fracture healing in a rat osteoporotic model.Bone2001; 28: 80–6.
15.
TorricelliP., FiniM., RoccaM., GiavaresiG., GiardinoR.In vitro pathological model of osteopenia to test orthopedic biomaterials.Artif Cells Blood Substit Immobil Biotechnol2000; 28: 181–92.
16.
ZhangH., LewisC.G., AronowM.S., GronowiczG.A.The effects of patient age on human osteoblsts' response to Ti-6Al-4V implants in vitro.J Orthop Res2004; 22: 30–8.
17.
HeetveldM.J., RaaymakersE.L., van Eck-SmitB.L., van WalsumA.D., LuitseJ.S.Internal fixation for displaced fractures of the femoral neck.Does bone density affect clinical outcome? J Bone Joint Surg (Br)2005; 87-B: 367–73.
18.
WittenbergR.H., SheaM., SwartzB.A., LeeS.K., WhiteA.A., HayesW.C.Importance of bone mineral density in instrumented spine fusions.Spine1991; 16: 647–52.
FranchiM., FiniM., GiavaresiG., OttaniV.Peri-implant osteogenesis in health and osteoporosis.Micron2005; 36: 630–44.
21.
JilkaR.L.Cytokines, bone remodelling and estrogen deficiency. A 1998 update.Bone1998; 23: 75–81.
22.
MorraM., CassinelliC., BruzzoneG., CarpiA., Di SantiG., GiardinoR., FiniM.Surface chemistry effects of topographic modifications of titanium dental implant surfaces: 1. Surface analysis.Int J Oral Maxillofac Implants2003; 18: 40–5.
23.
SchuhA., UterW., KachlerW., GoskeJ., ZeilerG., LillC.Comparative surface examinations on corund blasted titanium implants and explants in total hip arthroplasty.Arch Orthop Trauma Surg2005; 125: 676–82.
24.
ConfortoE., AronssonB-O, SalitoA., CrestouC., CaillardD.Rough surfaces of titanium and titanium alloys for implants and prostheses.Materials Science & Engineering2004; 24: 611–8.
25.
DegidiM., ScaranoA., IezziG., PiattelliA.Periimplant bone in immediately loaded titanium implants: histologic and histomorphometric evaluation in human. A report of two cases.Clin Implant Dent Relat Res2003; 5: 170–5.
26.
PiconiC., MaccauroG., MuratoriF., Brach Del PreverE.Alumina and zirconia ceramics in joint replacements.Journal of Applied Biomaterials & Biomechanics2003; 1: 19–32.
27.
BellinoF.L.Nonprimate animal models of menopause: workshop report.Menopause2000; 7: 14–24.
28.
JohnsonR.B., GilbertJ.A., CooperR.C., ParsellD.E., StewartB.A., DaiX., NickT.G., StreckfusC.F., ButlerR.A., BoringJ.G.Effect of estrogen deficiency on skeletal and alveolar bone density in sheep.J Periodontol2002; 73: 383–9.
29.
MartiniL., FiniM., GiavaresiG., GiardinoR.Sheep model in orthopaedic research: a literature review.Comp Med2001; 51: 292–99.
30.
NewmanE., TurnerA.S., WarkJ.D.The potential of sheep for the study of osteopenia: current status and comparison with other animal models.Bone1995; 16(suppl): S277–84.
31.
TurnerA.S.The sheep as a model for osteoporosis in humans.Vet J2002; 163: 232–9.
32.
FiniM., GiardinoR.In vitro and in vivo tests for the biological evaluation of candidate orthopedic materials: Benefits and limits.Journal of Applied Biomaterials & Biomechanics2003; 1: 155–63.
33.
RoccaM., FiniM., GiavaresiG., Nicoli AldiniN., GiardinoR.Osteointegration of hidroxyapatite-coated and uncoated titanium screws in long-term ovariectomized sheep.Biomaterials2002; 23: 1017–23.
34.
ParfittA.M., DreznerM.K., GlorieuxF.H., KanisJ.A., MallucheH., MeunierP.J., OttS.M., ReckerR.R.Bone histomorphometry: standardization of nomenclature, symbls and units.J Bone Miner Res1987; 2: 595–610.
35.
DhertW.J., JansenJ.A.The validity of a single push-out test. In: AnY.H., DraughinR.A.Mechanical testing of bone and the bone-implant interface.Boca Raton: CRC Press LLC; 2000.
36.
PedhazurE.J.Multiple regression in behavioral research explanation and prediction, 3rd Ed.Orlando Florida: Harcourt Brace College Publishers; 1993.
37.
ScheffeH.The Analysis of Variance.New York: John Wiley and Sons; 1959.
38.
Dalle CarbonareL., GianniniS.Diagnostica istologica delle malattie metaboliche dello scheletro: istomorfometria ossea (Histologic diagnosis of metabolic bone diseases: bone histomorphometry).Reumatismo2004; 56: 15–23.
39.
FiniM., PieriniG., GiavaresiG., BiaginiG., Mattioli BelmonteM., Nicoli AldiniN., RoccaM., MartiniL., GiardinoR.The ovariectomized sheep as a model for testing biomaterials and prosthetic devices in osteopenic bone: a preliminary study on iliac crest biopsies.Int J Artif Organs2000; 23: 275–8.
40.
GiavaresiG., FiniM., TorricelliP., MartiniL., GiardinoR.The ovariectomized ewe in the evaluation of biomaterials for prosthetic devices in spinal fixation.Int J Artif Organs2001; 24: 814–20.
41.
GiavaresiG., FiniM., Nicoli AldiniN., GiardinoR.Histomorphometric characterisation of the cancellous and cortical bone of ovariectomized sheep model.J Appl Anim Res2001; 20: 221–32.
42.
LuX.J., GallurA., FlautrèB., AnselmeK., DescampsM., ThierryB., HardouinP.Comparative study of tissue reactions to calcium phosphate ceramics among cancellous, cortical and medullar bone in rabbits.J Biomed Mater Res1998; 42: 357–67.
43.
VercaigneS., WolkeJ.G., NaertI., JansenJ.A.Histomorphometrical and mechanical evaluation of titanium plasma-spray-coated implants placed in the cortical bone of goats.J Biomed Mater Res1998; 41: 41–8.
44.
SeemanE.Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis.Osteoporos Int2003; 14(suppl 3): S2–8.
45.
HaraT., HayashiK., NakashimaY., KanemaruT., IwamotoY.The effect of hydroxyapatite coating on the bonding of bone to titanium implants in the femora of ovariectomised rats.J Bone Joint Surg (Br)1999; 81-B: 705–9.
46.
HayashiK., FotovatiA., AliS.A., OdaK., OidaH., NaitoM.Prostaglandin EP4 receptor agonist augments fixation of hydroxyapatite-coated implants in a rat model of osteoporosis.J Bone Joint Surg (Br)2005; 87-B: 1150–6.
47.
HayashiK., UenoyamaK., MashimaT., SugiokaY.Remodelling of bone around hydroxyapatite and titanium in experimental osteoporosis.Biomaterials1994; 15: 11–6.
48.
PanJ., ShirotaT., OhnoK., MichiK.Effect of ovariectomy on bone remodeling adjiacent to hydroxyapatite-coated implants in the tibia of mature rats.J Oral Maxillofac Surg2000; 58: 877–82.
49.
RoccaM., FiniM., GiavaresiG., Nicoli AldiniN., GiardinoR.Tibial implants: biomechanical and histomorphometric studies of stainless steel and titanium screws hydroxyapatite-coated and uncoated in long-term ovariectomized sheep.Int J Artif Organs2001; 24: 649–54.
50.
Nicoli AldiniN., FiniM., GiavaresiG., MartiniL., DubiniB., Ponzi BossiM.G., RustichelliF., KrajewskiA., RavaglioliA., MazzocchiM., GiardinoR.Osteointegration of bioactive glass-coated and uncoated zirconia in osteopenic bone. An in vivo experimental study.J Biomed Mater Res2004; 68A: 264–72.
51.
SoballeK., HansenE.S., Brockstedt-RasmussenH., HjortdalV.E., JuhlG.I., PedersenC.M., HvidI., BungerC.Fixation of titanium and hydroxyapatite-coated implants in arthritic osteopenic bone.J Arthroplasty1991; 6: 307–16.
52.
BeckerW., HujoelP.P., BeckerB.E., WillinghamH.Osteoporosis and implant failure: an exploratory case-control study.J Periodontol2000; 71: 625–31.
53.
KonttinenY.T., ZhaoD., BeklenA., MaG., TakagiM., Kivela-RajamakiM., AshammakhiN., SantavirtaS.The microenvironment around total hip replacement prostheses.Clin Orthop Rel Res2005; 430: 28–38.
