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    Periodontology

    2000 Vol.

    17 1998 36-46

    Printed in Denm ark. All rights reserved

    C o p y r i g h t M u n k s g a a r d 1 9 9 8

    PERIODONTOLOGY 2000

    I SSN 0906-6713

    Surface configurationsof

    dental implants

    JAN

    EIR IKELLINGSEN

    The use and development of implants for restoring

    single or multiple loss of teeth has been through sev-

    eral phases to reach the optimal goal of having a per-

    manent, artificial anchoring of fixed bridges or

    crowns in the upper and lower jaw. This period,

    mainly based on trial-and-error approaches, has led

    to the development of different implant materials,

    designs and treatment techniques that have not al-

    ways led to the results expected or desired.

    More needs to be known about the optimal situ-

    ation of the connection between an artificial ma-

    terial and the tissues what type of material that

    gives the best tissue response and what type of sur-

    face is preferred by the bone cells or the cells in the

    soft tissue.

    If

    this is known, the response of the bone

    or soft tissue can be predicted when the implants are

    installed into the jaws.

    Today's implant materials function well when the

    bone quality is good and especially when there is

    bicortical anchorage. However, in many cases the

    situation is not optimal and regions have cancellous

    bone and a thin cortical lamellae. Although some re-

    Table 1. Different types of materials used in the

    body as biomaterials

    Gold

    Cobalt-chromium alloys

    Stainless steel

    Titanium

    Zirconium

    Niobium

    Tantalum

    Hydroxyapatite

    Bioglasses

    Tricalcium phosphate

    Carbon

    Polymers

    A 1 2 0 3

    cent reports (52, 66,

    72,

    85) indicate that good clin-

    ical results can be achieved even after shorter heal-

    ing time using the conventional implants, most re-

    search (1, 2, 4 18-21) shows that a relatively long

    healing period without any stress is needed to

    achieve a tight bony contact with the implant ma-

    terial. The healing time, however, depends on the

    bone quality, and one aspect of current research is to

    try to determine the best treatment modalities with

    reduced bone quality, particularly in the maxillary

    region.

    Another aim of biomaterial research is to improve

    the bone quality after implantation by introduction

    of active bone-inducing substances. Structures on

    the implant surface or in the tissues may also have

    such an effect.

    The current situation concerning the clinical use

    of implants is based on basic research and animal

    and clinical trials that have been performed at many

    institutions worldwide during the last

    3

    decades. The

    result of this activity is that treatment with implants

    is now generally accepted in dentistry if the treat-

    ment is done according to some accepted principles:

    cylindrically shaped implants, preferably with

    threads, and the surgical and the subsequent pros-

    thodontic procedures performed according to an ac-

    cepted protocol.

    However, with all respect to the research per-

    formed in this field, the state of the art today is

    mainly a result of trial-and-error approaches to op-

    timizing already known materials and methods.

    Scientifically based engineering of new materials to

    reach a specific goal is rare. Most biomaterials used

    in implantology are not specifically developed for

    this purpose but were available before they were

    used as biomaterials. Examples of these materials

    are listed in Table

    1.

    The materials form a heterogen-

    eous group consisting of metals, precious and non-

    precious, oxide forming, corrosive, more or less non-

    corrosive, ceramics and non-metals and non-cer-

    amics. The effects of these materials in bone

    36

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    Ellinasen

    sults obtained with this type of implants and is not

    based to the same extent on systematic biomechan-

    ical research and knowledge of the optimal bio-

    mechanical connection between the implants and the

    bony structures. Following an implantation, the im-

    plant goes through several phases in which stability

    and the transfer of loads are important. To obtain op-

    timal healing of the bone close to the implant surface,

    stability of the implant bed is important

    (22, 73,

    88).

    Introduction of threads to the cylindrically implant

    improves the implant stability significantly

    (41).

    Threaded cylindrical implants help the surgeon in

    placing the implant exactly in the pre-drilled cavity,

    and due to the threads the implant is stable and fixed

    during the healing process. This probably has clinical

    consequences. Screw-shaped implants have been

    found to be in closer contact with bone than are cylin-

    drical implants without threads

    (24).

    The observation

    of improved bone healing around screw-shaped im-

    plants has also been confirmed by Albrektsson et al.

    (5)

    in a long-term clinical trial. Different types of

    thread profiles have been used on the cylindrical im-

    plants but all with the same goal: to establish a stable

    fixation between the implant and the bony tissue and

    to improve load transfer.

    Introduction of threads on cylindrical implants

    leads to a change in the distribution of the stress ap-

    plied to the implant compared with cylindrically

    shaped implants (80).A cylindrically shaped implant

    will largely transfer the stress to the apical part with

    axially directed loads and probably to the neck and

    apical part with horizontally directed loads. When

    bone implants are designed, attention should be di-

    rected towards distributing the loads evenly in the

    bone. This will reduce the possibilities for overloading

    the bone, and according to Wolff's law, induce bone

    remodeling

    or

    bone formation. Both excessive and in-

    sufficient stress have been suggested to promote bone

    resorption at the neck region (30,811.

    Overloading was suggested as a main causal factor

    behind loss of Brinemark (Nobel Biocare AB, Gote-

    borg, Sweden) implants (68). The same group found

    improved results with longer implants compared

    with shorter ones, further indicating that over-

    loading is a major factor in the loss of dental im-

    plants.

    An

    even distribution of loads in the bone thus

    increases the load-carrying capacity of the implant.

    Although the bone structure differs between differ-

    ent types of cancellous bone and cortical bone areas,

    studies have been performed to identify an optimal

    thread profile. Frandsen et al. (41) observed an in-

    creasing retention with increasing screw diameter

    and increasing thread length when testing the hold-

    ing power of four different screws implanted in can-

    cellous bone of cadaveric femoral heads.

    Most cylindrically threaded implants have a

    thread profile similar to machined screws. It has

    been argued that this is not an optimal profile in

    bone. Other groups have therefore constructed im-

    plants with different thread profiles and a different

    angle of the thread flank (Fig.

    2)

    (82). It is debated

    whether these changes in thread profiles have any

    real clinical significance. Both systems with different

    thread types have demonstrated long-term clinical

    success

    (1, 20).

    In a recent thesis, Hansson et al. (50) present an-

    other threading profile with minute threads with a

    depth of only 0.1 mm (Fig. 3). These authors argue

    that this type of threads have improved capacities to

    carry load compared with the regular type of threads,

    such as those on Branemark implants

    (50).

    These findings are in accordance with recent

    findings by Wong et al. (94) that demonstrated im-

    proved push-out strength for implant surfaces with

    many small peaks compared with a surface with

    high, but few peaks.

    Surface microstructure

    Fig.

    3.

    Example of an implant with a combination

    of

    microthreads and conventional threads: Astra Tech ST

    Molndal, Sweden)

    Another important factor of the surface configur-

    ation is the microstructure of the implant surface.

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    Surface configurations of dental implants

    This can vary considerably depending on the surface

    treatment of the implant. Variation of the surface

    microstructure has been reported to influence the

    stress distribution, retention of the implants in bone

    and cell responses to the implant surface.

    Gross et al. (45) investigated the in vivo responses

    to pellet-blasted or flame-sprayed cylinders made of

    titanium and Ti,+414V lloy, and furthermore to ti-

    tanium rods flame sprayed with hydroxyapatite,

    which were implanted into rabbit femurs. The

    authors concluded that, independent of the implant

    chemistry, each implant should have a micro-rough-

    ness that

    allows

    fixation of trabeculae and conse-

    quently a transmission of forces. The implants with

    rough surfaces had improved bone response, with

    bone trabeculae growing in a perpendicular direc-

    tion to the implant surface.

    An improved retention in bone has also previously

    been reported after implantation of rough-surfaced

    implants.

    Several authors have discussed the dimension of

    the ideal roughness that would provide increased re-

    tention and an improved bone response. The rough-

    ness can be considered on different levels: macros-

    tructural, microstructural and ultrastructural, and

    roughness on these different levels probably has dif-

    ferent effects on the living tissues. It has been estab-

    lished in the literature based on several studies that,

    to gain complete growth of bone into a materials

    irregularities, these need to be at least

    100

    pm in size.

    Growth of bone into cavities or pores of this size will

    give a mechanical interlocking of the material with

    bone. This was demonstrated by Bobyn et al. (12) in

    studying cobalt-based alloys with pore sizes of 50-

    400 pm, Bone ingrowth was also observed by Cle-

    mow

    et al.

    (29)

    when this group studied porous coat-

    ed

    Ti l,V

    femoral implants with pore sizes ranging

    from 175 to 235 pm.

    The optimal pore size to obtain bone ingrowth

    might also depend on the material. Breme et al. (14)

    stated that titanium alloy implants had an optimal

    pore size of 100 pm. Increased removal torque values

    were, however, also found when

    using

    titanium

    po-

    rous-coated screws of stainless steel with a pore size

    of 10-40 pm. These small pores do not allow a maxi-

    mal ingrowth of bone but may give increased reten-

    tion based on mechanical interlocking. This has

    also

    been stated by Predecki et al. (67) in a study of bone

    ingrowth to titanium and aluminum implants with

    channels with diameters of 95-1000 pm. This group

    reported the fastest bone ingrowth into channels

    with diameters of 500-1000 pm, and no ingrowth

    smaller scale was, however, found to be important

    for integration of the bone with the implant surface.

    These findings indicate that other mechanisms, not

    purely based on mechanical interlocking, determine

    the reactions between bony tissue and biomaterials.

    Although surface roughness on a micrometer scale

    gives some retention due to bone ingrowth,

    in vitro

    cell studies indicate that this property of the surface

    influences the function of the cells, the matrix depo-

    sition and the mineralization (13, 64, 78). Cells seems

    to be sensitive to microtopography and appear to be

    able to use the morphology of the material for orien-

    tation and migration

    116,

    25 , 2 6 . The maturation of

    the cells also affects the response to the surface

    roughness, which is in agreement with earlier obser-

    vations that indicated that chondrocytes are affected

    differently by local factors such as vitamin

    D

    and

    transforming growth factor

    p

    depending on the

    stages of maturation of the cells

    13,

    76-78, 84).

    Microtopography may therefore be one factor that

    influences the differentiation of mesenchymal cells

    into fibroblasts, chondrocytes or osteoblasts. Based

    on these studies, the authors hypothesized that

    osteogenesis may be favored by vascular ingrowth,

    whereas a limited vascular ingrowth may induce

    chondrogenesis.

    Implants exhibiting a micro-roughness on their

    surface have been tested and used both in animal

    studies and in human patients. Buser et al.

    (20)

    in-

    vestigated the correlation between different surface

    structures and the bone response, as measured by

    bone-to-implant contact. The surfaces investigated

    in that study included titanium plasma-sprayed ti-

    tanium, sandblasted and acid-etched titanium as

    Fig.

    4.

    Scanning electron micrograph

    with

    high resolution

    x503) of the surface of a machined, threaded implant

    fNobel Biocare Mark 111

    nto the 95-pm channels. Surface roughness on a

    .~

    _

    39

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    Fig. 5. Scanning electron micrograph with high resolution

    x503) of the surface

    of

    a titanium plasma-sprayed

    threaded implant

    IT1

    Bonefit)

    well as hydroxyapatite-coated titanium. The authors

    reported a positive correlation between increased

    roughness and bone contact measured by histologi-

    cal techniques. Titanium surfaces may also be blas-

    ted with T i 0 2 particles to give micro-roughness. In

    a clinical study in dogs, the biological response to

    implants with this surface was compared with ma-

    chined titanium. The authors reported significantly

    higher removal torque values for the blasted im-

    plants

    (44)

    (Fig.

    4-6).

    The ideal surface roughness for bone implants on

    a micrometer scale probably depends on the distri-

    bution of cortical or cancellous bone and on the

    level of loading to the implants. Nevertheless, an op-

    timal surface roughness has been proposed based on

    experimental studies. In a series of studies, Wenneb-

    erg et al. systematically investigated the effect of sur-

    face roughness of implants and the response in rab-

    bit bone (90-93). The implant surfaces were char-

    acterized by profilometry as well as with a three-

    dimensional laser technique. Titanium implants

    with four different surface structures were created by

    blasting with A12 3or Ti02 in addition to the ma-

    chined surface. The surfaces were blasted with 25-

    pm particles of

    T i 0 2

    or 25-pm, 75-pm or 250-pm par-

    ticles of A1203.The authors concluded that implants

    with a surface roughness of Sa 1 to 1.5 pm seemed

    to be at an optimal roughness with regard to reten-

    tion in bone as well as bone-to-implant contact as

    measured by histomorphometry. This optimal sur-

    face was created by blasting with 25- to 75-pm par-

    ticles and resulted in surface roughness of Sa=0.83

    and Sa=1.29 respectively.

    A

    rougher surface as

    created by 250-pm particles led to a surface rough-

    ness of Sa=2.11 and did not result in an improved

    bone response. Implants treated with the 25-pm par-

    ticles had significantly more bone-to-implant con-

    tact than implants treated with the 250-pm particles

    when the three best threads were considered.

    No

    sig-

    nificant differences could, however, be detected

    when the authors recorded the bone-to-implant

    contact to all threads on the screw implants. Blasting

    the titanium implants with 250-pm particles did not

    improve the retention of the implants in bone.

    Al-

    most identical removal torque values were recorded

    when the implants blasted with 25-pm particles and

    250-pm particles were removed. The observation of

    an improved response of bone to implants with a

    surface roughness of Sa 1.0-1.5 pm is also in accord-

    ance with observations by von Recum van Kooten

    (89) that reported excellent tissue attachment with-

    out signs of inflammation when implanting filter

    membranes with pore sizes of 1-3 pm. Based on

    these results, it seems that the benefit of increasing

    roughness on a micrometer scale reaches a maxi-

    mum level between 1.0 and 1.5 pm. Above this level

    no further positive response in the bone can be ex-

    pected. This observation indicates that the findings

    from in

    vitro

    cell experiments that bone cells are ru-

    gofile and respond positively with increased matrix

    deposition and mineralization are also true in an in

    vivo situation. This may be because the less rough

    surfaces to a certain extent stimulate the bony tissue

    through loading, which in return responds with in-

    creased bone growth. Another, or additional inter-

    pretation of the findings of Wennerberg et al. (90-

    93) could be that the rugofile bone cells recognizes

    the surface prepared by the course particle, as a

    Fig.

    6.

    Scanning electron micrograph with high resolution

    X503) of the surface of a titanium dioxide-blasted

    threaded implant Astra Tech TiO-blast)

    40

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    urface configurationsof dental implants

    smooth surface, whereas the 25-pm particles creates

    a rough surface that is identified by the osteoblasts

    (Fig.

    7).

    Surface ultrastructure

    Although micro-roughness seems to be an important

    characteristic for tissue response to biomaterials,

    there are also observations that indicate a biological

    response to irregularities on the nanometer level.

    Larsson et al. 59-61) studied the biological effect of

    changing the oxide thickness of titanium implants

    from an electropolished level, to thick oxide layers

    formed by anodization. By this treatment the surface

    changes from an amorphous metal surface with a

    noncrystalline oxide to a polycrystalline metal sur-

    face with a crystalline oxide layer. Analysis of these

    surface at a high resolution level demonstrated that

    the new surface was heterogeneous with mainly

    smooth areas of thick oxide but separated with po-

    rous regions on a nanometer level. This observation

    of an increased roughness after anodization of ti-

    tanium was in line with earlier transmission electron

    microscopic studies demonstrating increased pore

    sizes with increased oxide thickness (58). Implants

    with this thick, heterogeneous oxide seemed to have

    a slightly improved response in bone, particularly in

    the first weeks after implantation. This difference

    could, however, not be observed after longer healing

    periods. This is in accordance with earlier obser-

    vations by Ellingsen Videm

    36)

    that did not show

    any significant correlation between oxide thickness

    on titanium implants and the bony response. The

    latter observation was measured by push-out experi-

    ments and histomorphometry, after 8-week healing

    of titanium implants in rabbits. These authors ar-

    gued that the outermost molecular layers of the bio-

    material are the important part for the bone re-

    sponse, because the surface chemistry

    of

    these

    layers is exposed to the tissue. Morphological

    changes on a nanometer level may introduce ad-

    ditional effects to the tissue response which, in turn,

    can further improve the bone healing.

    The surface chemistry of the

    implants

    The chemical properties

    of

    the biomaterial surface

    play an important role for the tissue responses

    elicited by the material. This is at least one main rea-

    Fig. 7. Bone cells exposed to a medium rough and a very

    rough surface. The rugofile bone cells may recognize the

    very rough surface right) as

    a

    smooth surface, whereas

    the medium rough surface left) is recognized as a trough

    rough surface by the osteoblasts.

    son why the tissues responds differently to different

    materials. A material with a surface that is accepted

    by the tissue seems to exhibit improved integration

    with bone, either due to passive growth, leading to a

    tight connection between implants and bone, or by

    stimulation that probably leads to a bone-implant

    bonding. This is probably the case with the two main

    materials used in dental implants, hydroxyapatite

    and titanium. The calcified parts of the bone con-

    sists of hydroxyapatite (or rather carbonated apa-

    tite), and introducing this substance as an implant

    material often gives favorable responses in the bone.

    The chemical structure of the hydroxyapatite is,

    however, important, and small changes in this sur-

    face chemistry may have biological consequences.

    This was observed in a recent study 11) investigat-

    ing the osteoblastic responses to synthetic hydroxy-

    apatite powders supplied by different manufac-

    turers. Although both powders was shown to have a

    phase-pure hydroxyapatite structure as indicated by

    X-ray diffraction analysis, the calcium-to-phosphate

    ratio deviated significantly from the stoichiometric

    value for hydroxyapatite; one was rich in calcium

    and the other slightly calcium deficient. There were

    also small differences in impurities of carbon, so-

    dium, silica and alumina. The authors observed that

    one material seemed to be inferior to the other

    based on the way that the osteoblasts reacted. The

    cells cultured on this material had half the amount

    of alkaline phosphatase and DNA as the cells cul-

    tured on the other hydroxyapatite material. It seems

    justified to do similar experiments

    in

    viva

    In some elegant studies, Hanein et al.

    (47-49)

    demonstrated that cell adhesion

    is

    sensitive to vari-

    41

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    Ellingsen

    ations in the surface organization of the material on

    the atomic level. This group has tested the adhesion

    of epithelial A6 cells to chemically equivalent but

    structurally distinct phases or surfaces of calcium

    (R,R)-tartrate tetrahydrate crystals. The observations

    demonstrated that the outermost molecular layers of

    a surface influence the interaction between the cells

    and the biomaterial.

    The biological effects of modifying the biomaterial

    surface have also been elaborated by our group

    31,

    35-38). In an attempt to study the effect of the oxide

    layer of titanium on calcium-phosphate precipita-

    tion, titanium-dioxide(TiOz) and powder of oxidized

    and nonoxidized titanium were introduced into an

    in uitro nucleation test system 31). In this system

    we found that titanium powder enhances calcium-

    phosphate nucleation only after prolonged pre-in-

    cubation in an aqueous buffer, or after autoclaving.

    These treatments enhance the growth of the oxide

    layer. Calcium phosphate crystals could be identified

    on the surface

    of

    the oxidized titanium powder.

    X-

    ray diffraction analysis of the precipitates revealed

    the pattern of poorly crystalline hydroxyapatite. This

    observation indicated that the oxide content, or

    structure, is required for titanium to act as a nu-

    cleation substrate. Even more effective nucleation

    was observed when pure TiOZ was used as a nu-

    cleation substrate. The presence of serum proteins,

    as in the body, will probably mask the reaction sites

    and interfere with the capacity of these substances

    to induce nucleation. This effect was observed in the

    present study, but to a lesser extent when pure TiOa

    was present as nucleation substrate. The nucleation

    capacity and formation of calcium phosphate pre-

    cipitates is related to the biocompatibility of ti-

    tanium, and enhanced nucleation capacity may in-

    dicate improved biocompatibility.

    The biological activity of the TiOZ probably also

    influences the protein adsorption to titanium. In an

    in uitro study, serum proteins seemed to adsorb to

    titanium dioxide by the same mechanisms as to hy-

    droxyapatite through calcium binding

    35).

    The

    surface characteristics of TiOZprobably change from

    an anionic to a cationic state by the adsorption of

    calcium to the surface. This will subsequently in-

    crease its ability to adsorb acidic macromolecules,

    such as albumin, a property demonstrated for hy-

    droxyapatite (9,

    10).

    Manipulation of the surface oxide layer of ti-

    tanium results in modification of the surface prop-

    erties of the biomaterial with consequences for its

    biological properties. This was demonstrated in a

    study in which TiOZwas pretreated with lanthanum

    37).Lanthanum ions (La3+)are known to have high

    affinity for binding sites usually occupied by cal-

    cium. Lanthanum pretreatment of TiOz alters the

    properties of this substance, as shown by both in ui

    tro and in uiuo tests. The total capacity for adsorp-

    tion of serum proteins increased, and the amount of

    albumin adsorbed to TiOZ pretreated with lantha-

    num was shown to be more than five times increased

    compared with untreated TiOz. Marked effects by

    this modification were also observed in uiuo when

    TiOz was implanted subperiosteally on the rats

    sculls. Untreated TiOZ resulted in no adverse reac-

    tions from the tissues, as demonstrated by a tight

    connection between the TiOz powder with new bone

    formation after 4 weeks and no indication of bone

    resorption. Implantation of the lanthanum-pre-

    treated TiOz resulted in the formation of a layer of

    fibrous tissue with mononuclear cells that separated

    the implant material from the bone. A similar ten-

    dency was also observed when metallic titanium im-

    plants were pretreated with lanthanum and im-

    planted in rabbits and evaluated by the use of a

    push-out test. The lanthanum-pretreated implants

    had a significantly looser fit than untreated titanium

    implants.

    The mechanisms that lead to bone-bonding or to

    a firm connection between the biomaterial and bone

    are not completely known. The increased adsorption

    of proteins to lanthanum-treated TiOZ means that

    these proteins may therefore well contain more in-

    hibitors of mineralization than the proteins that ad-

    sorb to pure TiOz. Proteoglycans are important

    modulators in the mineralization of bone and may

    interact with mineral crystallites as an important

    stage in the control of mineral growth

    33, 87).

    Fluoride ions have documented activity in bone.

    This element is known to form fluoridated hydroxy-

    apatite or fluorapatite with improved crystallinity

    and better resistance to dissolution than hydroxy-

    apatite 8, 42). Fluoride also enhances the incorpor-

    ation of newly formed collagen into the bone matrix

    and increases the rate of seeding of apatite crystals

    as well as increasing trabecular bone density and

    stimulating osteoprogenitor cells number in uitro (6,

    79). The alkaline phosphatase activity, which is an

    indication of the bone formation, was also elevated

    after introduction of fluoride in an in uitro study

    40).Titanium fluoride forms a stable layer, a glaze,

    when applied onto tooth surfaces

    (86).

    This stable

    layer is assumed to consist of titanium, which shares

    the oxygen atoms of phosphate on the hydroxyapa-

    tite surface, giving a covalently bonding between ti-

    tanium and the hydroxyapatite.

    4

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    Surface configurations of dental implants

    titanium-bound oxygen and forms a titanium-fluor-

    ide compound. When fluoride-modified titanium

    implants are implanted into bone, the surfaces are

    exposed to phosphate from the bone at a neutral pH.

    This will make possible a reaction in which the oxy

    gen in phosphate replaces the fluoride and binds to

    titanium to create a covalently binding between

    bone and titanium. The fluoride ions released by this

    process may thus catalyze the new bone formation

    in the surrounding tissue through the bone-stimu-

    lating mechanisms discussed above (Fig.9). Fluoride

    has also an inhibiting effect on the proteoglycan and

    glycosaminoglycan adsorption to hydroxyapatite,

    which may further improve the bonding to bone (34,

    46, 71). ~~~~~~~l~~~~~nd

    g~ycosam~nog~ycans

    re

    known to inhibit mineralization 39).

    The surface qualities are

    Of

    utmost importance in

    establishing of a reaction between the implant and

    the tissues. This concerns the surface structure as

    well as its chemical and biological properties. Much

    attention has been focused on the importance of the

    macrostructure of the implants for establishing re-

    tention in the bone. More attention will probably be

    focused in the future on the biological effects of the

    surface structure on the microstructural and ultra-

    structural levels as well as on the surface chemistry

    of the implants. Progress in these fields based on

    knowledge of the biological effects may provide im-

    plants with improved tissue response and clinical

    performance in the future.

    Fig. 8. Scanning electron micrograph of a fluoride-modi-

    fied implant after the push-out procedure. The implant is

    partly right side) covered by bone that is firmly fixed to

    the implant surface, which indicates bonding between the

    titanium implant and bone.

    References

    Fig. 9. A possible mechanism between the fluoride-modi-

    fied titanium and bone. Oxygen in phosphate may replace

    the fluoride and bind to titanium to create a covalently

    binding between bone and titanium. The fluoride ions

    which are released by this process may thus catalyze the

    new bone formation in the surrounding tissue.

    When nonthreaded smooth surfaced titanium im-

    plants with a fluoride-modified oxide layer were in-

    stalled into rabbits, significantly increased retention

    in the bone was observed after a push-out test pro-

    cedure (38). This was observed after a 4-week heal-

    ing period, but an even more pronounced effect was

    observed after an 8-week healing period. Scanning

    electron microscopic analyses of the retrieved im-

    plants revealed that the fluoride-coated implants

    were partly covered by bone that had fractured in-

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