Author’s Accepted Manuscript

Flexural and torsional properties of a glass fiber-

reinforced composite diaphyseal bone model with
multidirectional fiber orientation

Kalle A. Dahl, Niko Moritz, Pekka K. Vallittu

www.elsevier.com/locate/jmbbm

PII: S1751-6161(18)30453-3
DOI: https://doi.org/10.1016/j.jmbbm.2018.07.027
Reference: JMBBM2895
To appear in: Journal of the Mechanical Behavior of Biomedical Materials
Received date: 5 April 2018
Revised date: 20 June 2018
Accepted date: 17 July 2018
Cite this article as: Kalle A. Dahl, Niko Moritz and Pekka K. Vallittu, Flexural
and torsional properties of a glass fiber-reinforced composite diaphyseal bone
model with multidirectional fiber orientation, Journal of the Mechanical
Behavior of Biomedical Materials, https://doi.org/10.1016/j.jmbbm.2018.07.027
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Flexural and torsional properties of a glass fiber-reinforced composite diaphyseal bone model with

multidirectional fiber orientation

Kalle A. Dahla,*, Niko Moritza,c, Pekka K. Vallittua,b

a
Department of Biomaterials Science and Biocity Turku Biomaterials Research Program, Turku

Clinical Biomaterials Centre – TCBC, Institute of Dentistry, University of Turku, Turku, Finland

b
City of Turku Welfare Division

c
Biomedical Engineering Research Group, Turku Biomaterials Research Program

*Correspondence to: Turku Clinical Biomaterials Centre – TCBC, Institute of Dentistry, University

of Turku, Itäinen pitkäkatu 4 B (2 nd floor), 20520 Turku, Finland. Tel.: +358 2333 8227 (office). E-

mail address: kaalda@utu.fi (K.A. Dahl)

Abstract

Although widely used, metallic implants have certain drawbacks in reconstructive bone surgery.

Their high stiffness in respect to cortical bone can lead to complications which include

periprosthetic fractures and aseptic loosening. In contrast to metallic alloys, fiber-reinforced

composites (FRC) composed of a thermoset polymer matrix reinforced with continuous E-glass

fibers have elastic properties matching those of bone. We investigated the mechanical properties

of straight FRC tubes and FRC bone models representing the diaphysis of rabbit femur prepared

from glass fiber/bisphenol A glycidyl methacrylate (BisGMA) - triethylene glycol dimethacrylate

(TEGDMA) composite in three-point bending and torsion. Three groups of straight FRC tubes with

different fiber orientations were mechanically tested to determine the best design for the FRC bone

model. Tube 1 consisted most axially oriented unidirectional fiber roving and fewest bidirectional

fiber sleevings. Fiber composition of tube 3 was the opposite. Tube 2 had moderate composition of

both fiber types. Tube 2 resisted highest stresses in the mechanical tests and its fiber composition

was selected for the FRC bone model. FRC bone model specimens were then prepared and the

mechanical properties were compared with those of cadaver rabbit femora. In three-point bending,

FRC bone models resisted 39 %-54 % higher maximum load than rabbit femora with similar

flexural stiffness. In torsion, FRC bone models resisted 31 % higher maximum torque (p<0.001)

and were 38 % more rigid (p=0.001) than rabbit femora. Glass fiber-reinforced composites have

good biocompatibility and from a biomechanical perspective, they could be used even in

reconstruction of segmental diaphyseal defects. Development of an implant applicable for clinical

use requires further studies.

Graphical abstract

Keywords:

Fiber-reinforced composite
Implant

Mechanical testing

Segmental bone defect

1. Introduction

Currently metallic implants are state-of-the-art applications in reconstructive bone surgery.

However, metallic alloys have certain drawbacks as materials in bone implants including their

mismatch of biomechanical properties with bone (Ramakrishna et al. 2001). Metallic alloys have

considerably higher modulus of elasticity than cortical bone. Therefore metallic implants are often

too rigid overprotecting bone from natural mechanical stresses. This stress shielding effect results

in bone resorption around the implant (Woo et al. 1984). Fracture fixation with rigid plates or

intramedullary nails overloads the bone-implant interface and prevents callus formation, thus

slowing the fracture healing process (Lill et al. 2003, Sha et al. 2009). Metallic implants are also

prone to wear releasing small particles causing cytotoxic and inflammatory reactions in the

surrounding tissues (Mokka et al. 2013). These factors may lead to mechanical complications

including periprosthetic fractures and aseptic loosening of an implant. Furthermore, metallic

implants limit postoperative imaging possibilities and radiation therapy in the area (Dabirrahmani et

al. 2015, Stenson et al. 1997).

The mismatch of mechanical properties between bone and metallic implants has stepped up

interest on research with fiber-reinforced composites in orthopedic applications since the 1980s.

Satisfying results with carbon-fiber-reinforced polyetheretherketone (CFR-PEEK) composite

implants have been reported with fracture fixation plates, intramedullary nails and in spine surgery

(Hak et al. 2014, Evans, Gregson 1998). In contrast to metallic alloys, glass fiber-reinforced

composites have a modulus of elasticity equivalent to that of cortical bone, which makes them

attractive materials for bone implants. Adequate stiffness of an implant can be achieved with even

high glass fiber composition in the polymer matrix, thereby enabling an implant to carry high loads

(Abdulmajeed et al. 2011). The use of thermoset polymers makes processing sophisticated
composite structures easier compared to thermoplastic polymers such as PEEK (Evans, Gregson

1998). E-glass containing fiber-reinforced composites (FRC) with thermoset polymer matrix have

acceptable biocompatibility (Lazar et al. 2016). In vivo studies have shown osseointegration of well

polymerized FRC comparable to titanium (Ballo et al. 2014). Osteoconductive, osteoinductive and

antibacterial properties of FRC can be promoted using different coating or surface modification

methods, such as adding bioactive glass in the composite (Nganga et al. 2012, Zhang et al. 2010).

Glass fiber/BisGMA-TEGDMA composites have already been successfully used in dentistry and

cranial surgery (Aitasalo et al. 2014, Piitulainen et al. 2015, Posti et al. 2016, Vallittu 2017). Studies

with implants of this composite material on rabbit long bones have shown promising results (Ballo

et al. 2014, Moritz et al. 2014, Zhao et al. 2009).

Table 1 – Mechanical properties of biomaterials (Vallittu et al. 2015)

Modulus (GPa) Tensile Strength (MPa)

Stainless steel 190 586

Cobalt-chromium alloy 210 1085

Titanium alloy 116 965

Glass fiber/BisGMA-TEGDMA 20 1200

(unidirectional 60 vol%)

Cortical bone (longitudinal) 17.7 133

Cortical bone can be considered as a continuously remodeling fiber-reinforced composite. Osteons

are basic units in cortical bone that have a cylindrical shape consisting of a central vascular canal

surrounded by multiple lamellae of collagen fibrils in a mineral matrix. The collagen fibrils are

oriented helically with the fibril orientation alternating in successive lamellae. Osteons with lamellae

of transversal spiral fibril orientation best resist compressive forces, whereas longitudinal spiral

course of fibrils make osteons resist tensile forces best. Distribution of osteon types varies in

different parts of bone reflecting the need to resist stresses specific for the part (Bonucci 2000). It
would be logical for a FRC diaphyseal bone model to be designed with various fiber orientations to

ensure its capability to resist different mechanical stresses. To our knowledge there haven´t been

studies investigating the mechanical properties of glass fiber/thermoset polymer composite

diaphyseal bone model.

Our long-term objective was to develop an FRC implant applicable for reconstruction of segmental

bone defects. In this study we investigated the influence of fiber orientation on flexural and

torsional properties of a tubular FRC structure; and the possibility of a roughly anatomical glass

fiber/BisGMA-TEGDMA composite diaphyseal bone model to match the elasticity and exceed the

strength of diaphyseal bone.

2. Materials and methods

2.1. Study design

First, three different groups of straight FRC tubes (tube 1, tube 2, tube 3) were prepared,

mechanically tested and analyzed to determine the best design for the FRC bone model. Amounts

of bidirectional glass fiber sleevings and unidirectional S-glass roving were the variables between

straight FRC tube groups (table 3). Then a series of FRC bone model specimens was prepared

and mechanically tested, and compared to data of cadaver rabbit femurs obtained from literature

and from earlier experiments in our laboratory.

2.2. Preparation of FRC

All specimens were designed to have a wall thickness of 1.5 mm which is slightly thicker than the

cortex in the diaphysis of rabbit femur. The composite consisted of BisGMA/TEGDMA (70/30 wt%)

matrix reinforced with pre-impregnated braided biaxial glass fiber sleevings and unidirectional S-

glass roving. Camphorquinone (0.7 wt%) and dimethylaminoethyl methacrylate (0.7 wt%) were

used as photoinitiator-activator system. For the preparation of straight FRC tube specimens, a

round plastic rod with 5 mm diameter was used as a mold. A three-dimensional geometrical model

of a rabbit femur was obtained as described in detail in our previous study (Zhao et al. 2009). The
shape of the medullary canal was extracted from this model. A teflon mold representing the

medullary canal of rabbit femur was made using a subtractive rapid prototyping machine (Roland

Model A MDX-40A, Roland Corporation, Hamamatsu, Japan). The pre-impregnated sleevings were

wrapped around the mold and pre-cured using a dental curing light (Elipar S10, 3M/ESPE, Seefeld,

Germany) (Fig. 1). The mold was removed and S-glass strands were added on the outer surface of

the sleevings as evenly as possible in axial orientation. Every strand was pre-cured separately with

a dental curing light. Subsequently the specimens were cured in a vacuum light oven (Visio Beta

vario, 3M/ESPE, Seefeld, Germany) for 15 min and in light oven (Targis Power, Ivoclar Vivadent

AG, Schaan, Liechtenstein) for 25 min. Materials used for the specimens are listed in table 2.

Table 2 – Materials used for the preparation of FRC

Material Type of material Manufacturer

Bisphenol A glycidyl methacrylate Co-monomer Esschem Europe Ltd,

(BisGMA) Seaham, United Kingdom

Triethylene glycol dimethacrylate Co-monomer Sigma-Aldrich Chemie GmbH,

(TEGDMA) Steinheim, Germany

2-(Dimethylamino)ethyl methacrylate Activator Sigma-Aldrich Chemie GmbH,

(DMAEMA) Steinheim, Germany

Camphorquinone Photoinitiator Sigma-Aldrich, Co., St. Louis,

USA

Sharx™ E26L25X, 0.25” diameter light Braided biaxial A&P Technology, Inc.,

fabric E-glass sleeving Cincinnati, USA

Sharx™ J26L50X, 0.50” diameter light Braided biaxial A&P Technology, Inc.,

fabric E-glass sleeving Cincinnati, USA

Sharx™ H29L50X, 0.50” diameter Braided biaxial A&P Technology, Inc.,

medium fabric E-glass sleeving Cincinnati, USA

XStrand® S roving MCX-S 21, fiber Unidirectional Owens Corning Mexico S. de

diameter: 24μ, bare glass tex: 2400 S-glass fiber R.L. de C.V., Mexico City,
tex roving Mexico

Table 3 – Glass fiber design of different FRC groups

Tube 1 Tube 2 Tube 3 Bone model

inner layer 0.25” light fabric 0.25” light fabric 0.25” light fabric 0.25” light fabric

sleeving sleeving sleeving sleeving

middle layer - 0.5” light fabric 0.5” medium 0.5” light fabric

sleeving fabric sleeving sleeving

outer layer 12 strands of S- 8 strands of S- 4 strands of S- 8 strands of S-

glass roving glass roving glass roving glass roving

Fig. 1 A) 3D-printed model of rabbit left femur. B) The teflon mold used for the fabrication of FRC

bone model specimens. C) Braided biaxial E-glass sleeving. D) Sleeving laid on the mold. E) Pre-
curing the sleeving. F) FRC bone model specimen after three-point bending test.

2.3. Mechanical testing

Three-point bending tests were performed with a material testing machine (Lloyd Instruments

LR30K Plus, Ametek Inc., Largo, USA) using configurations listed in table 4. FRC bone model

specimens were positioned with anterior direction in tension. Rods with 6 mm diameter were used

and axial bending load was applied until failure of specimens. In torsion tests a material testing

machine (Lloyd Instruments LRX, Lloyd Instruments Ltd., Fareham, England) was used as an axial

actuator attached to a custom-made fixture to achieve loading in torsion as shown in Fig. 1. Both

ends of the specimens were embedded in poly(methyl methacrylate) (PMMA) for a rigid fixation in

the testing machine. Torsional load was applied until failure and torque and rotation angle were

measured by a torque sensor (Kyowa TP-20KMCB, Kyowa Electronic Instruments Co. Ltd., Tokyo,

Japan) and an angle sensor (Green Pot CP-2F, Midori Precisions Co. Ltd., Tokyo, Japan).

Torsional rigidity (GJ) was calculated from the linear part of the torque-angle curve using following

equation: GJ=TL/θ, where T is the torque, L is the span length and θ is the angle in radians.

Table 4 – Configurations of the mechanical tests

 Subject Span length Loading rate No of

specimens

Three-point Tube 1 50 mm 1 mm/min 4

bending Tube 2 4

Tube 3 4

FRC bone 8

model

Torsion Tube 1 50 mm 64 deg/min 4

Tube 2 4

Tube 3 4

FRC bone 8

model

Rabbit femur 70 mm 64 deg/min 24

Fig. 2 – Setup in torsion tests

2.4. Micro-CT scan

One FRC bone model specimen was imaged by a micro-CT scanner (SkyScan 1072, Skyscan

N.V., Aartselaar, Belgium) to evaluate the fiber orientation of different glass fiber layers. Fiber

orientation of the inner and middle layers (biaxial sleevings) of the structure were measured from

four different sections of the specimen.

2.5. Burning

Six pieces of approximately 1 cm in length were cut from different FRC bone model specimens

after the mechanical tests, burned in an oven (Jelrus Infinity L30, Whip Mix, Louisville, KY, USA) at

700 deg C for 30 minutes and scaled before and after burning to evaluate fiber/resin –mass ratio.

2.6. Statistical analysis

ANOVA was used for comparison both between the straight FRC tube groups and between FRC

bone models and rabbit femora. Tukey´s HSD was used as a post-hoc analysis. The level of

statistical significance was considered to be 0.05. Statistical analysis was performed using IBM

SPSS Statistics program (version 24, IBM Corp., USA).

3. Results

Three-point bending and torsion tests were first performed for straight FRC tube groups: tube 1,

tube 2 and tube 3. Test results are listed in Table 5. Tube 2 resisted significantly greater bending

loads compared to tube 1 and tube 3 (p=0.048 and p=0.031 respectively). Torsional rigidity of tube

1 was significantly lower than that of tube 2 and tube 3 (p=0.001 and p<0.001). Other differences

were not significant and tube 2 was considered the best design for the FRC bone model.

Table 5 – Flexural and torsional properties of straight FRC tubes (sample mean ± sample standard

deviation)

Maximum Flexural Maximum Torsional

bending load stiffness torque (Nm) rigidity (Nm²)

 (N) (N/mm)

Tube 1 726 ± 30 894 ± 32 5.88 ± 0.91 0.91 ± 0.12

Tube 2 892 ± 133 971 ± 90 7.91 ± 1.50 1.27 ± 0.09

Tube 3 709 ± 48 858 ± 95 7.58 ± 0.69 1.41 ± 0.06

Sig. (ANOVA) p=0.023 p=0.164 p=0.057 p<0.001

Flexural properties of FRC bone models were compared to published properties of rabbit femora

obtained from literature (Table 6). In three-point bending, FRC bone models resisted 39 %-54 %

higher maximum load than rabbit femora with similar flexural stiffness but no statistical analysis

was performed. In torsion, FRC bone models resisted 31 % higher maximum torque (p<0.001) and

were 38 % more rigid (p=0.001) than rabbit femora. The micro-CT scan revealed the inner layer of

FRC bone models having a fiber orientation deviating 40.0° ± 4.7° and the middle layer 22.8° ±

2.6° from axial direction. Fiber/resin –mass ratio of FRC bone models was 0.72 ± 0.02.

Table 6 – Flexural and torsional properties of FRC bone models compared to rabbit femora

Maximum Flexural Maximum Torsional

bending load stiffness torque (Nm) rigidity (Nm²)

(N) (N/mm)

FRC bone 492 ± 46 439 ± 37 6.87 ± 0.64 1.52 ± 0.09

model
Rabbit femur, N/A N/A 5.23 ± 0.45 1.10 ± 0.30

our data

Rabbit femur, 353 ± 13 413 ± 19 N/A N/A

An et al. (1996)

Rabbit femur, 320 ± 33 488 ± 73 N/A N/A

Sevil, Kara

(2010)

4. Discussion

Results of the mechanical tests suggest that it is possible to produce diaphyseal bone models

matching the elastic properties and exceed the strength of diaphyseal bone using glass fiber/Bis-

GMA-TEGDMA composite. Utilizing various orientations of long glass fibers in the composite

results in beneficial mechanical strengths of a tubular FRC structure. Tube 2 was the strongest

design in axial bending despite containing less axially oriented fibers than tube 1. This is

assumably due to the greater amount of oblique fibers of the biaxial sleevings allowing tubular

structures to better resist deformation of the cross-section. Tube 3 contained even more oblique

and less axial fibers than tube 2, which however resulted in inferior axial bending strength without

improvement in torsional strength. Tube 2 and FRC bone model shared the same fiber design.

Maximum bending load and flexural stiffness, however, reduced to nearly half in FRC bone
models. This is mostly due to the ellipsoid cross-section of FRC bone models resulting in inferior

rigidity compared to circular cross-section of Tube 2.

Popular reconstruction methods in use after long bone diaphyseal resection include allografts,

fibular autografts, metallic endoprostheses and distraction osteogenesis (Panagopoulos et al.

2017). Segmental metallic endoprostheses offer early weight bearing and satisfactory functional

outcome but high rates of mechanical complications in the long term have limited their use

especially in younger patients with long life expectancy (Abudu et al. 1996, Aldlyami et al. 2005,

Benevenia et al. 2016, Hanna et al. 2010, Ruggieri et al. 2011). Harvesting a fibular autograft

creates a segmental defect in the fibula and is associated with donor site morbidity including ankle

instability and leg pain (Ling, Peng 2012, Vail, Urbaniak 1996).

Some studies on new alternative applications for reconstruction of segmental long bone defects

have been published. (Attias, Lindsey 2006, Lindsey et al. 2006) investigated a cylindrical titanium

mesh cage in combination with cancellous allograft bone, demineralized bone matrix putty and

titanium intramedullary nail in dog femora as well as three patients with traumatic tibial bone loss.

The method provided good new bone formation throughout the defect but it didn´t eliminate the

problematic elastic properties of metallic implants.

Tubular FRC implants could potentially be used in reconstruction of segmental long bone defects

instead of rigid metallic endoprostheses to prevent stress shielding and its complications, or to

reconstruct the segmental fibular defect decreasing donor site morbidity after harvesting a vascular

fibular autograft. Sufficient primary fixation at the bone-implant interface remains a challenge,

which could be achieved by using tubular FRC implants in combination with FRC intramedullary

nails for instance. Osseoincorporation is essential for long term survival of an implant and bioactive

glass granules could be used in the composite to enhance bone ongrowth on implant surfaces.

Thermoset polymer matrix such as Bis-GMA-TEGDMA allows fabrication of sophisticated FRC

structures as well as altering fiber composition and orientation in different parts of an implant using.
Femora and other load-bearing bones are also subjected to axial compressive forces and the lack

of torsion-compression test is a limitation in this study (Edwards et al. 2008). Compression tests

would be performed more practically alongside with the mechanical tests on the bone-implant

interfaces of a more developed implant with finished ends. The hand lay-up technique of the pre-

impregnated glass fibers is not suitable for implants used in clinic. Robot-assisted single fiber

braiding technique could be a solution for this implant fabrication challenge. Using both E- and S-

glass made estimating the vol-% of glass fibers in the composite difficult since micro-CT imaging

didn´t provide sufficient resolution for the fibers. In torsion testing the span used for FRC bone

models was 50 mm in contrast to 70 mm for rabbit femora because 50 mm was the maximal span

for FRC bone models for a sufficient fixation in the testing machine with PMMA embedding. The

torsion test results of rabbit femora could differ slightly if a span of 50 mm was used.

In conclusion, glass fiber-reinforced composites have great potential as future materials in

reconstruction of bone defects due to their cortical bone matching elastic properties and good

biocompatibility. From a biomechanical perspective they could be used even in load bearing

conditions such as reconstruction of segmental diaphyseal defects. Development of an implant

applicable for clinical use requires further studies.

Conflict of interest

Kalle Dahl has no financial disclosures. Niko Moritz is a shareholder in TraceRay Oy, a privately

owned company specializing in veterinary implant solutions. Pekka Vallittu consults Stick Tech Ltd

– GC Group in RD and training for dental resin composites and is a share holder and board

member of Skulle Implants Corporation.

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Highlights

 Glass fiber-reinforced composites have elastic properties matching those of bone

 Obliquely oriented fibers strengthened fiber-reinforced composite tubes
 A composite bone model was stronger than cadaver bone in mechanical tests
 The bone model has potential in reconstruction of segmental bone defects