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Review Article

Review Article Dental implants from functionally graded materials Mehdi Mehrali, 1 Farid Seyed Shirazi, 1 Mohammad

Dental implants from functionally graded materials

Mehdi Mehrali, 1 Farid Seyed Shirazi, 1 Mohammad Mehrali, 2 Hendrik Simon Cornelis Metselaar, 2 Nahrizul Adib Bin Kadri, 1 Noor Azuan Abu Osman 1

1 Department of Biomedical Engineering, Faculty of Engineering, University of Malaya, Kuala Lumpur 50603, Malaysia 2 Department of Mechanical Engineering and Center of advanced Material, University of Malaya, Kuala Lumpur 50603, Malaysia

Received 29 August 2012; accepted 4 January 2013 Published online 11 June 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/jbm.a.34588

Abstract: Functionally graded material (FGM) is a heteroge- neous composite material including a number of constitu- ents that exhibit a compositional gradient from one surface of the material to the other subsequently, resulting in a ma- terial with continuously varying properties in the thickness direction. FGMs are gaining attention for biomedical applica- tions, especially for implants, owing to their reported supe- rior composition. Dental implants can be functionally graded to create an optimized mechanical behavior and achieve the intended biocompatibility and osseointegration improve- ment. This review presents a comprehensive summary of biomaterials and manufacturing techniques researchers

employ throughout the world. Generally, FGM and FGM po- rous biomaterials are more difficult to fabricate than uni- form or homogenous biomaterials. Therefore, our discussion is intended to give the readers about successful and obstacles fabrication of FGM and porous FGM in dental implants that will bring state-of-the-art technology to the

bedside and develop quality of life and present standards of

care. V C

2013 Wiley Periodicals, Inc. J Biomed Mater Res Part A:

101A: 3046–3057, 2013.

Key Words: functionally graded material (FGM), biomaterials, dental implants, mechanical properties

How to cite this article: Mehrali M, Shirazi FS, Mehrali M, Metselaar HSC, Kadri NAB, Osman NAA. 2013. Dental implants from functionally graded materials. J Biomed Mater Res Part A 2013:101A:3046–3057.

INTRODUCTION

The aim of modern dentistry is to restore the patient to normal function, health, speech, and aesthetics. The dental implants could be an only restoration option for people in good general oral health who have lost a tooth owing to periodontal disease, an injury, or some other reasons. The most common cause for failure in dental implant is inad- equate bone formation around the biomaterial immediately after implantation. 1 Therefore, the development of new bio- materials for dental implants is one of the challenging tasks for materials science today. A single composition with a uni- form structure cannot satisfy the requirements for some biomedical applications as dental biomaterials must meet several important criteria and have properties such as bio- compatibility with a known degradation rate, osteoconduc- tivity, strength, corrosion resistance, elastic modulus, fatigue durability, and close chemical similarity to biological apatite present in human hard tissues. 25 Hence, in the field of bio- medical implants, we often observe a number of designs

produced both from conventional engineering and tissue en- gineering. Nowadays, bone implant research is mainly focused on four areas: (1) composites, (2) polymeric coat- ings on metallic implants, (3) tissue engineering, and recently (4), functionally graded material (FGM). 6 FGMs, first proposed in 1986 in Japan, represent a novel idea for the realization of innovative properties and/or func- tions that conventional homogeneous materials cannot ac- complish. 7,8 One extraordinary feature of biomaterials is the formation of gradable structures. Therefore, FGMs are useful as the composition of tissue shows a continuous change from one composition to another. 9 For example, the suitable design of porous bone with a porosity gradient from a dense, stiff external structure (the cortical bone) to a porous internal one (the cancellous bone), and with an adequate degree of interconnectivity exhibits that functional gradation is applied by biological adaptation. 1012 In the case of dental implants, the components are usu- ally much smaller and used to reconstruct the masticatory

Correspondence to: F. S. Shirazi; e-mail: f.shirazi@siswa.um.edu.my Contract grant sponsor: Ministry of Higher Education (MOHE) of Malaysia; contract grant number: UM.C/HIR/MOHE/ENG/10 D000010-16001 Contract grant sponsor: Institute of Research Management and Consultancy (IPPP), University of Malaya; contract grant number: PV008/2012A

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V C 2013 WILEY PERIODICALS, INC.

REVIEW ARTICLE

REVIEW ARTICLE FIGURE 1. View of an FGM dental implant with graded material composition in the

FIGURE 1. View of an FGM dental implant with graded material composition in the maxilla. 13 [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

function when a tooth root is wholly extracted or lost. The implant is located in the jaw bone in a manner to penetrate from the inside to the outside of the bone. The required function of a dental implant varies at the outside of the jaw- bone, inside it, and at jawbone boundary. 13 On the outside of the bone, the implant material needs to have sufficient mechanical strength to bear the occlusal force, whereas the part inside the jawbone must have stress relaxation, osteo- conductivity, and adequate bone-implant contact so that the new bone is created speedily and attaches directly to it. Nowadays, dental implants use single materials sometimes with a bioactive coating layer. The problems associated with the current, coated metallic implants consist of stress shielding of the surrounding bone and poor survival of coat- ings over time, resulting in severe biocompatibility issues. 6,14 The theory of stress shielding hypothesizes that bone loss around orthopedic and dental implants is owing to the removal of normal stress from the bone by an implant. 15 To improve the dental implant’s acceptance inside the living bone, the concept of FGM should be a favorable approach. 16,17 The primary advantages of using FGM dental implants include: (1) improvement of biocom- patibility, 18 (2) diminution of the stress shielding effect on the surrounding bones that regularly occurs in the presence of fully metallic implants, 1921 ; (3) precluding the thermal mechanical failure at the interface of hydroxyapatite (HA)- coated metallic implants, 22 and (4) improving the biome- chanical requirement and controllability for graded bioreac- tion at each region of the bone. 23 All these aspects of using FGM implants are discussed in this review. So far, function- ally graded dental implants use a variety of materials such as titanium (Ti), HA, titanium nitride (TiN), polymer, zirco- nia (zirconium dioxide, ZrO 2 ), and so on. In this review arti- cle, we consider materials and fabrication techniques used in this application field in recent years. Furthermore, the

design of functionally graded dental implants and optimiza- tion is also a subject of this review.

THE STRUCTURE OF FUNCTIONALLY GRADED DENTAL IMPLANTS

Many natural tissues and organs are not homogeneous materials, and observations show their structures to be functional gradients, for example mollusk shells, bamboo, bone, and skin. 2426 Tissues or organs are described as functionally graded if each layer of the tissue or organ has one or more particular functions to achieve the local func- tional requirements. Therefore, to regenerate the natural functionality, a successful conception of dental implant should also include FGM. 5,17,2730 Figure 1 shows a sche- matic view of an FGM dental implant with graded material composition used in dentistry. For FGM dental implant purposes, a cylindrical shape was designed with composition varying in the axial direc- tion. The upper part has more strength and mechanical properties necessary as the occlusal force is applied directly on the top and then transmitted down to lower parts implanted inside the trabecular bone where more biocom- patible materials are desirable. 6,31,32 Mostly, implant failure is owing to the lack of biomechanical bonding between the implant and the surrounding jawbone; therefore, the lower parts should have a high osteoconductivity and have a good bone-to-implant contact for regenerating bone and rapid osseointegration. 20,3335 Also, the implants might fail owing to insufficient strength and mechanical properties or over- load. Consequently, a possible solution is to design adequate mechanical properties in the upper parts of FGM dental implants. 3437 As discussed in detail above, when consider- ing an implant design, the use of FGM is expected to improve both the mechanical and the biological perform- ance of dental implants.

TABLE I. Materials and Bone Properties

Young’s

Poisson’s

Density (kg/m 3 )

Materials

Modulus (GPa)

Ratio

Reference

Cortical bone

14

0.3

1700

Rho et al. 44 Rho et al. 44 Dowker et al. 45 and Kitagawa et al. 46 Kitagawa et al. 47 and Angker et al. 48 Benzing et al. 49 and Lin et al. 50 Hedia and Mahmoud 19 Stone et al. 51 , Sherif El-Eskandarany et al. 52 , and Namazu et al. 53 Marti 54 Gahlert et al. 55 and Andreiotelli and Kohal 56 Zhou et al. 57

Cancellous bone

3

0.3

270

Enamel

10.5

0.33

2906

Dentin

19.7

0.33

1800

Ti

110

0.35

4500

HA

40

0.27

3219

TiN

251

0.29

5300

Co

210

0.31

8900

ZrO

2

200

0.31

6000

SiO

2

75

0.17

2200

CHALLENGES FOR MATERIALS

In the last few years, a variety of biomaterials and biocer- amics were investigated for FGM dental implants such as Ti/HA, 16,17,38 titanium/cobalt (Ti/Co), 39 Ti/ZrO 2 , 40 tita- nium/silica (Ti/SiO 2 ), 41 and TiN/HA. 42,43 Table I summa- rizes the Young’s modulus, Poisson’s ratio, mass density of bone, and material densities for reference. 19,31,4453 Studies have shown that Ti and its alloys are among the most suc- cessful metallic biomaterials for dental and orthopedic applications because of their good mechanical properties (elastic modulus, toughness and fatigue, strength), excellent corrosion resistance, and good biocompatibility. 5860 How- ever, Ti and Ti alloys are bioinert and cannot promote tissue bonding to the implants. Generally, a dental implant should have sufficient mechanical strength to maintain integrity; for this reason, Ti and Ti alloys were used along the longitu- dinal direction from Ti, which is rich in the upper parts where occlusal force is directly applied to ceramics or met- als rich in the other material that is implanted inside the jawbone. Watari et al. 39 investigated Ti/Co FGMs. They evaluated the mechanical properties and biocompatibility for implants. They reported that in the implantation analysis of Ti/Co into the soft tissue, a thin fibrous connective tissue was formed in the pure Ti region while the thickness of the fi- brous tissue layer increased with the Co concentration, lead- ing to inflammation problems at the Co-rich part. Therefore, the CO’s change of concentration seemed to affect the bio- compatibility of implant material. Other clinical studies also indicated that epithelial cells as well as fibroblasts have a stronger negative response to a Co-chrome alloy than to Ti. 61 In this context, Co exhibited several advantages in me- chanical properties, wear resistance, and good corrosion resistance. Takahashi 40 studied the use of Ti/ZrO 2 FGM for dental implants. Zirconia appears to be an appropriate dental implant material because of its tooth-like color, biocompati- bility, and good mechanical properties in strength and frac- ture toughness. 62 The inflammatory reaction and bone resorption provoked by zirconia particles are less than those influenced by Ti particles; therefore, ZrO 2 is suitable

3048 MEHRALI ET AL.

for long-term use in vivo. 6365 Recently, Fujii et al. 66,67 described the successful preparation of partially stabilized zirconia (PSZ) and pure Ti FGM by the hot pressing of pow- der. Fujii et al. evaluated the mechanical properties such as bending strength, Young’s modulus, and Vickers hardness. One of the results was that the bending strength and Vick- ers hardness decreased with increasing Ti content in the PSZ–Ti because the strength and hardness of 100% PSZ are much higher than those of pure Ti. The Young’s modulus increases from pure PSZ to 20% Ti content and then declined with increasing Ti. Also, they found that brittle fracture occurred after elastic deformation except for pure Ti. 66 Figure 2 shows the fracture surfaces in SEM micro- graphs. They reveal that transgranular fractures occurred in the PSZ and Ti phases. It is worth noting the brittle fracture surface is detected even in the Ti-rich region. Takahashi et al. 41 carried out the synthesis of Ti/SiO 2 FGM for dental work in 1992. Some studies reported that silica is believed to play a critical role in bioactivity of bio- active materials for the bonding of bone and muscle and as a crosslinking agent in connective tissue. 6870 There are three functions of silica. (1) Silica performs a specific meta- bolic function that is thought to partake in cellular develop- ment and gene expression. 7173 (2) There is a chemical function in which the bonding to bone is established by the precipitation of apatite surface layer that must be formed on the bioactive silica-based glasses surface when in contact with in vivo applications or simulated body fluid. 71,74,75 The in vitro studies observed that composites containing bioac- tive glass–ceramic (BGC) nanoparticles with lower phospho- rous and higher silica content have better bioactivity than that of the BGC with higher phosphorous and lower silica content. 76,77 (3) There is a mechanical function as silica par- ticles showed to improve the strength of a HA coating by particle-mediated reinforcement, leading to crack deflection or crack arrest. Amorphous SiO 2 is a good candidate to enhance the mechanical properties of HA coatings. 68 HA is one of the best among the bioactive materials as it can bond to human bone because osteoblast cells penetrate into HA. Therefore, HA is clinically applied to the teeth. 7880 However, the mechanical strength of HA is remarkably low

DENTAL IMPLANTS FROM FGM

REVIEW ARTICLE

REVIEW ARTICLE FIGURE 2. SEM micrographs of fracture surface of PSZ-Ti. 6 6 and the application

FIGURE 2. SEM micrographs of fracture surface of PSZ-Ti. 66

and the application of HA to teeth was limited. 8183 Another study by Watari et al. 16,17 used HA and Ti to prepare FGM dental implants. This team reported that a good combina- tion of HA and the mechanical properties of Ti is considered as a promising approach to fabricate suitable FGM dental implants. During sintering of Ti/HA FGM, the HA is not decomposed at 850 C. 42 On the other hand, this tempera- ture is too low for sintering HA and mechanical properties did not develop. Kondo et al. 42 used TiN to improve the sin- tering of HA at higher temperature. They reported that by using TiN instead of Ti, the decomposition of HA can be suppressed. However, the sintering of the TiN-rich region was still inadequate for the temperature up to 1200 C. To avoid these problems, researchers have used different fabrication techniques. In the following sections, there is a review of the processing methods to fabricate FGM dental implants. As mentioned earlier, PSZ has good biological compatibility and a high mechanical strength; however, it is not expected that PSZ embedded as an artificial bone com- bines with a bone because it has no osteoconductivity. When a material devoid of osteoconductivity is applied for bone implantation, there is a gap between the material and the bone that grows with the passing of time and causes both pain and abrasion of the material. Many have carried out several investigations to solve this problem by producing a composite of HA and PSZ. 8486 Matsuno et al. 87 reported that a laminated HA/PSZ-sintered composite with a gradient composition can be produced from HA and PSZ. This study said to expect wide reception of HA/PSZ gradient composition as a biomaterial for hard tissue because it has osteoconductivity and high mechanical strength. Guo et al. 88 have used yttria-stabilized tetragonal zirconia (Y-TZP) to develop functionally graded HA/ZrO 2 composites. The authors reported that HA/Y-TZP function- ally graded composites showed considerable improvement in mechanical properties, whereas the HA phase in the com- posite layers was stable up to 1200 C and the Y-TZP second phase remained the tetragonal zirconia (t-ZrO 2 ) phase after processing at the highest temperature of 1250 C. Figure 3 is a back-scattering electron (BSE) micrograph of a cross-sec- tion of the HA/Y-TZP FGM. The microhardness and the Young’s modulus increased stepwise from the pure HA layer

to the HA þ 40 wt % Y-TZP layer across the HA/Y-TZP func- tionally graded composites as shown in Figure 4(a,b). Besides the FGM dental implants discussed above, po- rous functionally graded biomaterial such as Ti and its alloys also work. Nowadays, most oral implants are fabri- cated from Ti-6Al-4V (90% Ti, 6% aluminum, and 4% vana- dium) and pure Ti. Although Ti and its alloys have good physical, mechanical properties, corrosion resistance, and biocompatibility, 89,90 the stiffness of metallic dental implants is not well-adapted to bone. This situation leads to stress shielding from the residual bone, which may result in detri- mental resorptive bone remodeling. 91 The stiffness of a metal is determined by the Young’s modulus of the material used as well as its area of moment inertia. In the case of Ti dental implants, the Young’s modulus is far higher than that of cortical bone as summarized in Table I. 44 Therefore, it is proposed that the level of porosity is gradable, from a more porous surface layer to a denser core, giving the potential to have the same stiffness of the bone tissue at the implant–bone interface. 92,93 Hirschhorn 94 in the 1970s used the concept of function- ally graded porous biomaterials to fabricate femoral stems. However, the study appeared abandoned owing to the

stems. However, the study appeared abandoned owing to the FIGURE 3. BSE composite. 8 8 image

FIGURE 3. BSE composite. 88

image

of the HA/Y-TZP functionally

graded

FIGURE 4. (a) Microhardness and (b) Young’s modulus as a function of Y-TZP content for

FIGURE 4. (a) Microhardness and (b) Young’s modulus as a function of Y-TZP content for the HA/Y-TZP functionally graded composites by SPS. 88

concerns over poor fatigue performance until a resurgence of interest in 1995 by Becker et al. 95 Becker investigated the mechanical properties of different biomedically approved alloys such as 316L stainless-steel, Co-29Cr-6Mo alloy, and Ti-6Al-4V alloy. 95 Becker and Bolton’s study 92 showed that it is possible to use porous FGM Ti alloys for orthodontic or maxillofacial implants. It is possible to alter and optimize mechanical properties of porous materials in dental implants by controlling poros- ity, pore size, and pore distribution. Oh et al. 96 investigated the effects of different pore sizes in vitro and in vivo and found a suitable size range of 5–15 l m for fibroblast ingrowth, 70–120 l m for chondrocyte ingrowth, and 100– 400 l m for bone regeneration, depending on the porosity as well as scaffold materials. Meanwhile, the surface microstruc- ture of dental implants is another crucial design feature. Some have reported that rough surfaces can promote better and faster bone apposition as they are more osteoconductive than smooth surfaces. 97 Wong et al. 98 and Carlsson et al. 99 reported that a surface with R a between 1 and 10 lm was optimal for promoting bone apposition and stimulating mes- enchymal cell differentiation into functional osteoblasts.

TABLE II. Materials and Fabrication Techniques

The following section outlines the various fabrication methods of porous FGM for dental implants and provides an indication as to how far they can provide control over these parameters. Different synthesis methods for FGM den- tal implants are focused in the next section.

FABRICATION TECHNIQUES AND MECHANICAL BEHAVIOR FOR FUNCTIONALLY GRADED DENTAL IMPLANTS

In this section, we discuss the processing methods to fabri- cate FGM dental implants and their mechanical behavior. There are several methods for the fabrication of FGM and porous FGM dental implants as summarized in Table II.

Functionally graded dental implants containing Ti and TiN Ti/HA FGM can make a promising material for tissue im- plantation, orthopedic, and dental applications because of its outstanding biocompatibility and bioactivity. As men- tioned above, different fabrication methods are used such as cold isostatic pressing (CIP), spark plasma sintering (SPS), hot pressing, and powder metallurgy (PM). Watari et al. 17 in 1997 showed the synthesis of HA/Ti as an FGM dental

Functionally Graded

 

Dental Implants

Fabrication Methods

References

Ti/HA

CIPþ EF, CIPþ HF, SPS, PM, hot pressing SPS PM

 

TiN/HA

Ti/Co

Ti/SiO

2

CIPþ

HF

Ti/ZrO

2

HA/ZrO 2

Porous FGM

CIPþ HF, hot pressing SPS, hot pressing PM, one-step microwave, PECS, LENS TM , and DLMS

Watari et al. 16 , Fujii et al. 66 , Watari et al. 100 , Chu et al. 101 , and Chenglin et al. 102 Kondo et al. 42 Watari et al. 39 Watari et al. 16 and Takahashi et al. 41 Takahashi 40 and Fujii et al. 66 Guo et al. 88 Matsuno et al. 87 , Traini et al. 93 , Kutty and Bhaduri 103 , Suk et al. 104 , and Krishna et al. 105

FIGURE 5. Change of Brinell hardness with HA content in Ti/HA FGM sintered by EF

FIGURE 5. Change of Brinell hardness with HA content in Ti/HA FGM sintered by EF at 1300 C and SPS at 850 C. 16

implant using CIP and sintered by high-frequency induction heating to satisfy both mechanical and biocompatible prop- erties. Watari et al. 16,38,100 tried CIP, sintered electric fur- nace (EF) heating and SPS methods for sintering. In the EF sintering, powders were packed into the thermo-contractive tube after heat treatment of a tube at 60 C, which was then compressed by CIP at 800–1000 MPa, and the implants of the miniature cylindrical shape were densified by sintering in a vacuum at 1300 C. In the high-frequency induction heating, they packed powders into the thermo-contractive tube or silicone rubber impression mold with the shape of a dental implant. After CIP, the packing was sintered at above 1300 C in Ar gas atmosphere. For SPS process, the mixed powders of Ti hydrate and HA were put into a graphite mold with the gradient composition ranging from 100% Ti to pure HA in the height direction and sintered at 850 C at a pressure of 40 or 80 MPa. Watari et al. reported that Ti/ 100HA FGM decomposition in the sintering process is sig- nificant. Internal stress also arises from the difference of thermal expansion coefficient and shrinkage at the interface from one region to other. Moreover, they lowered the sinter- ing temperature by using SPS to avoid autodestruction. There was much improvement in sintering by SPS compared with the conventional CIP and furnace sintering methods. Fracture of the FGM occurs near the weakest region or its neighbor. In the three-point flexural test of Ti/HA FGM prepared with SPS at a pressure of 40 MPa, fracture occurred deviated from the center in the HA-rich side, which is weaker. In the FGM prepared with 80 MPa, fracture occurred inside the single layer in the center. The flexural strength was increased to 36 MPa and the compressive strength 88 MPa, respectively. The Brinell hardness test observed for FGM sintered by SPS and EF in Figure 5 shows

REVIEW ARTICLE

the decreasing tendency of the hardness in the direction of the tooth root region in SPS contributes to the stress relaxa- tion, which relieves the jawbone from damage by imposition of high spike of impact stress near the implant. It is important to control the temperature distribution in a work piece during and after sintering in SPS and the re- sidual stress distribution at the interface of each layer after sintering to obtain the desired mechanical properties. Sasaki and Asaoka 106 investigated and analyzed the effects of tem- perature distribution and residual stress at the interface of each layer in SPS sintering by finite element method (FEM) to develop an optimization approach for conducting opti- mum production conditions. FEM analysis can be used with SPS method to simulate the whole heating process in a manner comparable to the actual experimental experience, where a controllable heating rate, variable die size, and pressure are implemented. 107,108 They reported that the measured residual stress was higher than that predicted from FEM. This group also observed that hardness increased, whereas fracture toughness and bending strength decreased with rising HA content. Chu et al. 109 investigated HA/Ti biomaterial FGM by employing a hot-pressing method without bending deforma- tion and microcracks parallel to the graded direction of the FGM on the surfaces. Chu et al. 101 developed HA/Ti FGM by optimizing the best combination of their biocompatibility and mechanical properties. In their method, they first exam- ined the thermoelastic properties of uniform HA/Ti related to each graded layer of the FGM. In their results, the ther- mal expansion coefficients of the HA/Ti increased with the rise in temperature or content of HA, and the residual ther- mal stress was confirmed by an X-ray and theoretical method. They have also used powder metallurgy to produce HA/Ti FGM sintered at 1100 C. 102 In this method, hardness grew with increasing volume fraction of HA as opposed to SPS sintering in which the hardness decreased. It is impor- tant to note that the Young’s modulus is higher than natural bones in all regions of Ti/HA FGM that can cause severe stress concentration, namely load shielding from a natural bone, which may weaken the bone and deteriorate the implant/bone interface. Chu et al. reported that the exis- tence of Ti can promote decomposition of HA at the sinter- ing temperature (1100 C). The decomposed phases are a- Ca 3 (PO 4 ) 2 and Ca 4 P 2 O 9 . However, no new compounds form between HA and Ti. 102 Kondo et al. 42 studied TiN/HA functionally graded implants by SPS method. They reported that by using TiN instead of Ti and sintering at 1100 and 1200 C, the decom- position of HA is suppressed. It was found that the mechani- cal properties TiN/HA are comparable to Ti/HA obtained by SPS and are sufficient for practical use. The Brinell hardness was around 60, whereas the hardness in the HA region did not decrease. The flexural strength of TiN/HA sintered at 1100 and 1200 C was 65.4 and 71.3 MPa, respectively, and the compressive strength of TiN/HA FGM was more than 100 MPa. However, the sintering of the TiN-rich region was still insufficient even at 1200 C. They observed little inflam- matory reaction at the TiN part in animal experiments.

Watari et al. 39 produced Ti/Co FGM by powder metal- lurgy using both a wet technique to produce a gradient by differentiated sedimentation in a solvent liquid and a dry method to pack mixed powders gradiently into a mold, fol- lowed by CIP, and sintering at 1300 C. The Ti/Co FGM specimens were implanted in the subcutaneous tissue of dorsal part of rat and after implantation were evaluated from histological observation by optical microscopy. One of the evidences of infection is pus formation that is a result of macrophages and neutrophils, which die after killing the foreign parasites. To avoid the spread of infection, fibrous tissues usually form around the pus. 110 The thickness and texture of fibrous tissues created around the implant can depend on the type of implant material, shape and size of the implant, site of surgery in terms of functionality, and type of tissue that needs to be healed. 111 Watari et al. 39 have found that the thickness of the fibrous connective layer is small in the pure Ti region. However, the thickness of the fibrous connective layer increased with Co concentration along the longitudinal direction of the FGM. It was also observed that more inflammatory tissue and necrosis occurred near some Co-rich parts. Takahashi et al. 41 manufactured Ti/SiO 2 FGM dental implants by CIP method and then sintered in argon gas by high-frequency induction heating at a temperature of 1300 C. This group reported that the fracture stress changed from 2000 MPa in pure Ti to 100 MPa at the ce- ramic content. In their research, they also used Ti/ZrO 2 FGM for dental implants 40 by following the same method as mentioned above for Ti/SiO 2 . It was found that at the same volumetric content, the Ti–zirconia composite showed the same flexural strength as the Ti–apatite composite and higher values of elastic modulus and strain. It was shown that the sintering at higher ceramic contents could improve by adding 5% of Pd to the Ti. Recently, Fujii et al. 66 developed Ti and PSZ FGM using hot pressing. The Young’s modulus and Vickers hardness were higher in the full range of Ti than predicted from the rule of mixture, and the bending strength decreased with increasing Ti content as the strength of pure PSZ is much higher than that of pure Ti. According to the X-ray diffrac- tion (XRD) analysis, the sintering process created reaction products such as Ti oxide, and these reactions influenced the mechanical properties. 66 It is often stated that there are different stoichiometrics in Ti oxide which are TiO 2 , TiO, Ti 2 O 3 , Ti 3 O 2 , Ti 3 O 5 , TiO 0.325 , and TiO 0.5 , and it seems that the Young’s modulus depends on the stoichiometrics. 112 Hence, various Young’s modulus of Ti oxide have been reported. 67,113 Hence, the mechanical properties of the Ti/ PSZ FGM could not be explained by the rule of mixture. Teng et al. 114 reported that there was no reaction product in the Ti/ZrO 2 interfaces fabricated by hot pressing, whereas according to the thermodynamic analysis, it is pre- dictable that Ti can react with ZrO 2 in the synthesis proc- esses of Ti/ZrO 2 FGM, and the bonding state between Ti and ZrO 2 is physical in the composite. The XRD results were demonstrated that the volume fraction of Ti in the compo- sites has remarkable effect on the phase transformation

3052 MEHRALI ET AL.

effect on the phase transformation 3052 MEHRALI ET AL. FIGURE 6. Schematic diagram showing a cross-section

FIGURE 6. Schematic diagram showing a cross-section of a disk specimen of the HA/Y-TZP functionally graded composite, consisting of symmetric layers with graded compositions. 88

from t-ZrO 2 to monoclinic zirconia (m-ZrO 2 ). Under the same sintering conditions, the volume fraction of m-ZrO 2 increases with the increase of Ti content. 114 In high-temper- ature sintering at 1500 C, studies with 90 mol % Ti showed that ZrO 2 particles were almost completely dissolved in Ti, being accompanied by simultaneous precipitation of Y 2 Ti 2 O 7 . 115

Functionally graded ceramic–ceramic materials Guo et al. 88 described the successful preparation of HA/ ZrO 2 FGM which is useful for dental implants at 1200 C within 5 min by the SPS method and found that equiaxial Y- TZP grains uniformly dispersed in the HA matrix. They showed 88 that there was no phase change of HA in the com- posites sintered at 1100 C, but HA started to decompose into a -TCP at 1200 C. On the other hand, the Y-TZP remained the t-ZrO 2 phase even after the maximum temper- ature of 1250 C. A thin layer of CaZrO 2 phase was found on the interfaces among HA grains and zirconia grains. The Young’s modulus of these FGM grew with increasing zirco- nia content and sintering temperature up to 140 GPa sin- tered at 1100 C and 160 GPa at 1200 C, which is high com- pared to Ti/HA. Guo et al. 88 reported that the bending strength of the composites SPS at 1200 C reached 200 MPa, which is double the strength of pure HA ceramics. It has enough durable strength in the clinical practice. Matsuno et al. 87 have also investigated HA/ZrO 2 FGM by hot pressing, but the significant difference between the Guo study and the Matsuno’s study was the design and arrangement of the individual layers. Guo et al. 88 designed the pure HA layer as the middle layer and the HA þ 40% Y-TZP layers on both ends of a prepared disk as shown in Figure 6. This design’s use introduces compressive stresses that can be developed on both ends of the disks, and there were no long micro- cracks observed in their spark plasma-sintered samples. The microcracks are the direct evidence of thermal stresses owing to a cooling process from a high temperature to room temperature and are generally present in both compo- sites and coatings. Guo et al. 88 reported that the tensile stress developed in the HA layer because of its higher

DENTAL IMPLANTS FROM FGM

thermal expansion coefficient than that of the ZrO 2 layer, and therefore causing the microcracking in the HA layer.

Porous FGM dental implants The simplest fabrication technique for manufacturing po- rous FGM dental implants is based on the partial densifica- tion during sintering of metal powders. This method is known as powder metallurgy. Thieme et al. 116 produced po- rous Ti FGM destined for orthopedic implants with a poros- ity gradient perpendicular to the surface by a powder met- allurgy technique. The porous FGM demonstrated adequate Young’s modulus in the range of 5–80 GPa so that it is adapted to the elastic properties of bone with the purpose of avoiding stress shielding effects and to present better long-term performance of the implant-bone system. The results indicated that the modulus is inversely connected with the porosity gradient. 116 Kutty and Bhaduri 103 developed a graded porosity on the surface while maintaining a dense core in a Ti sam- ple. 116 In their research, the synthesis was carried out in a semi-industrial grade microwave cavity using a -SiC suscep- tor. The Ti samples were sintered at 1, 1.25, and 1.5 kW for 30 min. The result was that a pore size in the range of 30– 100 lm is ideal for fibroblast ingrowth. 12 A mechanical study showed the highest strength of about 400 MPa when the samples were sintered at 1.25 kW for 20 min and this value is close to bulk CP Ti (345–550 MPa). In addition, FGM porosity and the graded nature of change from dense core to porous surface should result in a better stress trans- fer than a coated surface. Therefore, a one-step processing technique works for fabricating various implants and dental implants. A pulsed electric current sintering (PECS) process exists for the production of porous structure with a porosity gradient in the micrometer size. 106 PECS permits more rapid sintering at lower temperature than conventional sin- tering, primarily by means of a spark pulse current that forms between the powder particles. 117 Suk et al. 104 used a pressureless PECS method for manu- facturing porous FGM, and the obtained specimen has a gradual change in pore distribution. This experiment was carried out without rapid and strong neck formation and with no volume shrinkage. The major interest in this pro- cess is where to obtain good pore interconnectivity, easy po- rosity control, and short processing time, but low porosity and expansiveness. 12,104 Figure 7 shows the graphite mold used in the PECS technique for the preparation of the po- rous material with a porosity gradient. Three K-type ther- mocouples at various positions, as shown in Figure 7 (posi- tions 1–3), checked the temperature difference along the longitudinal direction within the graphite mold. This process confirmed that a suitable temperature gradient was estab- lished for preparing the porous structure with a porosity gradient of reasonable degree. Sintering was generally per- formed with a thermocouple inserted completely into the hole at position 2, the temperature of which was taken as the significant sintering temperature. Laser-Engineered Net Shaping (LENS TM ) is a technique able to obtain gradient structures and can also produce net-

REVIEW ARTICLE

gradient structures and can also produce net- REVIEW ARTICLE FIGURE 7. Schematic illustration showing the graphite

FIGURE 7. Schematic illustration showing the graphite mold used in the PECS process: (1) specimen (powder), (2) die, and (3) punch. Holes for inserting thermocouples are located at positions 1–3. 104

shaped implants with designed porosities and can extend to other metallic biomaterials as well. 118,119 Krishna et al. 105 used LENS to produce porous Ti implants with mechanical properties matching those of natural bone. They reported the bulk density and porosity of these samples varied, depending on the LENS-processing parameters. 105 Young’s modulus increased linearly with increasing density of the samples. The experimental data indicate that the modulus and strength of laser-processed Ti specimens can be tai- lored in the range of 2–45 GPa and 21–461 MPa, respec- tively, whereas the porosity was in the range of 35–42 vol %, close to those of human cortical bone. They also observed that it is possible to fabricate porous Ti samples with a porosity higher than 40 vol % that have appreciable mechanical properties, whereas in other literatures, it was reported that the strength of compacts with a porosity higher than 40 vol % is diminished to approximately 0 MPa. 120,121 Generally, the important points in this process are good pore interconnectivity, control over porosity, and ability to realize complex shapes. However, this technique is limited to small pore sizes. More recently, the development of direct laser metal sin- tering (DLMS) processes has considerably increased the field of application of Ti alloys and allowed implants to be fabricated more economically in comparison with traditional techniques. Among the several direct metal-forming techni- ques, selective laser sintering promises great potential bene- fits in the field of the biomaterials, especially in implant dentistry, owing to its capability to directly build three- dimensional (3D) metallic components from metal powder with minimal or no postprocessing required. 122,123 Traini et al. 93 used DLMS and subsequently modified it with acid- etching methods to improve the surface microstructure for the production of isoelastic FGM for porous Ti dental implants. In their research, the original surface consisted of spherical particles in the range of 5–50 l m. In the next steps, they used different etching techniques using inorganic and organic acids. It was observed that after exposure to hydrofluoric acid, some of the spherical particles were removed and the microsphere diameter was in the range of 5.1–26.8 l m. After an organic acid treatment, grooves from 14.6 to 152.5 l m in width and 21.4–102.4 lm depth

FIGURE 8. SEM images at 500 magnification of surface’s fabricated disks after different treatments. (a)

FIGURE 8. SEM images at 500 magnification of surface’s fabricated disks after different treatments. (a) Untreated disk; (b) disk treated with hydrofluoric acid; and (c) disk treated with organic acid. 93

replaced particles. The SEM images of the surface’s DLMS- fabricated disks after different treatments are shown in Figure 8. Moreover, they assessed the variation of surface roughness by use of a Chi-square test. It is important to control the surface morphology of the dental implants to obtain the desired surface roughness and the wettability to allow the absorption of plasma proteins on the implant sur- face. 124 Young’s modulus of the exterior porous Ti was 77 6 3.5 GPa, but the mean of porosity was 28.7% of the metal surface, and that of the inner core Ti was 104 6 7.7 GPa. The fracture face indicated a dimpled appearance typical of ductile fracture. However, the method is also limited in the arrangement and the control of pore size that can be fabricated.

FUTURE CONSIDERATIONS

For nearly all dental implants, the main goals are rapid return to function (i.e., mastication), stronger, safer osseoin- tegration, and long-term fixation of implants to bone. To achieve these goals, designers of dental implants must con- front biomechanical and biomaterials subproblems, includ- ing in vitro and in vivo performances on implants, mechani- cal compatibility to smooth transfer the stress between the placed implant root and the receiving hard tissue, and inter- facial tissue response. As a promising candidature, FGM can be applied to improve the success of dental implants while there are no many examples of actual FGM dental implants that have been used in clinical applications. The hurdle may be the producing cost and transferring the techniques to shape of a dental implant, which will prevent the realization of the potential of functionally graded dental implants. In our research to create the ideal implant designed with FGMs approaches, we are required to close key gaps in our basic knowledge and make a series of prototype dental implants with increasing functionality. We must start by dis- tinguishing the specific gaps, in our present knowledge, and then look widely for advances that will facilitate us to link them. We must try to uncover the relationships linking com- position and biomaterials architecture in functionally graded dental implants with mechanical behavior, length scales, and the capability for osteogenesis. Finally, these relationships should be tested and evaluated systematically in vivo and finally in clinical studies.

3054 MEHRALI ET AL.

Although many biomaterials and ceramics can be made into the FGM and gradient porous dental implants, but so far they have received little attention and still need for improvement. For example, recently bioactive glass scaffolds with strengths comparable to those of cortical bone have been produced. Therefore, these bioceramics may have potential for the FGM in dental implants. But, the mechani- cal properties and reliability of BG remain as limiting fac- tors for applications in dental implants; however, still more consideration is needed for development. The study of the literature suggests that many different parameters might be important for the long-term osseointe- gration and better performance in bone, where the goal can be achieved by lowering the FGM material gradient. But, it is well established that this will, at the same time, decrease the stiffness of implantation, as a result locating the bone implant interface at higher risk of damage during the early healing stage. The problem might be minimized by the mul- tiobjective optimization processes that are yet to be used in biomechanical studies up to date, whereas machining, den- tal, and material demands must be considered. There is a need to further analyze and further information on the machining characteristics and machining-induced surface of dental bioceramics and FGM dental implants to improve quality, efficiency, bone–implant contact, and cost production. Depending on the clinical advantage required for, merged with the regulatory landscape, the commercial de- velopmental efforts will finally provide new products with novel and unique properties.

CONCLUSIONS

Close studies of natural tissue and organs illustrate that they are not homogenous and natural functional gradients exist in their formation. Biomaterial and tissue engineering research literature shows that there is a requirement in developing implants with FGM. Therefore, the great poten- tial of FGM lies not only in the field of bone tissue engineer- ing but also in dentistry. To improve the acceptance of den- tal implants inside the living bone, the concept of FGM is a favorable approach. The works reviewed here show that the development of functionally graded dental implants and po- rous functionally graded dental implants is feasible for

DENTAL IMPLANTS FROM FGM

commercial dental implants. Porous functionally graded dental implants were reviewed to improve mechanical prop- erties, especially Young’s modulus as the high stiffness of Ti generally is not well-matched to bone, which can lead to stress shielding of the residual bone, which in turn may result in detrimental resorptive bone remodeling. There are a variety of techniques for producing FGM dental implants and gradients of porosity. However, these structures are largely still in the stage of laboratory research. The obstacle may be the producing cost, which will prevent the realization of the potential of FGM dental implants. Also, more tests and studies are needed with regard to design and production of combinations of bioinert and bioactive materials for FGM for dental implants.

ACKNOWLEDGMENTS

The authors are grateful for the grants.

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