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Biomaterials 49 (2015) 135e144

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Biomaterials

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Biodegradable poly-lactic acid based-composite reinforcedunidirectionally with high-strength magnesium alloy wires

X. Li a, b, C.L. Chu a, b, *, L. Liu a, b, X.K. Liu a, b, J. Bai a, b, *, C. Guo a, b, F. Xue a, b, P.H. Lin a, b,Paul K. Chu c

a School of Materials Science and Engineering, Southeast University, Nanjing 211189, Chinab Key Laboratory for Advanced Metallic Materials, Southeast University, Nanjing 211189, Chinac Department of Physics and Materials Science, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China

a r t i c l e i n f o

Article history:Received 30 October 2014Accepted 20 January 2015Available online

Keywords:Biodegradable PLA-based compositeMagnesium alloy wiresMechanical propertiesStrengthening and tougheningDegradation behaviors

* Corresponding authors. School of Materials SciencUniversity, Nanjing 211189, China. Tel./fax: +86 25 52

E-mail addresses: clchu@seu.edu.cn (C.L. Chu), bai

http://dx.doi.org/10.1016/j.biomaterials.2015.01.0600142-9612/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

Biodegradable poly-lactic acid (PLA) e based composites reinforced unidirectionally with high-strengthmagnesium alloy wires (MAWs) are fabricated by a heat-compressing process and the mechanicalproperties and degradation behavior are studied experimentally and theoretically. The compositespossess improved strengthening and toughening properties. The bending strength and impact strengthof the composites with 40 vol% MAWs are 190 MPa and 150 kJ/m2, respectively, although PLA has a lowviscosity and an average molecular weight of 60,000 g/mol. The mechanical properties of the compositescan be further improved by internal structure modification and interface strengthening and a numericalmodel incorporating the equivalent section method (ESM) is proposed for the bending strength. Microarc oxidization (MAO) of the MAWs is an effective interfacial strengthening method. The compositesexhibit high strength retention during degradation and the PLA in the composite shows a smallerdegradation rate than pure PLA. The novel biodegradable composites have large potential in bonefracture fixation under load-bearing conditions.

© 2015 Elsevier Ltd. All rights reserved.

1. Introduction

Orthopedic implants play important roles in restoring thenormal activity and improving the quality of life of millions ofpeople. Orthopedic implants are commonly categorized as recon-structive or fracturemanagement ones. One desirable characteristicis the ability to degrade spontaneously in the physiological envi-ronment to avoid a second operation for removal and reduce therisk of local inflammation which may appear after long-term im-plantation of non-biodegradable implants [1e3]. Poly-lactic acid(PLA), one of the naturally degradable materials having excellentbiological properties and versatility, is used in commercial appli-cations [4e7]. However, the mechanical properties of pure PLAcannot meet the stringent requirements of weight-bearing bonefracture fixation devices. One reinforcing technique is to orient thechains of PLA [8e10]. For instance, Weiler et al. [8] used a solid-state extrusion technique to prepare PLA rods and the bending

e and Engineering, Southeast090689.jing@seu.edu.cn (J. Bai).

strength and modulus of the rods were 200 MPa and 9 GPa,respectively, compared to 140 MPa and 5 GPa, respectively, for rodsprepared by conventional injection molding. Another effectiveapproach is to incorporate filler materials such as bioactive glass,bioceramics, and fibers into PLA. Shikinami et al. [11] reported aPLA-based composite composed of high molecular weight poly-L-lactic acid (PLLA) as the matrix and 40 wt% hydroxyapatite (HA) asthe reinforcement. This composite prepared by a forging techniquehad an initial bending strength of 270 MPa and it remained over200 MPa for up to 24 weeks after soaking in a phosphate-bufferedsaline (PBS) at 37 �C. Addition of HA fillers can suppress hetero-geneous degradation which has been reported to be related to theacidic degradation products from PLA resulting in a local low pHenvironment and probable bone resorption [12,13]. Besides HA,many other filler materials such as calcium carbonate [14], chitosan[15], titania nanoparticle [16], bioglass [17], and magnesium alloyfibers [18] have been investigated to overcome the low pH problemand among them, magnesium-based fillers which are themselvesbiodegradable have attracted much interest.

Magnesium is an essential element and plays an important rolein human metabolism by participating in protein synthesis and

X. Li et al. / Biomaterials 49 (2015) 135e144136

activating some enzymes [19]. The biocompatibility of magnesiumand its alloys has been investigated and verified [20e23]. In addi-tion, the fracture toughness of magnesium is greater than that ofmost bioceramics and its mechanical strength is better than that ofbiopolymers. The elastic modulus and density are also close tothose of natural cortical bones. These advantages suggest potentialuse of Mg and Mg alloys in biodegradable applications [24e27] aswell as reinforcement for ceramic [28] and polymeric [18] implants.Currently, the major drawback of magnesium and its alloys is thelow corrosion resistance and production of hydrogen in thecorrosion process [29e31]. Much effort has beenmade to overcomethe hurdles by for example, alloying [32e34] and surface treatmentsuch as deposition of protective coatings [35e38]. Alkaline degra-dation of magnesium by adjusting the local pH of the immersionmedium has been reported [18] and this may provide a newway tosolve the low pH problem associatedwith long-term degradation ofPLA.

In this work, low-molecular-weight PLA-based biocompositesare reinforced unidirectionally with high-strength Mg alloy wires(MAWs) and studied experimentally and theoretically by the finiteelement method (FEM). Micro arc oxidization (MAO) is conductedon the MAW reinforcements to strengthen the composites. Accel-erated and regular degradation tests are performed to assess thedegradation behavior with the objective of developing novelbiodegradable composites for load-bearing applications.

2. Materials and methods

2.1. Materials

MAWs composed of AZ31 (96% Mg, 3% Al and 1% Zn by weight) with a diameterof 0.3 mm were fabricated by continuous smelting, casting, hot extrusion, wetdrawing, and annealing. PLA particles with a density of 1.24 g/cm3 were purchasedfrom Shenzhen Esun Industrial Co., Ltd., China. The viscosity average molecularweight ðMvÞ of PLA was calculated to be 60,000 g/mol using the Mark-Houwink-Sakurada formula [39] according to the intrinsic viscosity at 25 �C using an Ubbe-lohde viscometer. The crystallinity and glass transition temperature of the PLA were38% and 64 �C based on differential scanning calorimetry (DSC) [11].

2.2. Methods

2.2.1. Materials preparationThe MAW contents in the composites were predetermined to be 5, 10, 20, and

40 vol% (mean volume fraction). The dimensions of the samples were120 mm� 12 mm� 2 mm (length �width � height) and the approximate amountsof MAWs were 16, 34, 68, and 136 to obtain mean volume fractions of 5, 10, 20, and40 vol%, respectively. The true volume fraction of the MAWs was calculated bydividing the real volume of theMAWs by the volume of the specimen and the resultsare shown in Table 1. For a mean volume fraction of 5 vol%, the true volume fractionwas 4.7 vol%. The composite specimens were fabricated by the lamina stackingmethod. The dimensions of the laminawere 120mm� 12mm� 0.4 mm. Two kindsof laminas including MAW-containing laminas and pure-PLA laminas were utilizedto ensure the total thickness of the laminas to be about 2 mm. The amount of theMAW-containing laminas in the different composites and corresponding quantity ofMAW per lamina are shown in Table 1. The MAWs in each lamina were uniformlydistributed and the MAW-containing laminas were symmetrically distributed aboutthe middle plane of the stack along the height direction.

Preparation of the composite is schematically illustrated in Fig. 1. The PLA par-ticles were dissolved in chloroform. TheMAWswere directionally arranged and PLA/chloroform solution was poured to overlay the directional MAWs, followed byevaporating in air for 12 h to form the thin pre-impregnating composite laminas. Thepure-PLA laminas were fabricated by the same process. Afterwards, the laminas

Table 1Characteristics of MAWs/PLA composites.

Mean volumefraction (%)

True volumefraction (%)

MAW-containinglamina numbers

MAW numbersper lamina

Pure-PLA e e e

5 4.7 2 810 10 2 1720 20 4 1740 40 4 34

were stacked in a mold cavity. The stack was heated and compressed for 15 min at5 MPa and 190 �C. Finally, the stack was cooled naturally to room temperature alongwith the mold in an oven at 5 MPa. After demolding, the plate specimens with thepredetermined dimensions of 120 mm � 12 mm � 2 mm were produced and purePLA specimens were prepared by the same process as controls. The dissolvingprocess was to further determine the surface morphologies of MAWs in the com-posite after immersion tests. The composites reinforced with the micro-arc oxidized(MAO) MAWs were fabricated by the same procedures.

2.2.2. Finite element method (FEM)The theoretical strength of the composite, including the tensile and bending

strength, was calculated by the finite element method (FEM) using Ansys softwarewith the implicit solver. The beam element and solid element were, respectively,assigned to MAWs and PLA. The elastic model of PLA and elasto-plastic model of Mgalloy wires were applied. The interfaces between the MAWs and PLA during simu-lation were theoretically treated implying complete bonding.

2.2.3. Micro arc oxidationThe MAWs were gently washed with acetone, distilled water, and ethanol and

ultrasonically cleaned three times. The wires were suspended in an aqueous elec-trolyte composed of sodium silicate (15 g/L), sodium phosphate (5 g/L), sodiumhydroxide (2 g/L), and K2ZrF6 (3 g/L) and subsequently processed in the WHD-30type MAO equipment [40] for 3.5 min. The constant current mode was used andthe forward and negative current was 6 A/dm2. Afterwards, the wires were removedand washed with deionized water.

2.2.4. In vitro degradation testsTheMAWs in the specimens for the invitro degradation testswere pretreatedusing

MAO. The individual samples were placed in 50 mL screw-top plastic bottles and fullyimmersed in the Sorensen's phosphate-buffered solution (SPB). The SPB was preparedby mixing stock solution A (9.078 g KH2PO4 in 1000 mL distilled water) and stock so-lution B (11.876 g Na2HPO4 in 1000 mL distilled water) at a volume ratio of 18.2e81.8.Thebottleswerekept ata constant temperatureof37 �C fornormaldegradationor50 �Cin accelerated degradation [41]. The ratio of the solution inmilliliters to themass of thespecimen in grams was greater than 30:1. The immersion durations for normal degra-dationwere 7,14, 28, and 56 days, whereas those for accelerated degradationwere 1, 7,14, and 21 days. The solutionwas changed every 1 day to keep the pH value at 7.4± 0.2.Before the immersion solutionwas changed, the pH wasmeasured.

The viscosity average molecular weight ðMvÞ of the PLA during immersion wascalculated by the Mark-Houwink-Sakurada formula [39] based on the intrinsic vis-cosity at 25 �C monitored by the Ubbelohde viscometer. The initial mass (m0) of thesample with dimensions of 25 mm � 12 mm � 2 mm for the mass loss test wasrecorded and the final mass (mt) of the sample after immersion was obtained afterdrying for 48 h in an oven at 37 �C. The overall percentage mass change (u) wascalculated by the following equation:

u ¼ ((m0�mt)/m0) � 100%. (1)

2.2.5. Determination of mechanical propertiesBefore the mechanical tests of the composites, the tensile properties of the initial

MAWswith a length of 120mmand PLAwith dimensions of 120mm� 12mm� 2mmfabricatedby the same fabricationprocessweredetermined. The typical tensile curve ofMAWs is depicted on the left of Fig. 2. The MAWs show approximately bilinear-plasticdeformation under tension and the mechanical properties of the MAWs and PLA forFinite Element Method (FEM) analysis are listed in Table 2.

The fabricated specimens were cut into dimensions of 60 mm� 12mm� 2mm,60mm� 12mm� 2mm, and 30mm� 12mm� 2mm for the bending, impact, andshear tests, respectively conducted on the CMT4503 electronic universal testingmachine at room temperature. In order to produce similar wet testing conditions forthe immersed specimens according to the literature [9,42], the as-prepared com-posites were immersed in the SPB solution for 1 h before their mechanical propertieswere determined. The crosshead speed was, respectively, 5, 2, and 5 mm/min andthe Charpy impact test was performed on the unnotched samples using the ZBCimpact testingmachine, as shown in Fig. 2. The tensile strength (St) of the samples inthe wire direction was measured. The bending strength (Sb) of the samples wasmeasured by the three-point bending method according to the standardASTMD790-2010 for a span of 32 mm. The shear strength (Ss) of the compositessubjected to transversal shear loading was measured by the dual shear test. Theshear test was similar to that used byWeir et al. [41]. The plate sample was fixed andsheared simultaneously on both ends of the crosshead under constant speed control.All the mechanical strength values were the averages of three measurements.

2.2.6. Microstructural characterizationSmall pieces of thewiresweremounted on stubs using adhesive tapes. The stubs

and composites were sputter-deposited with a thin gold layer in an argon atmo-sphere. The wire and fracture morphology was examined on a Philips XL30 FEGscanning electron microscope (SEM) at an accelerating voltage of 20e25 kV.

Fig. 1. Illustration of preparation process of the MAWs/PLA composites and the pictures in the center are those of the as-prepared specimens.

Fig. 2. Load-displacement curve of MAWs under tension and illustration of the mechanical tests conducted on the composite.

X. Li et al. / Biomaterials 49 (2015) 135e144 137

3. Results

3.1. Mechanical properties

Mv of the PLA in the fabricated composites and pure PLA sam-ples can be controlled to be between 50,000 and 55,000 g/mol. Thisenables more direct investigation of the MAW effects on the me-chanical strength of the composites, as shown in Table 3. The in-crease in the tensile strength (St) is proportional to the MAWcontent and a high strength of nearly 110 MPa is achieved at 40 vol%. The load-displacement curves of the composites under tensionare shown in Fig. 3. The load increases linearly at first, exhibits an

Table 2Properties of MAW (f 0.3 mm) and poly-lactic acid (PLA).

Poisson ratio Density (g/cm3) Elastic modulus (G

MAW (f 0.3 mm) 0.35 1.8 45PLA 0.36 1.24 4.0

abrupt drop, and then declines gradually. The sharp drop may bedue to breakage of PLA because it is the same as the bearing load ofthe PLA matrix in the composite when failure occurs. The ratio ofthe bearing load of each component in the composite to themaximum load of the composite (uLoad) at this time can be calcu-lated. uLoad of the PLA matrix in the composite (uLoad-PLA) is calcu-lated by dividing the reduced value by the maximum load value ofthe composite and uLoad of the MAWs in the composite (uLoad-Mg)can be obtained. At 5 vol%, uLoad-Mg is 43.7%, indicating that theMAWs constitute the main underpinning body. When the MAWcontent goes up to 10 vol%, uLoad-Mg increases significantly to 70.5%.If the MAW content is increased from 20 to 40 vol%, uLoad-Mg

Pa) Yield strength (MPa) Tensile strength (MPa) Tensile strain

270 316 0.16e 46 0.0115

Table 3Mechanical properties of MAWs/PLA composites.

Mean volume fraction of MAWs (vol%) St (MPa) Sb (MPa) Si (kJ/m2) Ss (MPa)

Mean SD FEM Mean SD Mean SD Mean SD

Pure PLA 46 (±5.66) 47 88 (±0.95) 5 (±3.0) 45 (±0.74)5 50 (±2.05) 57 99 (±4.24) 18 (±4.07) 56 (±0.13)10 65 (±0.06) 68 119 (±2.16) 27 (±10.19) 63 (±1.55)20 80 (±3.54) 91 136 (±7.54) 90 (±26.94) 73 (±0.91)40 108 (±3.73) 136 190 (±0.41) 150 (±40.38) 67 (±0.70)

X. Li et al. / Biomaterials 49 (2015) 135e144138

increases slightly from 83.1% to 84.0%. The final gradual declinein the curve may stem from gradual fracture and evulsion ofthe MAWs due to poor interface bonding between the MAWs andPLA.

The bending strength (Sb) of the composites increases to about190 MPa at 40 vol% and it is about twice that of pure PLA. The load-deflection curves of the composites under bending loads are pre-sented in Fig. 4. The load increases linearly initially and then de-creases gradually at 0 and 5 vol% but stepwise at 10 and 20 vol%.This decrease may be related to breakage of the PLA on the bottomsurface of the composite as shown in the upper right picture inFig. 4. The later stepwise decrease may be associated with gradualrupturing of the MAWs along the bending direction of the com-posite. Fig. 5(a) and (b) depict the bending fracture morphology ofthe 20 vol% composite. Fig. 5(a) shows decreased wire diameter atthe fracture section, suggesting that the wires undergo plasticdeformation during the bending tests.

The impact strength (Si) of the composites increases signifi-cantly from 18 kJ/m2 for 5 vol% to 150 kJ/m2 for 40 vol%. The value ofthe 40 vol% composite is approximately 29 times larger than that ofpure PLA and almost equal to that of the PLLA e 30 wt% HA

Fig. 3. Load-displacement curves of the composites with different MAW co

composite reported previously [11]. This high impact strengthprotects the fixed bone fracture parts from external impact. Fig. 5(c)and (d) show the impact fracture morphology of the 20 vol%composite. The size of the MAWs decreases at the fracture sectionand there are plenty of cracks in the matrix around the MAWssuggesting that the composites have large Si.

The shear strength (Ss) of the composites displays a differenttendency which increases initially and then decreases withincreasing MAW content. At 20 vol%, Ss reaches a peak value ofabout 73 MPa which is 0.65 times larger than that of pure PLA,indicating that the composite has good rigidity and ductility.Fig. 5(e) and (f) show the shear fracture morphology of the 20 vol%composite. The MAWs have an oval shape and there are manydisordered cracks in the matrix.

3.2. Theoretical mechanical strength assessed by FEM

In spite of the aforementioned encouraging results, the prop-erties, especially St and Sb, are not ideal due to the poor interfacebetween the MAWs and PLA and so the force cannot be efficientlytransferred from the matrix to the reinforcements [30,31]. Hence, it

ntents under tension: (a) 5 vol%; (b) 10 vol%; (c) 20 vol%; (d) 40 vol%.

Fig. 4. Load-deflection curves of the composites with different MAW contents underbending load.

X. Li et al. / Biomaterials 49 (2015) 135e144 139

is essential to conduct a theoretical evaluation of the mechanicalstrength in order to improve the interface. The theoretical St of thecomposites derived by FEM is shown in Table 3. At a content below10 vol%, the FEM results are almost in line with experimental data.However, there is a marked increase at 40 vol% reaching 136 MPa

Fig. 5. Fracture morphology of the composites with 20 vol% MAWs: (a) Bending fracture (lmagnification); (d) Impact fracture (high magnification); (e) Shear fracture (low magnificat

that is 0.26 times larger than that of the experimental value, sug-gesting the possibility to further improve St.

Sb is an important index for bone fixation devices. However, thepresent composites are anisotropic and the bending strength isrelated to various factors such as the volume fraction and distri-bution of the MAWs as well as distance between the MAWs andneutral plane of the composite samples (hi). The different distri-butions along the cross section (involving different hi, MAW-containing lamina number, and MAW number per lamina) of theMAWs in the 40 vol% composite are shown in Fig. 6. A large value of300 MPa can theoretically be attained at 40 vol% and it is muchlarger than the experimental value, indicating that the mechanicalproperties can be further improved by modifying the internalstructure. Moreover, the theoretical properties can be tailored sinceSb varies between 200 MPa and 300 MPa.

FEM is performed to investigate the bending behavior of thecomposites by changing the volume fraction and diameter of theMAWs (assuming no change in the tensile properties of the MAWswith diameters between 0.3 mm and 0.5 mm). Fig. 7 shows that200 MPa which is sufficient for load-bearing bone fixation appli-cations can be achieved from the 20 vol% composite. In order tostudy the influence of various parameters, the equivalent sectionmethod (ESM) commonly used to calculate Sb of reinforced con-crete in computational mechanics is adopted [43]. Compared toreinforced concrete, these composites share some similarities suchas the brittle matrix, high strength, and directional reinforcement,whereas the main difference is that the MAWs here and steel barsin concrete exhibit plastic deformation and elastic deformation,

ow magnification); (b) Bending fracture (high magnification); (c) Impact fracture (lowion); (f) Shear fracture (high magnification).

Fig. 6. Sb of 40 vol% MAWs/PLA composite with different wire distributions by FEM.

X. Li et al. / Biomaterials 49 (2015) 135e144140

respectively, when the matrix fractures. If deformation of MAWscan be treated as an elastic behavior, Sb of the composites can bedetermined by ESM and in this case, the effective elastic modulus isadopted.

The PLA on the bottom surface of the composite only experi-ences tensile stress during bending followed by early-stage frac-ture. The stress on the bottom surface (s) during failure is about thesame as that of pure PLA. As the MAWs in the composite aresymmetrically arranged about the neutral plane, Sb of the com-posites can be calculated as follows:

s ¼ M*y=Iz ¼ Sb�PLA; (2)

Iz ¼ IMg þ IPLA ¼ bh3.12þ

Xi

�n� 1

�pr2i h

2i ; (3)

M ¼ FL=4; (4)

Sb ¼ 3FL.2bh2 ¼ 12Sb�PLAIz

.bh3: (5)

whereM is the bendingmoment (N,mm), y is the distance betweenthe bottom surface and neutral plane (mm), Iz is the equivalentinertia moment of the composite (mm4), Sb-PLA is the bendingstrength of pure PLA (MPa), IMg is the inertia moment of the MAWs

Fig. 7. Sb of the predetermined composites by FEM and ESM with the predetermineddiameters of the MAWs being 0.3 mm, 0.4 mm, and 0.5 mm.

(mm4), IPLA is the inertiamoment of the PLA (mm4), b is thewidth ofthe specimen (mm), h is the thickness of the specimen (mm), n isthe ratio of the effective elastic modulus of the MAW to the elasticmodulus of the PLA matrix, ri is the radius of MAW (mm), hi is thedistance between MAW and neutral plane (mm), F is the bendingload (N), L is the support span (mm). The ESM calculation process isillustrated in Fig. 8. The first step is to obtain Sb of the pre-determined composites by FEM, followed by derivation of thecorresponding Iz and n. Thereafter, n is manipulated by a least-square method to obtain a value of 6.667, suggesting that theeffective elastic modulus of theMAW is 26.67 GPa. Sb is recalculatedusing n ¼ 6.667 and the results are shown in Fig. 7. The ESM resultsare in general agreement with those by FEM thus validating thatthe proposed model is feasible and reliable.

3.3. Interface improvement by MAO

The importance of interface improvement is apparent accordingto the experimental and FEM results. In this respect, MAO canproduce a rough and porous surface on the MAWs to improve thebonding between the MAWs and PLA in the composites. The sur-facemorphology of theMAWs before and afterMAO are depicted inFig. 2. A rough and porous surface can be observed from the MAWsafter MAO and the tensile strength of the MAWs decreases to about310 MPa. The load-displacement curves of the composites rein-forced with the MAO MAWs (composites-MAO) under tension andpictures of the broken specimens are shown in Fig. 9(a). Comparedto the composites reinforced with the untreated MAWs, no obviousevulsion can be observed when failure occurs, indicating improvedinterfacial bonding between the matrix and reinforcements.

St and Sb of the MAO composites are shown in Fig. 9(b). At 20 vol%, St is nearly 100 MPa that is 14% larger than that of the compositewithout undergoing MAO. However, St of the MAO composites is alittle larger than that provided by FEM. This may be attributed tothe larger contact regions and special interfacial micro-anchoringaction between the PLA and MAWs. This phenomenon providesclues about the benefits of using MAO to strengthen the interface.Since the samples are prepared under the same conditions, thechange in Sb reflects the effects of MAO on the mechanical prop-erties of the samples. Obviously, Sb of the MAO composites is largerthan that without undergoing MAO. Sb of the 20 vol% MAO com-posite is about 150 MPawhich is 11% larger than that without MAO.

3.4. Degradation characteristics

Although degradation of PLA is relatively complex, the mainchanges are reduction in the molecular weight initially as well as

Fig. 8. Calculating process on Sb of ESM.

Fig. 9. Effects of MAO of MAWs on the mechanical properties of the composites: (a) Load-displacement curves of the MAO composites under tension and pictures of the brokensamples; (b) Mechanical properties of different composites and the interface illustration between PLA and MAO MAWs in the composite.

X. Li et al. / Biomaterials 49 (2015) 135e144 141

loss of mechanical strength and subsequently real mass [9,44].There are many factors that influence the degradation rate of PLA.High crystallinity, low stress, and orientation may suppress thedegradation rate [45,46], while high temperature [41] and acidity[11] tend to increase the degradation rate. To investigate the effectsof the molecular weight and crystallinity of the PLA, immersion for21 days (3 weeks) at 50 �C for accelerated degradation and 56 days(8 weeks) at 37 �C for normal degradation is performed. The MAWreinforcements in the immersed specimens undergo MAO toimprove the interface and prevent the MAWs from rapid corrosion.The degradation behavior is examined as a function of MAW con-tent (0e20 vol%) in relation to u, Mv, Sb, and the results are sum-marized as follows.

The percentage mass loss (u) during accelerated and normaldegradation is shown in Fig. 10(a). Both u values exhibit a slightincrease proportional to the MAW content. As there is hardly anymass loss from pure PLA, this slight increase may be related todegradation of the MAO MAWs. However, the largest u is no morethan 1% indicating a fairly low degradation rate of MAWs duringimmersion and suggesting long-term reinforcing action of MAWsand good strength retention ability of the composites.

The change in Mv of the pure PLA and the PLA in the 20 vol%MAWs/PLA composite versus immersion time at different temper-ature is shown in Fig. 10(b). Mv decreases significantly with im-mersion time and a larger decrease rate is observed at a highertemperature. Obviously, Mv of the PLA in the composite shows asimilar trend as pure PLA in the early stage. A smaller decrease rate

Fig. 10. (a) Changes in the mass of the composite with MAW contents and (b) Viscosity averadifferent immersion temperature.

after 7 days at 50 �C or 14 days at 37 �C indicates a differentdegradation behavior. After immersion for 21 days at 50 �C, the Mv

values of pure PLA and PLA in the composite are 25% and 45% of theinitial values, respectively. The values are 49% and 66% after 56 daysat 37 �C denoting relatively larger Mv retention at 37 �C. Moreover,during the immersion period, the pH of the solution is measured.The average pH of the solution immersed with pure PLA varies inthe range between 7.32 and 7.39 during the immersion period,whereas that immersed with the composite (20 vol%) changes from7.38 to 7.60. These variations are within the controlled pH range ofthe solution (7.4 ± 0.2), indicating that little degradation productsare released from both samples into the solutions duringimmersion.

The change in Sb of the composite versus immersion time isshown in Fig. 11(a) and (b). Sb of pure PLA at 37 �C and 50 �C de-creases with a similar concave shape, whereas Sb of the 20 vol%composite shows a convex decrease. At 37 �C, Sb of pure PLA and thecomposites decreases gradually versus immersion time. After 56days, the Sb values of pure PLA and 20 vol% composite are 56 MPaand 110 MPa, respectively, which are 64% and 74% of the initialvalues, indicating good strength retention ability. This ability isfurther verified by the integrity of the MAWs. There are MAOcoating fragments and no visible corrosion pits on the wire surfaceafter immersion. At 50 �C, a faster decrease in Sb is observed. After21 days, the Sb values of pure PLA and the 20 vol% composite are10 MPa and 96 MPa, respectively, which are 11% and 65% of theinitial values. The higher level of strength retention may be

ge molecular weight of pure PLA and PLAwith 20 vol% MAWs versus immersion time at

Fig. 11. Changes in Sb of the composites with different MAW contents versus immersion time at (a) 37 �C and (b) 50 �C.

X. Li et al. / Biomaterials 49 (2015) 135e144142

attributed to the MAWs which retain the integrated and continu-ously reinforced PLA during immersion. Sb of the composites after14 days at 50 �C is the same as that of the composites after 56 daysat 37 �C and hence, Sb of the composite after immersion for 2 weeksat 50 �C reflects that of the corresponding composite after 2monthsat 37 �C.

4. Discussion

4.1. Strengthening and toughening of the composites

High-strength biodegradable PLA-based composites havebeen investigated. The materials can be classified as self-reinforcing, particle-reinforcing, and fiber-reinforcing and thematerials described here are considered fiber-reinforcing. TheMAW reinforcements have large diameters and deliver betterfailure strain than conventional fibers. For instance, the tensilestrain of the MAWs is 0.16 that is 14 and 15 times larger than thatof pure PLA and carbon fibers, respectively [47]. The toughened40 vol% composite has a remarkable impact strength of 150 kJ/m2

which is nearly 5 times larger than that of PLA incorporated withthe same amount of carbon fibers [47], although carbon fibershave larger tensile strength and elastic modulus. The value of150 kJ/m2 is sufficient to satisfy the impact-resistant re-quirements of human bones enabling effective protection againstexternal impact.

Even though themolecular weight of PLA is only about 60,000 g/mol that is smaller than those of other materials (Table 4), Sb of190 MPa which is sufficiently large in practice arises from thestrengthening effects of MAWs as their tensile strength is as large as316 MPa. The low molecular weight leads to large degradation ratewhich bodes well for temporary bone fixation.

Table 4Characteristics and mechanical properties of PLA-based composites used for fixation dev

Shape Initial Mv

(1000 g/mol)St (MPa) S

PLLA/HA-30 wt% Rod 400 121 2PDLA Rod 280 e 1SR-PLLA Pin 660 e 2PLLA Rod 220 e 2PLLA Rod 133 69.8 e

SR-PLLA Rod 260 e 2PLA/unidirectional carbon fibers-40 vol% Plate 100 220 e

PLA/unidirectional MAWs-40 vol% Plate 60 108 (~136a) 1

e No mention.a In theory.

One strengthening approach is internal structure modification.Sb of the composites can go up to 300 MPa in the 40 vol% com-posites by adjusting the internal MAW distribution. It is a conve-nient way to obtain composites with variable strength to cater todifferent applications and would be difficult to achieve using asingle type of materials. The numerical model on Sb proposed hereenables quick evaluation of the materials. Different biomedicaldevices have special requirements such as geometry, size, andmechanical properties and this model can be used to assess themechanical properties to validate and expedite the design.

Another approach to strengthen the composite is interfacestrengthening. Poor interfacial bonding between the PLA andMAWs compromises the mechanical integrity. Conventional inter-face strengthening methods utilize covalent bonding between themodified region and substrate, for example, by applying acompatible layer to the interface or incorporating the appropriatefunctional groups to create strong adhesion between the substrateand layer [46]. In this work, MAO is employed to prepare a roughand porous coating on the MAWs to anchor the PLA while in-gredients in the PLA solution penetrate the pores, as shown in theupper right of Fig. 9(b). The micro-anchoring provides strongphysical bonding to strengthen the interface, transfer the loadingfrom the matrix to reinforcements, strengthen the MAWs, and ul-timately enhance mechanical properties of the composites.

High-strength PLA-based composites are commonly producedby self-reinforcing at a low temperature, as shown in Table 4, butour composites are prepared at a relatively high temperature. Theself-reinforcing process can alter the chain orientation to improvethe properties of the PLA. Although the degradation rate increasesslightly by increasing the molecular weight or changing theorientation, the materials can satisfy the requirements of long-termweight-bearing bone fixation.

ices reported previously.

b (MPa) Si (kJ/m2) Fabricating process Fabricatingtemperature (�C)

Reference

69 166 Forging 103 [11,48]80 e Solid-state extrusion 120 [8]80 e Die-drawing e [12]40 e Die-drawing 100 [9]

e Mold-compressing 200 [49]71 e Mold-compressing 162e174 [50]

25 Mold-compressing 110 [47]90 (~300a) 150 Mold-compressing 190 Present

Fig. 12. Illustration of degradation process of the composites: (a) Degradation of PLA; (b) Cracks in the MAO coating on the MAWs; (c) Disintegration of MAO coating from theMAWs.

X. Li et al. / Biomaterials 49 (2015) 135e144 143

4.2. Analysis of the degradation behavior and biocompatibility

The ideal temporary bone fixation device should have highstrength retention during healing and undergo fast degradationafter healing. Therefore, it is imperative to fathom the degradationbehavior. The main degradation mechanism of PLA is hydrolysis[7,11,51] which involves hydrolytic cleavage of the ester linkage toform acidic carboxyl end groups and oligomers. The solubledegradation products close to the surface escape readily but thosein the bulk cannot diffuse out of the PLA, resulting in high internalacidity and reduced pH. Moreover, the acidic products catalyze theester hydrolysis reaction [11]. The PLA in the composites describedhere have a different degradation behavior for its higher mass lossrate and slower molecular weight decrease than pure PLA. Ac-cording to theMAO coating fragments on the surface of MAWs afterimmersion for 56 days at 37 �C and visual integrity of MAW sub-strate after 21 days at 50 �C, the degradation process is shown inFig. 12. Initially, water molecules penetrate the PLA to trigger hy-drolytic degradation of the ester linkage and form acidic carboxylend groups [11]. As time elapses, the water molecules diffusethrough the PLA into the MAO coating causing degradation of theMAO coating. The initial MAO coating is a basic oxide. Cracksemerge locally and propagate resulting in eventual disintegrationwhich deteriorates the bonding between the MAO coating andMAW substrate. During degradation of the MAO coating, somesoluble ions such as OH� and Mg2þ are released and diffuse to theSPB resulting in the obvious mass loss from the compositescompared to pure PLA.

The slower degradation rate of the PLA in the composite miti-gates the pH decrease. It has been reported that the delayedadverse biological response such as bone resorption arises from pHreduction [52,53]. Many types of filler materials such as ceramicsand bioglass have been proposed to overcome the hurdle. Hennaet al. [14] reported that PLA-based composite filled with a bioactiveglass led to a more constant pH in the buffer solution and slowerdecreasing rate of the viscosity averagemolecular weight than purePLA in vitro. Agrawal and Athanasiou [54] studied the in vitrodegradation of PLA-PGA composites incorporated with calciumcarbonate, sodium bicarbonate, and calcium hydroxyapatite andshowed that the three ingredients altered the rate of pH decrease inthe vicinity of the PLA-PGA implants. Our composites exhibiteffective long-term stability due to degradation of the MAO coatingor MAWs. Hydroxide ions (OH�) released during degradationdiffuse into the PLA to counteract the acidic hydrogen ions releasedfrom the acidic carboxyl end groups. This neutralization maintainsa steady pH to mitigate degradation of the PLA matrix and enhancethe strength retention ability of the composites.

The biocompatibility of PLA and magnesium has been studied.Although the toxicity rendered by aluminum in Mg alloys iscontroversial, MgeAl alloys are generally considered biocompatiblebased on in vitro and in vivo experiments [21,55,56]. Degradableporous scaffolds made of the magnesium alloy AZ91D wereimplanted into the distal femur condyle of rabbits [57] and no

significant harm or inflammation was observed. Osteolysis aroundthe implants in rabbits was observed [55] and Xue et al. [58]investigated the in vivo biocompatibility of AZ31 and AZ91D al-loys at different places of the mouse. Histological results obtainedfrom the liver, heart, kidney, skin, and lung of the mouse after twomonths suggested that the MgeAleZn alloys had good biocom-patibility. Furthermore, the dispersive MAWs prevent a largeamount of hydrogen release which would otherwise occur on bulkmagnesium alloys. Consequently, the risk of tissue reaction causedby needle-shape fibers or fragments is reduced substantiallyreduced.

5. Conclusion

Biodegradable PLA-based composites reinforced with high-strength magnesium alloy wires are produced for load-bearingbone fixation applications. The materials have excellent strength,toughness, and impact strength due to the unidirectional rein-forcing effects rendered by the MAWs. Analysis by FEM indicatesthat the strength of the composite can be further improved. Anumerical model about the bending strength is formulated andpredicts that the bending strength can be larger than 300 MPa for40 vol% MAWs, although the PLA has a low viscosity average mo-lecular weight of 60,000 g/mol. Micro arc oxidation conducted onthe MAWs improves the interfacial bonding between the MAWsand PLA and consequently, the tensile strength and bendingstrength of the composites are enhanced. The materials have highstrength retention ability according to the accelerated and normaldegradation tests and moreover, the degradation rate of PLA de-creases after incorporation of the MAO treated MAWs. The rein-forced composites are promising biodegradable materials in load-bearing applications.

Acknowledgments

The work was supported by Hong Kong Research Grants Council(RGC), General Research Funds (GRF) No. CityU 112212 and CityUniversity of Hong Kong Strategic Research Grant (SRG) No.7004188.

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