effects of implant surfaces sandblasted with titanium dioxide microparticles: An experimental study using the rabbit tibia model

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1 Histologicl nd iomechnicl effects of implnt surfces sndlsted with titnium dioxide microprticles: An experimentl study using the rit tii model Astrct Ojective Sérgio Alexndre Gehrke, José Edurdo Mté Sánchez de Vl, Piedd Nieves de Az, Jun Crlos Prdos Frutos, c Jime Srdá Armurú Júnior, d Pulo Henrique Orlndo Rossetti e & José Luis Clvo Guirdo Deprtment of Reserch, Interntionl Reserch Cthedr, Universidd Ctólic Sn Antonio de Murci, Murci, Spin Institute of Bioengineering, Miguel Hernández University, Elche, Spin c Deprtment of Stomtology, Rey Jun Crlos University, Mdrid, Spin d Veterinry Deprtment, Itpirng Fculty of Veterinry Medicine, Itpirng, Brzil e Privte prctice, Buru, Brzil Corresponding uthor: Dr. Sérgio Alexndre Gehrke Ru Dr. Bozno, 571 PC: Snt Mri (RS) Brzil T/F sergio.gehrke@hotmil.com How to cite this rticle: Gehrke SA, Mté Sánchez de Vl JE, Nieves de Az P, Prdos Frutos JC, Srdá Armurú Júnior J, Orlndo Rossetti PH, Clvo Guirdo JL. Histologicl nd iomechnicl effects of implnt surfces sndlsted with titnium dioxide microprticles: n experimentl study using the rit tii model. J Orl Science Rehilittion Dec;2(4): The ojective of this study ws to investigte the effect of sndlsted, lrge-grit, cid-etched (SLA) implnt surfces treted with titnium dioxide (TiO 2 ) microprticles on the implnts stility nd resistnce to reverse torque. Mterils nd methods Six rits received 24 cylindricl dentl implnts nd were plced in two groups (n = 3 per group): control group, with smooth surfces; nd test group, with the SLA surfce treted with TiO 2 microprticles. All of the nimls were scrificed fter four weeks. Hlf of the implnts (one per niml from ech group) were used to test removl torque vlues nd hlf of them were used for the histologicl nlysis. Results Reverse torque ws significntly different etween the groups (p = ). The histologicl nlysis showed higher degrees of one orgniztion in surfce smples from the test group. Conclusion Results indicte tht lsting implnt surfces with TiO 2 prticles is n pproprite tretment option, with miniml risk of contmintion y residul deris from the procedure. Keywords Implnt surfce, osseointegrtion, removl torque, titnium dioxide microprticles. 32 Volume 2 Issue 4/2016

2 Introduction Per-Ingvr Brånemrk, Swedish professor, demonstrted tht osseointegrtion of titnium implnts is such tht the one remins in close contct with the implnt surfce without ny intervention y the connective tissue, lthough the titnium dioxide (TiO 2 ) lyer intercts directly with the one tissue. 1 The physicl nd chemicl fetures of titnium, prticulrly its intrinsic properties, such s iocomptiility, low specific weight, high strength weight rtio, low modulus of elsticity, nd excellent corrosion resistnce, re fvorle for the mnufcture of dentl implnts. 2 Furthermore, titnium surfces cn e modified in n ttempt to enhnce their iologicl properties. 3 Such modifictions re chieved y dding cot consisting of different types of ioctive sustnces, y removing portions of the externl lyer with the use of lsting mterils of different prticle sizes, or y pplying chemicl tretments nd/or physicl ones, such s lser. 4 Among these, lsting nd cid etching hve een the most widely used. In ddition, their comintion hs shown improved iologicl ctivity of titnium surfces in terms of implnt osseointegrtion reltive to smooth (mchined) surfces. 5 The modifiction of the implnt surfce cn thus hve enefits regrding the response of the surrounding one tissue, ccelerting the heling process nd/or improving the qulity of the newly formed one. 5 7 Studies hve shown tht osseointegrtion is relted to microgeometric fetures, such s the degree of surfce roughness, nd to fctors such s the physicl nd chemicl properties of surfces. 7, 8 Rough surfces were found to stimulte osteolstic gene expression nd to enhnce one formtion nd one implnt fixtion. 9, 10 While n ssocited inflmmtory response ws reported, 11 the overll success rte ws stisfctory, with the mjority of implnts yielding good osseointegrtion nd stility one yer fter surgery. 12 Dentl implnt mnufcturers hve developed nd mrketed implnts with severl types of chemicl nd physicl surfce tretments. 13 However, there is still no consensus on wht the optiml conditions for periimplnt one growth re. It is known tht one response cn e influenced y implnt surfce topogrphy t the micrometer level, nd it hs een hypothesized tht nnometric surfce cn lso hve n effect. 14 Notwithstnding, the mechnisms ehind n optiml one response to given type of surfce still remin lrgely unknown. Surfces known s SLA (sndlsted, lrgegrit, cid-etched) re produced y lsting with microprticles of some mterils followed y cid etching. Alumin is one of the most widely used mterils, ut some uthors hve highlighted some fetures of lumin lsting tht could compromise osseointegrtion (e.g., prticle detchment during the heling process nd sorption y the surrounding tissues). 15 The presence of lumin residues on implnt surfces due to the mnufcturing process hs een regrded s potentil risk, compromising long-term osseointegrtion. 16, 17 Alterntively, TiO 2 is used s lsting mteril nd hs shown interesting results in experimentl studies. Prticulrly, TiO 2 -lsted implnts were ssocited in humns with significnt enhncement of one- toimplnt contct (BIC) when compred with mchined surfces Under unfvorle clinicl conditions, such s in the presence of poor- qulity one, fst nd predictle osseointegrtion would e eneficil, llowing prosthetic rehilittion. In the cse of insufficient one quntity or ntomicl limittions, or in the presence of locl nd systemic conditions tht could compromise longterm osseointegrtion, implnts with rough surfce show etter one pposition nd BIC thn do those with smooth surfces. 21, 22 There fore, the im of the present in vivo study ws to evlute the ehvior of surfces shortly fter implnttion y mesuring removl torque nd nlyzing histologicl prmeters. Mterils nd methods Twenty-four cylindricl self-tpping implnts with internl hexgon pckged nd redy for sle were used for in vivo testing. Twelve implnts with mchined surfce (Fig. 1) were used in the control group (C group). Twelve implnts with surfces sndlsted with μm TiO 2 micro prticles t 5 tm pressure for 1 min, ultrsoniclly clened with n lkline solution, rinsed in distilled wter nd then conditioned with mleic cid (Fig. 2) were used in the test group (T group). The implnts (Implcil De Bortoli, São Pulo, Brzil) were 4 mm in dimeter nd 8 mm in length. Six mture New Zelnd white rits were used in this study. This study ws pproved y the Ethics Committee (# ) of the Volume 2 Issue 4/

3 Figs. 1 c (c) Imge of the implnt used s control (C group), with smooth surfce. ( & c) SEM imges of the surfce t 1,000 nd 5,000 mgnifiction. Figs. 1 c Figs. 2 c (c) Imge of the implnt used s test (T group), with SLA surfce. ( & c) SEM imges of the surfce t 1,000 nd 5,000 mgnifiction. c Figs. 2 c c 34 Volume 2 Issue 4/2016

4 Figs. 3 & 4 Itpirng Fculty of Veterinry Medicine, Itpirng, Brzil. The rits were nesthetized y intrmusculr ketmine (35 mg/kg; Agener Phrm ceutic, Brzil). Therefter, muscle relxnt (Rompum 5 mg/kg, Byer, Brzil) nd trnquilizer (Aceprn 0.75 mg/kg, Univet, Brzil) were injected intrmusculrly. Additionlly, 1 ml of locl nesthetic (3% prilocine-felypressin, Astr, Mexico) ws injected sucutneously t the site of surgery to improve nlgesi nd control leeding. A skin incision with periostel flp ws used to expose the one in the proximl tii. The preprtion of the one site ws done with urs under copious sline irrigtion. Two implnts were inserted into the tiil metphysis of ech rit (Fig. 3), one most proximl t 5 mm from the rticultion nd the other 10 mm to the distl, thus voiding differences in one typology in this re. The implnt position ws rndomized for ech niml t The tii ws chosen s the implnt site ecuse it provides esier surgicl ccess. The implnt insertion ws performed y hnd with torque of < 20 N until locking of the implnt in the opposite corticl portion of the osteotomy, s prt of the implnt shoulder just out in reltion to the top of the corticl one crest, therey voiding excessive compression of the one due to implnt design. The periosteum nd fsci were sutured with ctgut nd the skin with silk. Postopertively, single dose of 600,000 IU of enzthine penicillin (Benzetcil, Eurofrm Lortórios, Rio de Jneiro, Brzil) ws used. After surgery, the nimls were plced in individul cges with 12-h cycles of light, controlled temperture (21 C), nd food nd wter d liitum. No complictions or deths occurred in the postopertive period. All of the nimls were euthnized fter four weeks using n intrvenous overdose of ketmine (2 ml) nd xylzine (1 ml). A totl of 24 implnts were retrieved. The implnts of ll right tiie were immeditely nlyzed using torque-testing mchine (CME, Técnic Industril Oswldo Filizol, Gurulhos, Brzil), which ws fully controlled y DynView Torque Stndrd/ Pro M softwre (Fig. 4). All of the implnts of the left tiie were used for histologicl nlysis nd were plced in 10% formlin fter removl nd tken to the Biotecnos Lortory (Snt Mri, Brzil). After the fixtion period, they were dehydrted in n scending series of lcohols nd emedded in glycol methcrylte resin (Technovit 9100 VLC, Kulzer, Hnu, Germny) to produce undeclcified sections. Undeclcified cut nd ground sections tht contined the centrl prt of ech implnt nd hd finl thickness of 15 μm were produced using mcro-cutting nd -grinding system (Isomet 2000, Buehler, Brunschweig, Germny). The sections were stined with picro-siriushemtoxylin, nd histomorphometric nlysis ws then crried out. The specimens prepred for the nlysis of the tissue round the implnt were exmined under light microscope (EOS 200, Nikon, Tokyo, Jpn). After digitizing the phse of ech specimen under light microscope, the percentge of one-to-implnt contct (BIC%) ws mesured using the Imge Tool softwre for Microsoft Windows (Version 5.02). BIC% ws clculted s the percentge of the totl length of one in direct contct with the implnt surfce, from the first crestl one contct to the most picl contct. The sttisticl nlysis ws performed using the t-test for comprison etween groups. Two correltion mesurements were used to ssess the reltionship etween the groups: Person s correltion coefficient (with -1 < R < 1; when R is Fig. 3 Imge of the implnts inserted into the tii. Fig. 4 Imge of the computerized torque mchine used in the removl torque test. Volume 2 Issue 4/

5 Fig. 5 Removl torque vlues (N cm) t four weeks in oth groups. Fig. 5 close to ± 1 this indictes tht the vriles re correlted; however, the reltionship is liner) nd Spermn s rnk correltion coefficient, simi lr to Person s correltion coefficient, with -1 < R < 1. This mesurement ws more comprehensive ecuse we ssessed whether the reltionship etween the vriles ws nonliner. All of the tests were performed using specific softwre (MedClc, MedClc Softwre, Belgium). The level of significnce ws set t = Results The surgicl procedures were uneventful nd ll of the nimls presented pproprite heling within the first weeks fter surgery. Inspections mde during two postopertive weeks indicted no infection or inflmmtion. The iomechnicl tests indicted osseointegrtion of ll of the implnts, ut torque fter four weeks ws higher in the T group (71.0 ± 13.4 N cm; medin of 73.5) thn in the C group (54.5 ± 10.0 N cm; medin of 56.5). The men ± stndrd devitions nd the sttisticl comprison re presented in Figure 5. The pired sttisticl tests showed tht torque ws significntly higher in the T group thn in the C group t four weeks (p < ). BIC% ws higher in the T group (64.8 ± 7.4%; medin of 66.0) fter four weeks thn in the C group (50.4 ± 7.9%; medin of 49.5). These dt nd sttisticl significnce (p = ) re shown in Figure 6. The new one formed round the implnts in the C group ws not completely minerlized (Fig. 7). In the T group, however, etter orgniztion nd minerliztion were found fter four weeks (Fig. 8) nd there ws etter stimultion of the medullry one portion (Fig. 9). The Kolmogorov Smirnov test identified tht only the BIC% of the T group hd nonprmetric dt. Thus, the correltion etween reverse torque nd BIC% (mchined) ws determined y Person s correltion coefficient (R = -0.52; p = 0.08; 95% CI [ ]), wheres the correltion etween reverse torque nd BIC% (treted) ws determined y Spermn s correltion coefficient (R = 0.08; p = 0.79; 95% CI [ ]). The sttisticl dt re summrized in Tle 1. Discussion Over the pst decdes, severl in vivo studies hve exmined the effect of implnt surfces on one heling nd pposition. 23, 24 Modifictions in implnt surfce morphology nd roughness were initilly ttempted to hsten host response to implnts nd to increse the level of mechnicl interlock etween the one nd implnt surfce, thus improving initil stility nd su- 36 Volume 2 Issue 4/2016

6 Implnt surfce sndlsted with titnium dioxide microprticles Fig. 6 Fig. 6 BIC vlues (%) t four weeks in oth groups. Figs. 7 & Histologicl imges showing one mturtion nd minerliztion in the C group fter four weeks, with new one formtion round the implnts showing incomplete minerliztion. () 200 nd () 400 mgnifiction. Stining with picro-siriushemtoxylin. Figs. 8 & Histologicl imges showing one mturtion nd minerliztion in the T group fter four weeks, with more dvnced new one formtion round the implnts in the new one orgniztion res. () 100 nd () 400 mgnifiction. Stining with picro-sirius-hemtoxylin. Figs. 7 & Figs. 8 & Volume 2 Issue 4/

7 C group T group Fig. 9 Fig. 9 Histologicl imges showing one mturtion nd the BIC fter four weeks. There ws visily etter stimultion of the medullry one portion in the T group in comprison to the C group (yellow rrows). Tle 1 Men ± SD nd medin (reverse torque nd BIC%) vlues t seline nd t eight weeks. Groups Reverse torque (N cm) BIC (%) Men ± SD Medin Men ± SD Medin Coefficient of correltion Control 54.5 ± ± Test 71.0 ± ± P-vlue < * * * Between-group comprisons (Wilcoxon s test; significnce level: p < 0.05). Tle 1 sequent stress dissiption during functionl loding. 25, 26 Histologicl investigtions hve shown tht the surfce texture creted y lsting leds to greter BIC thn tht of mchined surfces, 27 which is desirle response, s it llows improvement of the overll iomechnics of the system. Blsting the implnt surfce with gritting gents mde of mterils other thn lumin my chnge the surfce composition nd implnt iocomptiility. 28 Arsive lsting increses surfce roughness nd metl surfce rectivity. 28 With the use of lsting mteril such s lumin, potentil risk of contmintion y remnnts of lsting prticles, with dissolution of luminum ions into the host tissue, cnnot e excluded. 28 It hs een reported tht luminum ions my inhiit norml differentition of one mrrow stroml cells nd norml one deposition nd minerliztion, nd luminum hs een shown to induce net clcium efflux from the cultured one. 32 Moreover, luminum my compete with clcium during the heling of the implnt ed. Aluminum hs een shown to c- 38 Volume 2 Issue 4/2016

8 cumulte t the minerliztion front nd in the osteoid mtrix itself. 33 Therefore, other lterntive sndlsting methods were developed in order to roughen the implnt surfce, such s the use of resorle prticles sed on clcium 34 nd TiO 2, 35, 36 oth of which re unprolemtic if smll residues remin fter surfce tretment procedures. The effects of sndlsting the implnt surfce with titnium oxide s n lterntive to luminum oxide hve een investigted previously. 19, 20, 27, 28, The reserch protocols took into ccount iomechnicl (removl torque), interfcil nd histologicl nlyses, s well s histomorphometric nd microhrdness mesurements. Only one study oserved nd nlyzed specimens using oth scnning electron microscopy (SEM) nd histomorphometry, s well s the removl torque test, in dogs. 37 This study demonstrted tht implnts lsted with TiO 2 prticles hd etter nchorge thn implnts with mchine-produced surfce, in spite of there eing no difference in BIC. 37 Animl models re essentil in providing phenomenologicl informtion on iologicl rection to endosseous implnts. 41 The removl torque test is mong the in vivo mechnicl tests commonly used to evlute the strength of the interction etween the one nd implnt surfce High resistnce to implnt removl encountered during these tests indictes good integrtion etween the one nd implnt surfce, or in the cse of porous mterils, high degree of one ingrowth into the pores of the implnt. 44 The present study evluted the extent of osseointegrtion nd the chrcteristics of the one round the surfce within four weeks fter implnttion. Previous reserch hs shown tht surfce chrcteristics influenced BIC, with sttisticlly significnt differences on different implnt surfces. 41 Histomorphometric nd removl torque mesurements re two representtive tests used to ssess the nture of the implnt tissue interfce. 45 In this study, oth surfce iocomptiility nd osteoconductive properties were confirmed y the iomechnicl tests. Such interction ws more pronounced for the textured surfce compred with the mchined one, indicting possile synergistic interction of the mechnicl interlock etween the one nd implnt surfce nd higher one formtion compred with the mchined surfce. The reverse torque vlues my pper rther high even for implnts with mchined surfce. This hs to do with the experimentl model chosen. In fct, the corticl one of rit tii is very compct nd my firmly interlock with the implnts. However, the im of the present study ws not to estimte prmeter vlues tht could e directly trnsferred to ptients, ut to compre two different surfces using oth in vitro nd in vivo pproches. The results confirm tht TiO 2 -lsted surfces llow for greter osteoconductivity nd ccelerted one formtion compred with mchined surfces nd re therefore recommended for nticipted loding protocols. Conclusion Despite the limittions of this study, TiO 2 lsting displyed positive effect on osseointegrtion nd on the iomechnicl fetures of the implnts. The histologicl results confirmed the hypothesis tht the SLA surfce using lsting with TiO 2 microprticles positively ffects the osseointegrtion of titnium dentl implnts. Competing interests The uthors declre tht they hve no conflict of interests relted to this study. References 1. Sullivn R. Implnt dentistry nd the concept of osseointegrtion: historicl perspective. J Clif Dent Assoc Nov;29(11): Lemons JE, Venugopln R, Lucs L. Corrosion nd iodegrdtion. In: AF von Recum, editor. Hndook of iomterils evlution: scientific, technicl nd clinicl testing of implnt mterils. New York: Tylor Frncis; Liu X, Chu PK, Ding C. Surfce modifiction of titnium, titnium lloys, nd relted mterils for iomedicl pplictions. Mter Sci Eng R Rep Dec;47(3-4): Wennererg A, Alrektsson T. Effects of titnium surfce topogrphy on one integrtion: systemtic review Sep;20 Suppl 4: Noves AB Jr, Souz SL, Brros RR, Pereir KK, Iezzi G, Pittelli A. Influence of implnt surfces on osseointegrtion. Brz Dent J. 2010;21(6): Wennererg A, Alrektsson T. On implnt surfces: review of current knowledge nd opinions Jn-Fe;25(1): Sul YT, Johnsson C, Wennererg A, Cho LR, Chng BS, Alrektsson T. Optimum surfce properties of oxidized implnts for reinforcement of osseointegrtion: surfce chemistry, oxide thickness, porosity, roughness, nd crystl structure My-Jun;20(3): Volume 2 Issue 4/

9 References 8. Le Guéhennec L, Soueidn A, Lyrolle P, Amouriq Y. Surfce tretments of titnium dentl implnts for rpid osseointegrtion. Dent Mter Jul;23(7): Ellingsen JE, Johnsson CB, Wennererg A, Holmén A. Improved retention nd one-to-implnt contct with fluoride-modified titnium implnts Jul;23(7): Arhmsson I, Alouy JP, Berglundh T. Heling t fluoride-modified implnts plced in wide mrginl defects: n experimentl study in dogs Fe;19(2): Stnford CM, Johnson GK, Fkhry A, Grtton D, Mellonig JT, Wnger W. Outcomes of fluoride modified implnt one yer fter loding in the posterior-mxill when plced with the osteotome surgicl technique. Appl Osseointegr Res. 2006;5: Vriol F, Brunski JB, Orsini G, Tmsco de Oliveir P, Wzen R, Nnci A. Nnoscle surfce modifictions of mediclly-relevnt metls: stte-of-the rt nd perspectives. Nnoscle Fe;3(2): Binon PP. Implnts nd components: entering the new millennium Jn-Fe;15(1): Bressn E, Sricoli L, Guzzo R, Tocco I, Romn M, Vindigni V, Stellini E, Grdin C, Ferroni L, Sivolell S, Zvn B. Nnostructured surfces of dentl implnts. Int J Mol Sci Jn 17;14(1): Apricio C, Gil FJ, Fonsec C, Bros M, Plnell JA. Corrosion ehvior of commercilly pure titnium shot lsted with different mterils nd size of shot prticles for dentl implnt pplictions. Biomterils Jn;24(2): Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biologicl fctors contriuting to filures of osseointegrted orl implnts. (II). Etiopthogenesis. Eur J Orl Sci Jun;106(3): Johnsson C, Alrektsson T, Thomsen P, Sennery L, Lodding A, Odelius H. Tissue rections to titnium-6 luminum-4 vndium lloy. Eur J Exp Musculoskel Res. 1992;1: Ivnoff CJ, Hllgren C, Widmrk G, Sennery L, Wennererg A. Histologic evlution of the one integrtion of TiO2 lsted nd turned titnium microimplnts in humns Apr;12(2): Rsmusson L, Khnerg KE, Tn A. Effects of implnt design nd surfce on one regenertion nd implnt stility: n experimentl study in the dog mndile. Clin Implnt Dent Relt Res Jn;3(1): Gehrke SA, Tschieri S, Del Fro M, Coelho PG. Positive iomechnicl effects of titnium oxide for sndlsting implnt surfce s n lterntive to luminium oxide. J Orl Implntol Oct;41(5): Pittelli A, Degidi M, Polntonio M, Mngno C, Scrno A. Residul luminum oxide on the surfce of titnium implnts hs no effect on osseointegrtion. Biomterils Oct;24(22): Cochrn DL, Buser D, ten Bruggenkte CM, Weingrt D, Tylor TM, Bernrd JP, Peters F, Simpson JP. The use of reduced heling times on ITI implnts with sndlsted nd cid-etched (SLA) surfce: erly results from clinicl trils on ITI SLA implnts Apr;13(2): Misch CE. Density of one: effect on tretment plns, surgicl pproch, heling, nd progressive one loding. Int J Orl Implntol. 1990;6(2): Hsu SH, Liu BS, Lin WH, Ching HC, Hung SC, Cheng SS. Chrcteriztion nd iocomptiility of titnium dentl implnt with lser irrdited nd dul-cid etched surfce. Biomed Mter Eng. 2007;17(1): Alrektsson T, Brånemrk PI, Hnsson HA, Lindström J. Osseointegrted titnium implnts. Requirements for ensuring long-lsting, direct one-to-implnt nchorge in mn. Act Orthop Scnd. 1981;52(2): Textor M, Sittig C, Fruchiger V, Tostti S, Brunette DM. Properties nd iologicl significnce of nturl oxide films on titnium nd its lloys. In: Brunette DM, Tengvll P, Textor M, Thomsen P, editors. Titnium in medicine. Berlin: Springer; p Ivnoff CJ, Widmrk G, Johnsson C, Wennererg A. Histologic evlution of one response to oxidized nd turned titnium micro-implnts in humn jwone My-Jun;18(3): Wennererg A, Alrektsson T, Johnsson C, Andersson B. Experimentl study of turned nd grit-lsted screw-shped implnts with specil emphsis on effects of lsting mteril nd surfce topogrphy. Biomterils Jn;17(1): Thomson GJ, Puleo DA. Ti-6Al-4V ion solution inhiition of osteogenic cell phenotype s function of differentition time course in vitro. Biomterils Oct;17(20): Ste S, Svrino L, Toni A, Sudnese A, Giunti A, Pizzoferrto A. Micrordiogrphic nd histochemicl evlution of minerliztion inhiition t the one lumin interfce. Biomterils. 1992;13(10): Cpdevielle MC, Hrt LE, Goff J, Scnes CG. Aluminum nd cid effects on clcium nd phosphorus metolism in young growing chickens (Gllus gllus domesticus) nd mllrd ducks (Ans pltyrhynchos). Arch Environ Contm Toxicol Jul;35(1): Bushinsky DA, Sprgue SM, Hllegot P, Girod C, Chl JM, Levi-Setti R. Effects of luminum on one surfce ion composition. J Bone Miner Res Dec;10(12): Nim L, Jensen JS, Gotfredsen K. Interfce mechnics nd histomorphometric nlysis of hydroxyptite-coted nd porous glss-cermic implnts in cnine one. J Biomed Mter Res Dec;29(12): Alrektsson T, Wennererg A. Orl implnt surfces: Prt 1 review focusing on topogrphic nd chemicl properties of different surfces nd in vivo responses to them. Int J Prosthodont Sep-Oct;17(5): Alrektsson T, Wennererg A. Orl implnt surfces: Prt 2 review focusing on clinicl knowledge of different surfces. Int J Prosthodont Sep-Oct;17(5): Buser D, Broggini N, Wielnd M, Schenk RK, Denzer AJ, Cochrn DL, Hoffmnn B, Lussi A, Steinemnn SG. Enhnced one pposition to chemiclly modified SLA titnium surfce. J Dent Res Jul;83(7): Gotfredsen K, Nim L, Hjörting-Hnsen E, Jensen JS, Holmén A. Histomorphometric nd removl torque nlysis for TiO2-lsted titnium implnts. An experimentl study on dogs Jun;3(2): Drvell BW, Smmn N, Luk WK, Clrk RK, Tidemn H. Contmintion of titnium cstings y luminium oxide lsting. J Dent Oct;23(5): Wennererg A, Alrektsson T, Andersson B. Bone tissue response to commercilly pure titnium implnts lsted with fine nd corse prticles of luminum oxide Jn-Fe;11(1): Sennery L, Dsmh A, Lrsson B, Iverhed M. Bone tissue responses to surfce-modified zirconi implnts: histomorphometric nd removl torque study in the rit. Clin Implnt Dent Relt Res. 2005;7 Suppl 1:S Pittelli A, Mnzon L, Scrno A, Polntonio M, Pittelli M. Histologic nd histomorphometric nlysis of the one response to mchined nd sndlsted titnium implnts: n experimentl study in rits Nov-Dec;13(6): Meredith N, Shgldi F, Alleyne D, Sennery L, Cwley P. The ppliction of resonnce frequency mesurements to study the stility of titnium implnts during heling in the rit tii Jun;8(3): Perce AI, Richrds RG, Milz S, Schneider E, Perce SG. Animl models for implnt iomteril reserch in one: review. Eur Cell Mter Mr;13: Steigeng J, Al-Shmmri K, Misch C, Nociti FH Jr, Wng HL. Effects of implnt thred geometry on percentge of osseointegrtion nd resistnce to reverse torque in the tii of rits. J Periodontol Sep;75(9): Meredith N. Assessment of implnt stility s prognostic determinnt. Int J Prosthodont Sep-Oct;11(5): Volume 2 Issue 4/2016