Article history:Received 18 June 2012Received in revised form 21 September 2012Accepted 1 December 2012Available online 8 December 2012
Keywords:Metal foamMetal releaseImplantSimulated body fluidArtificial saliva
Highly porous 17-4 PH stainless steel foam for biomedical applicationswas produced by space holder technique.Metal release and weight loss from 17–4 PH stainless steel foams was investigated in simulated body fluid andartificial saliva environments by static immersion tests. Inductively coupled plasma-mass spectrometer wasemployed to measure the concentrations of various metal ions released from the 17-4 PH stainless steel foamsinto simulated body fluids and artificial saliva. Effect of immersion time and pH value on metal release andweight loss in simulated body fluid and artificial saliva were determined. Pore morphology, pore size andmechanical properties of the 17-4 PH stainless steel foams were close to human cancellous bone.
Metal foams offer opportunities for a wide range of applications,such as energy absorbers, heat exchangers and biomedical implants[1–4]. Space holder technique has been used to produce foams fromstainless steels and titanium which have high melting temperatures.This process also produces open-cell structure with sufficient porositysuitable for biomedical applications [5–7]. Open-cell foams exhibit a po-rous structure similar to cancellous bone. Use of metal foam as implantallows mechanical anchorage of bone with implant by bone tissue in-growth into the pores. Additionally, by adjusting the porosity, stiffnesscan be controlled in order to reduce the stress-shielding effect betweenimplant and bone [5–8]. Requirements for implant materials are bio-compatibility, open porosity, low density, corrosion resistance, wear re-sistance and sufficient mechanical strength close to bone [8–11].
Corrosion of biomaterials is critical because it can affect the biocom-patibility andmechanical integrity. Release ofmetal ions can result in ad-verse reactions including toxicity, carcinogenicity and genotoxicity [12].Stainless steels, Ti alloys and Co alloys are widely used as load-bearingimplants. Implants fabricated from Co-based alloys produce elevatedCo, Cr and Ni concentrations. Ti–6Al–4V alloy has been used as implantand the cytotoxicity of V is an issue of concern. V is considered to be anessential element, but may become toxic at high levels [13]. Cr toxicityis related to its valence state. Cr3+ is the actual agent of toxicity. Corro-sion resistance of stainless steels is a function not only of chemical com-position but also of microstructure, surface condition, and production
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route, all of which may change the thermodynamic activity of surface[14,15].
The environment of the human body is buffered so that the pH ismaintained at ~7.40 at 36.5 °C. Different parts of body may have differ-ent pH and oxygen concentrations. Moreover, pH can change in tissuethat has been infected. In a wound, pH can be ~3, and in an infectedwound pH can increase to ~9 [16,17]. Two features control the severityof this environment. Firstly, the saline solution is an excellent electrolyteand facilitates corrosion. Secondly, there aremolecules that catalyze cer-tain reactions. Corrosion behavior ofmaterials can be studied using sim-ulated body fluids (SBF) which simulates the inorganic part of bloodplasma. These tests are focused on the examination of materials andprovide information to evaluate their suitability for biomedical applica-tions [18–22]. A comparison of nominal concentrations of ions in humanplasma and in simulated body fluid at pH of 7.4 is given in Table 1.
Metals that are used in dentistry are exposed to changeable condi-tions of oral environment. Saliva contains organic and inorganic sub-stances suspended in an aqueous medium. The pH of saliva may varybetween 2 and 11 while the temperature may be between 0 and70 °C. Saliva is dependent on the age, eating habits, and oral hygiene[23–25]. Hence, corrosion behavior and metal release of materials fordental applications must be studied in artificial saliva.
In the present study, we characterized the 17-4 PH stainless steelfoams for biomedical applications by immersion tests in simulatedbody fluid and artificial saliva. The 17-4 PH stainless steel is used for ap-plications in the aerospace, chemical and food processing industries andin biomedical applications. Traditional AISI 316L and AISI 304 austeniticstainless steels are used in biomedical applications. However, thesesteels contain high amount of Ni to maintain their austenitic micro-structure. Nickel may lead to metal sensitivity when released. 17-4 PH
NaCl 0.40CaCl2 2H2O 0.79KCl 0.40NaH2PO4 2H2O 0.78Na2S 9H2O 0.005Urea–CO(NH2) 2 1.00Distilled water 1000 ml
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stainless steel has relatively lower Ni content than these austeniticstainless steels. In addition, 17-4 PH stainless steel has higher mechan-ical properties and its mechanical properties can also be improved byaging. In metal foams, mechanical properties are connected to density.In the foams, density cannot always be varied and in order to controlmechanical properties, heat treatment is desirable. 17-4 PH stainlesssteels offer a combination of strength, ease of heat treatment (aging),and corrosion resistance not found in any other steel grade. The advan-tages of steel foams are their ability to provide mechanical anchoragefor the surrounding tissue via ingrowth of tissue into pores, low densityand sufficient strength close to bone. For implants, the effect of implanton body and effect of body on implant are major considerations beforeimplant is approved for use. In the present study, 17–4 PH stainless steelfoams were immersed in simulated body fluids and artificial saliva.Metal release and weight loss was determined. Effects of pH and im-mersion time on metal release were investigated.
2. Experimental
Starting material for foam production was 17–4 PH stainless steelpowder (Carpenter, Sweden) with spherical morphology. The chemicalcomposition of the powder was Fe, 4.6 wt.%; Ni, 15.2 wt.%; Cr, 0.7 wt.%;Mo, 0.4 wt.%; Nb, 4.9 wt.% Cu, 1.4 wt.%; Si, 0.07 wt.% C. Mean particlesize of the steel powder was 14.6 μm. As a space holder, carbamide(Merck, Germany), in the fractions of 1000–1400, 710–1000, 500–710 μm with irregular shape and the fraction of 1000–1400 μm withspherical shape, was used for its high solubility in water. To enhancesintering process, 0.5 wt.% boron (Merck, Germany) was added to steelpowder to create a liquid phase during sintering. The binder for greenstrength was polyvinylalcohol (PVA), supplied by Merck, Germany.2.5 wt.% PVA was added to the steel.
The mixture was compacted at 180 MPa into cylindrical specimenswith a diameter of 12 mm and different heights. Green specimenswere immersed in water at room temperature and ~90% of the carbam-ide was leached out in ~10 hours. Thermal debinding temperature ofthe PVAwas determined to be 410 °C by using thermogravimetric anal-ysis (TA, SDT Q600). The PVA in the green specimens was thermally re-moved as part of sintering cycle, which consisted of heating at a ramprate of 5 °C/minutes to 410 °C (debinding) with a dwell time of 40 mi-nutes, followed by heating at rate of 10 °C/minutes to sintering temper-atures. The foams were sintered at 1260 °C for 40 minutes in H2.
Kokubo's simulated body fluid and Hank's simulated body fluidwere prepared from calculated amounts of chemicals supplied byMerck, Germany according to procedure described in the literature[12,13,18]. The amount of reagents for preparation of simulated bodyfluid solutions is given in Table 2.
In preparation of Kokubo's SBF solution, firstly 750 ml of distilledwater was put into a 1000 ml beaker. The temperature was kept at~37 °C. Reagents, which were listed in Table 2, were added into thewater until the tris (tris-hydroxymethylaminomethane). The pHwas measured and monitored using a pH meter (WTW, inoLab 720,Germany). After the addition of the tris, the temperature of the solu-tion was checked, and the electrode (WTW, SenTix 81, Germany) of
the pH meter was placed in the solution. After the adjustment of pH,the solution was transferred from the beaker to a volumetric flask.Distilled water was added to the solution to adjust the total volume to1000 ml. The pH of Kokubo's SBF is adjusted to 7.40 (human bodycondition), by adding 50 mM of tris and 45 mM of HCl. Solutions withpH values of 3.0 and 5.0 were also prepared to study the effect of pHon metal release. Preparation procedure of the Hank's solution wasalso included the similar steps. The reagents, which were listed inTable 2 for Hank's solution, were added to distilled water in the orderthey are listed. The pH of the solution was measured as 6.70.
The artificial saliva composition used in this study conformed to thatdescribed by Fusayama et al. [23,25] and the recipe is presented inTable 3. The pH of the prepared artificial saliva was 5.50. In addition, be-cause the short-termpHvariations of human saliva include the intake ofacidic beverages (pH of ~2.0) and secretion of gastric acid (pH of ~1.0),lactic acid was also added to artificial saliva to decrease the pH to 2.30.
Seventy percent porous specimens were cut along longer axes andsemi-cylindrical specimens were obtained. Thus, maximum solidsurface area exposured to solution was obtained. Then, the specimenswere machined and polished. Total porosity and surface area of eachspecimen was equal in immersion tests. Samples were then exposedto simulated body fluid and artificial saliva in closed polyethylenebottles. Foams with equal porosity levels were immersed in solutionsat 37 °C for several soaking times up to 7 days. Solution volume tospecimen surface area ratio was constant in all tests. The inductivelycoupled plasma-mass spectrometer, ICP-MS, (Thermo Scientific Ele-mental X Series 2) was employed tomeasure the concentrations of var-ious metal ions like Fe, Cr, Ni, Cu and Mo which might be released. Asolution without a specimen was used for the blank. After differentsoaking periods, foams were removed from the solutions. The driedspecimens were weighed and the weight loss was determined. Thearea of the pores was subtracted from total surface area of the foamsto find actual solid surface area.
Themicrostructure of foamswas examined by scanning electronmi-croscopy (SEM), Jeol 5600 and by optical microscope (Nikon, ME600).Energy dispersive spectroscopy (EDS) analysis was carried out to studythe chemical composition (IXRF, 550i model EDS). The digital images
Fig. 1. (A) Photograph of the sintered 17-4 stainless steel foams, (B) SEM image fromcrack surface of the 17-4 PH stainless steel foam.
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were used to determine mean pore size and shape by image analyser(Clemex Vision, PE). Total porosities of the foams were determinedfrommeasurements of weights and dimensions of specimens. Open po-rosity was measured by Hg porosimeter (Quantachrome Poremaster).Mechanical properties were studied by the compression tests (Zwick-Roell Z050, Germany). Surface roughness parameters (average rough-ness Ra, maximum height of the profile, Rt and average maximumheight of the profile, Rz) were determined by using Mitutoyo, SurftestSJ-301 surface roughness tester. The energy absorption is also an impor-tant property of the foams. Thus, energy absorption of the foams wasdetermined by using Zwick–Roell materials testing machine. The ener-gy absorption is defined as the energy necessary to deforma given spec-imen to a specific strain and is the area under the compressive stress–strain curve up to densification strain.
Biocompatibility of the foams was studied by XTT [2,3-bis-(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboksianilide in-nersalt] in vitro cytotoxicity assay. XTT assay provides a method for de-termination of live cell number,which is used to assess cytotoxicity. XTTmeasures cell viability based on the activity ofmitochondria enzymes inlive cells that reduce XTT and are inactivated after death of cell. Theamount of product generated from XTT is proportional to the numberof living cells and can bedetermined spectrophotometrically. Cytotoxic-ity of sterilized foams was evaluated in L929 mouse fibroblast cell cul-ture. Positive and negative control articles were prepared to verify theproper functioning of the system. After incubation, at 37 °C in a humid-ified atmosphere, containing 5% CO2, XTT/PMS labelling solution (finalXTT concentration: 0.3 mg/mL) was added to cell culture and the cul-ture incubated for another 4 hours. Absorbance (optical density) mea-surements were performed at 450 nm using a spectrophotometer(Shimadzu BioSpec-1601, Japan).
3. Results
In thepresent study, 17–4 PH stainless steel foamswere produced byspace holder technique. Fig. 1 (A) shows the photograph of the sinteredfoams and Fig. 1 (B) shows SEM image from crack surface of the foam.Since the open porosity is important for tissue ingrowth, the amountof open porositywas determined. Total porosity of the 17–4 PH stainlesssteel foams consists of ~80–90% open and ~10–20% closed porosity.There were also some micropores on the edges of the macropores andon cell walls with a size of a few microns. A certain amount of micro-pores is expected to be beneficial to vascularization in implants.
Porosity and pore size both play a role in bone ingrowth. The mini-mum requirement for pore size is considered to be ~100 μm due tocell size, migration and transport, and higher porosity and larger poresize result in greater bone ingrowth. For the pores with size less than100 μm, cells did not grow into the pores because of spanning of poresby cells. The pore size andmorphology of the foams replicated the initialsize and morphology of the carbamide particles. In the present study,pore size of the foams, which were produced by fraction of 710–1000 μm carbamide, was ~600 μm, which is suitable for biomedical ap-plications. Pore morphology was also investigated in terms of sphericityand found to be ~0.57, while sphericity of carbamide particles was~0.64. The decrease in the particle size and sphericity was attributedto crushing of the carbamide particles during pressing and to moisten-ing. Fig. 2 shows SEM image of the foams which were produced from(a) spherical carbamide, and (b) irregular carbamide.Mean spherical di-ameter (pore size) distribution of the steel foamwas illustrated in Fig. 3.The size and shape of carbamide particles and resulting pore size andshape of the foams were summarized in Table 4.
Compressive yield strength and Young's modulus of the foams,which having porosities between ~40% and 80%, were in the ranges of~50–290 MPa and ~0.5–5.0 GPa respectively. In particular, compres-sive yield strength and Young's modulus of the 70% porous steelfoams were ~70 MPa and ~0.60 GPa respectively. The mechanicalproperties of the foam, which are aimed to use in implant applications,
must fall in the range of cancellous bone. Meanwhile, compressive yieldstrength and Young's modulus of human cancellous bone are in theranges of 40–150 MPa and 0.09–1.5 GPa respectively [9]. As a result,mechanical properties of the foams, especially those having ~70–80%porosity, were close to cancellous bone. Fig. 4 shows the effects of po-rosity on the Young's modulus and compressive yield strength of thefoams. It is clear that the porosity affects the Young'smodulus and com-pressive yield strength.
Determination of the chemical interaction of metallic implants withthe body fluids is essential in order to understand their stability in thebody. The quantities of primary metal elements released from 17-4 PHstainless steel specimens into simulated body fluid and artificial salivaat 7 days of soaking time are compared in Fig. 5.
Fig. 6 shows the influence of immersion time on quantity of metalsreleased from 17-4 PH stainless steel foams into Kokubo's simulatedbodyfluid at pH of 7.4. As seen from Fig. 6, the quantity of metal ions re-leased from steel foams slightly increased with increasing immersiontime. Fig. 7 shows the effect of immersion time on quantity ofmetals re-leased from specimens into Hank's solution and similar behavior wasobserved.
Fig. 8 illustrates the effect of pH on the quantity of released metalfrom steel foams into Kokubo's simulated body fluid solution for7 days of immersion time. As seen from Fig. 8, the quantity of Fe re-leased from 17-4 PH stainless steel specimen was decreased with in-creasing pH value. The effect of pH on quantity of Cu released fromthe 17-4 PH stainless steel specimen was small. The quantity of Ni, Crand Mo released from stainless steel specimens gradually decreasedwith increasing pH value.
Fig. 9 shows the effect of pH on quantity of metals released from17-4 PH stainless steel specimens into artificial saliva solution for7 days of immersion time. Fig. 10 shows the effect of immersion time
Fig. 2. SEM image of the 17-4 PH stainless steel foams (A) produced from spherical carbam-ide, (B) produced from irregular carbamide.
Table 4Mean size and shape of carbamide particles andmean pores size and shape of the sinteredfoams.
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on metal release from foams into artificial saliva. It can be said fromFigs. 9 and 10 that, increasing immersion time and decreasing pHvalue increased the quantities of released metal ions in artificial saliva.
It can be said from the static immersion tests results that there wasnot a higher metal ion release than reference levels of these metal ionsin human body fluids [26–28]. This was attributed to the resistance ofstrong passive film on the 17-4 PH stainless steel. Biological risks ofmetal ions include wear debris, organometallic complexes, free metalions, and metal salts or oxides. Organometallic complexes are formedby metal ions binding to proteins. Proteins increase corrosion rate of
Fig. 3. Mean spherical diameter (pore size) distribution of the steel foam.
an implant by increasing the dissolution of metals. The only ion takenup by red blood cells following corrosion is Cr6+. Ni atom is verysmall and has a low affinity for blood cells. Despite the fact that Ni isan essential element in body, the maximum daily intake should not ex-ceed ~500 μg, and threshold concentration of ~30 ppm is required totrigger any cytotoxic response. In this study, observed Ni levels are neg-ligible compared with daily intake of Ni. Transition metals in toxicdoses, especially Cr and Ni, disrupt the body's oxidation–reduction bal-ance and, can cause increase in the body's pH value. Ni2+ substitutes es-sential elements like Ca2+, Mg2+ and Zn2+ in proteins and enzymesand then modifies their structures [26–28].
Fig. 11 shows the relationship between weight loss and immersiontime in the 70% porous foams. The data shown in Fig. 11 indicate thatweight loss was slightly increased with increasing immersion time, inall solutions. In general, weight loss values of the 17-4 PH stainlesssteel foams were small. Relatively rapid increase in the weight losswas observed in the initial immersion period and further increase in im-mersion time caused a slight increase in the weight loss. It can be saidfrom these results that the 17-4 PH stainless steel foams have an appro-priate resistance to weight loss in both simulated body fluid and artifi-cial saliva. Fig. 12 shows the effects of porosity and pore size onweight loss. As seen from Fig. 12, as the porosity was increased andthe macro-pore size was decreased, the weight loss was increased,due to increase in the actual surface area, while the corrosion potentialdid not change.
Fig. 13 shows the SEM images from the surfaces of the 17–4 PHstainless steel foam, before and after 7 days of immersion. It can besaid from these SEM images that there was not an important damageon the surfaces of the steel foams after soaking to simulated body fluidand artificial saliva environments. In addition, EDS study showed thatthere is no a change in chemical composition of the 17-4 PH stainlesssteel after immersion in artificial saliva.
Biomedical implants require both biomedical safety and biomechan-ical compatibility. In terms of biomechanical compatibility, it is neces-sary that the mechanical properties and corrosion resistance do notdegrade over prolonged use. In particular, high corrosion resistance
Fig. 4. Effect of porosity on the compressive yield strength and Young'smodulus of thepo-rous 17-4 PH stainless steel.
Fig. 5. Quantity ofmetals released from70% porous 17-4 PH stainless steel specimens intovarious solutions after 7 days.
Fig. 7. Effect of immersion timeonquantity ofmetals released from17-4 PH stainless steelspecimens into Hank's solution at pH of 7.4.
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with low metal release is a requirement for metallic biomedical im-plants. Corrosion resistance of stainless steels is due to the formationof a protective passive film. The stronger the passive film, the better isthe corrosion resistance. This passive film acts as a barrier to preventmetal ions from releasing from the bulk metal. The quantity of releasedmetal changes depending on the nature and strength of themetal-oxidebond, structure (vacancies, interstitial elements, degree of ordering),role of alloying elements, chemical composition and thickness of theoxide films.
Stainless steels react with oxygen and form a surface oxide (passivefilm) layer which acts as a barrier against further reaction. This acts as ablock to the spreading of oxygen into bulk alloy. Passive film plays animportant role as an inhibitor of metal release. Metals with strong pas-sive films exhibit lower metal release. The maintenance of passivityconsumes oxidizing species, so a supply of oxidizing agent is required.Weakly oxidizing environments as air and water are sufficient to pas-sivate the stainless steels. Stainless steels may corrode inside the bodyin oxygen depleted regions. In order to obtain a compact and continu-ous passive film, a Cr content of at least 11% is required. The rate ofmetal release decreases with the increase in Cr/(Cr+Fe) ratio in thepassive film. The protective passive film on the 17-4 PH stainless steelmainly consists of Cr2O3. This thin film is invisible and the thickness ofthe oxide film is usually a few nanometers.
Fig. 6. Effect of immersion time onquantity ofmetals released from17-4 PH stainless steelspecimens into Kokubo's simulated body fluid solution at pH of 7.4.
Metal ions from implants are released by various mechanisms, in-cluding corrosion, wear, and electrochemical processes. Two essentialfeatures determine corrosion of metals. The first involves thermody-namic driving forces, which cause corrosion reactions, and the secondinvolves kinetic barriers. The thermodynamic driving forces correspondto the energy required during a reaction. There are two sources of ener-gy in corrosion. The first is a chemical driving force. The second occurswhen positive and negative charges are separated. This separation con-tributes to electrical double layer and creates an electrical potential atinterface. The basic reaction that occurs during corrosion is the increasein the valence state. The second factor that governs the corrosion are ki-netic barriers that prevent corrosion by physical limitation of the rate.Passive films are the best-known forms of kinetic barriers.
The corrosion behavior of materials is also related to surface rough-ness. In addition, roughness influences the wear rate of implants. Aver-age roughness (Ra) of the steel foam was measured as ~7 μm, which issuitable for biomedical applications [29]. Maximum height (Rt) and av-erage maximum height (Rz) values are also measured and found to beas 8 μm and 18 μm respectively. The roughness parameters werefound to be homogeneous at the surface. Meanwhile, surface roughnessparameters could be changed by grinding and polishing. Surface rough-ness showed a negligible effect on metal release at Ra values of 2 and7 μm, according to immersion tests.
Fig. 8. Effect of pHonquantity ofmetals released from17-4 PH stainless steel specimens intoKokubo's simulated body fluid solution for 7 days.
Fig. 9. Effect of pHonquantity ofmetals released from17-4 PH stainless steel specimens intoartificial saliva solution for 7 days.
Fig. 11. Weight loss-immersion time relationship in the 70% porous 17-4 PH stainless steelfoams.
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Energy absorption is an important property of the steel foams. Ener-gy absorption is also important in implants, because orthopedic or hardtissue (bone) implants are exposed to impact forces during day-life.Thus, implants must withstand to a specific level of impact forces.Metal foams have a high-energy absorption capacity with high energyabsorption efficiency because of the extensive plateau region. Effectsof porosity and pore morphology on energy absorption capacity of the17-4 PH stainless steel foams were illustrated in Fig. 14. It can be saidfrom Fig. 14 that increasing porosity decreased the energy absorption.In addition, foams with spherical pores show slightly higher energy ab-sorption than foams with irregular morphology. Meanwhile, effect ofpore morphology on energy absorption capacity was not at excessivelevels.
According to XTT in vitro cytotoxicity assay, it is confirmed that 17–4PH stainless steel foams do not have a cytotoxic potential. Viabilityvalue of the foam (~81%) was close to the viability of the negative con-trol (~91%), which means the 17-4 PH stainless steel has no cytotoxicpotential. Meanwhile, viability of the positive control specimen was~4%. Consequently, the results indicated potential applications of the17–4 PH stainless steel foam as implant.
Fig. 10. Effect of immersion time on quantity of metals released from 17-4 PH stainless steelspecimens into artificial saliva solution.
4. Conclusions
In the present study, characterization of highly porous 17-4 PH stain-less steel foam for biomedical applications was investigated in simulatedbody fluid and artificial saliva environments. Highly porous 17-4 PHstainless steel foams with tailored pore content and morphology wereproduced by space holder-water leaching route. Pore size, total porosityand mechanical properties of the highly porous 17-4 PH stainless steelfoams were found to be similar to human cancellous bone. In static im-mersion test, weight loss of the 17–4 PH steel foams is low. While theFe, Cr, Ni, Cu and Mo elements would be released from the stainlesssteel foams, therewas not a highermetal ion release than reference levelsof these metal ions in body fluids. The quantity of metal ions releasedfrom the 17-4 PH stainless steel foam was slightly increased with de-creasing pH of solutions. In contrast, metal releasewas increasedwith in-creasing immersion time. In vitro cytotoxicity assay showed that the17–4 PH stainless steel foamdoes not have a cytotoxic potential. Viabilityvalue of the foam (~81%) was close to viability of the negative control(~91%), which means the 17-4 PH stainless steel has no cytotoxic poten-tial. Preliminarily, the 17–4 PH stainless steel foam, with its lowmetal re-lease and weight loss in simulated body fluid and artificial salivaenvironments, showed advantage for long-term biomedical implant
Fig. 12. Effects of porosity and pore size on weight loss in the 17-4 PH stainless steel foams.
Fig. 13. (A) SEM image from surfaces of the 17-4 PH stainless steel foam, (a) before immer-sion, (B) after immersion.
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applications.Meanwhile, evaluation of amaterial for implant applicationsshould also include electrochemical corrosion tests. Corrosion parametersof 17–4 PH stainless steel foam will be investigated by electrochemical
Fig. 14. Effect of porosity and poremorphology on energy absorption capacity of the steelfoams.
impedance spectroscopy, open circuit potential and potentiodynamic po-larization methods. In addition, in order to improve integrity of implantto bone, a bioactive ceramic will be coated and examined.
Acknowledgments
This work was supported partially by Scientific Research ProjectsCoordination Unit of Istanbul University, Project number 1430. The au-thors are grateful to Professor Suat Yılmaz for pH measurements.
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