Journal of the Mechanical Behavior of Biomedical Materials 70 (2017) 1–6

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Journal of the Mechanical Behavior of Biomedical

Materials
journal homepage: www.elsevier.com/locate/jmbbm

Mechanics of additively manufactured biomaterials

art ic l e i nf o a b s t r a c t

Keywords: Additive manufacturing (3D printing) has found many applications in healthcare including fabrication of
Biomaterials biomaterials as well as bioprinting of tissues and organs. Additively manufactured (AM) biomaterials
Mechanical performance may possess arbitrarily complex micro-architectures that give rise to novel mechanical, physical, and
Shape-property relationship biological properties. The mechanical behavior of such porous biomaterials including their quasi-static
Additive manufacturing mechanical properties and fatigue resistance is not yet well understood. It is particularly important to
understand the relationship between the designed micro-architecture (topology) and the resulting
mechanical properties. The current special issue is dedicated to understanding the mechanical behavior
of AM biomaterials. Although various types of AM biomaterials are represented in the special issue, the
primary focus is on AM porous metallic biomaterials. As a prelude to this special issue, this editorial
reviews some of the latest findings in the mechanical behavior of AM porous metallic biomaterials so as
to describe the current state-of-the-art and set the stage for the other studies appearing in the issue.
Some areas that are important for future research are also briefly mentioned.
& 2017 Elsevier Ltd. All rights reserved.

1. Introduction the design of AM biomaterials including the different micro-ar-

chitectural designs (Fig. 2) and the different spatial distributions of
Additive manufacturing (AM) has emerged as a powerful multiple biomaterials on the one hand and the resulting properties
technique for fabrication of biomaterials, tissues, and organs on the other have received much attention recently.
(Zadpoor and Malda, 2017). The free-form nature of AM offers The mechanical properties of AM materials are among the most
several possibilities for design and manufacturing of biomaterials important properties of AM biomaterials that could be adjusted
and medical devices. For example, medical devices can be de- through the above-mentioned approaches. Last few years have
signed and fabricated to exactly match the anatomy of the pa- seen a rapid growth of studies that address the problem of design-
tients. Moreover, AM makes it possible to develop medical devices property relationships specifically for the quasi-static (Fig. 2a) and
with complex shapes and multiple materials that cannot be easily fatigue resistance of biomaterials (Fig. 2b). The current special is-
manufactured using conventional techniques. sue presents a number of such studies on the mechanical behavior
Most importantly, however, AM adds a new chapter to several of AM biomaterials. As a prelude to the issue, this editorial sket-
decades of effort in development of biomaterials with specific me- ches the current research landscape on the mechanical behavior of
chanical, physical, or biological properties. The focus of most bio- AM biomaterials and summarizes some of the most important
materials research in the previous decades has been development of findings reported in this special issue as well as in a number of
new materials such as new polymers, metallic alloys, or ceramics other studies. Even though different types of biomaterials have
that present novel properties, which are beneficial for their intended been covered in the special issue (see e.g. Bootsma et al. (2017)
biological function. A powerful consequence of the free-form nature and Zhou et al. (2017)), the emphasis is on AM porous metallic
of AM is that it enables obtaining completely new set of properties biomaterials (see e.g. Speirs et al. (2017) and Van Hooreweder
using the currently available biomaterials and simply through a so- et al. (2017)). The editorial will therefore focus primarily on such
called ‘designer biomaterials’ approach. In this approach, the prop- materials.
erties of the biomaterial are, in addition to the properties of the bulk The mechanical behavior of AM porous metallic biomaterials
materials that are they made of, originating from the design of their has been systematically studied during the last few years. Porous
micro-architecture and spatial arrangement of multiple biomater- biomaterials based on titanium and its alloys (Cheng et al., 2014;
ials. This has close connections with the concept of meta-materials Heinl et al., 2008; Parthasarathy et al., 2010) have received the
(Florijn et al., 2014; Lee et al., 2012; Shalaev, 2007; Smith et al., 2004; most attention, while other types of porous metallic biomaterials
Zheng et al., 2014) where the physical properties of materials are based on cobalt chromium (Hedberg et al., 2014; Xiang et al., 2012;
originating from the ultrastructure of the material (Fig. 1). Xin et al., 2013), tantalum (Wauthle et al., 2015), and stainless steel
Given the possibility of obtaining novel properties through (Hao et al., 2009; Lin et al., 2007) have been studied as well. The
such a ‘designer biomaterial’ approach, the relationship between bio-inert nature of such metallic biomaterials together with the

http://dx.doi.org/10.1016/j.jmbbm.2017.03.018
1751-6161/& 2017 Elsevier Ltd. All rights reserved.
2 A.A. Zadpoor / Journal of the Mechanical Behavior of Biomedical Materials 70 (2017) 1–6

Wieding et al., 2012) techniques. In general, there is a power law

relationship between the relative density (porosity) of AM porous
biomaterials and their elastic modulus and yield stress (Zadpoor and
Hedayati, 2016) (Fig. 3a-b). However, the coefficients of the power
law relationship are very different from one unit cell to another such
that very different mechanical properties could be obtained for the
same porosity simply by changing the type of unit cell (Fig. 3a-b).
This allows for freedom in the design of porous biomaterials where
competing requirements such as appropriate mass transport prop-
erties (Van Bael et al., 2012) and pore size/shape should be balanced
with the required mechanical properties (Zadpoor, 2015).
Even when strong metallic alloys have been used for fabrication
of AM porous biomaterials, it has been possible to achieve quasi-
static mechanical properties comparable to those of trabecular and
cortical bone (Ahmadi et al., 2015; Cheng et al., 2012). The fact that
Fig. 1. An example of a penta-mode mechanical metamaterial manufactured using the homogenized mechanical properties of AM porous biomater-
selective laser melting at the Additive Manufacturing Laboratory, TU Delft (Medical ials with different unit cell types match those of bone allows for
Delta © de Beeldredacteur). avoiding stress shielding and stimulating bone regeneration when
designing orthopedic implants and bone tissue engineering scaf-
relatively simple mechanical behavior of metallic materials (e.g. folds. The effects of mechanical properties of AM porous bioma-
absence of strong viscoelastic behavior) creates the perfect setting terials on bone tissue regeneration have been studied in a few
to study the relationship between the topology and properties of studies in which in vivo animal models are used (Schouman et al.,
AM porous metallic biomaterials including both quasi-static me- 2016; Van der Stok et al., 2013). It has been found that the lower
chanical properties and fatigue resistance. The biomaterials used mechanical properties of AM porous biomaterials as compared to
for such studies are generally fabricated using powder bed fusion corresponding solid implants result in improved bone tissue re-
technologies including selective laser melting (Fukuda et al., 2011; generation performance of biomaterials (Schouman et al., 2016).
Pattanayak et al., 2011; Vandenbroucke and Kruth, 2007) and Another study that compared the bone tissue regeneration per-
electron beam melting (Hrabe et al., 2011; Murr et al., 2011; Po- formance of two different types of AM porous metallic biomater-
nader et al., 2008). ials with different mechanical properties did not show sig-
nificantly different bone tissue regeneration performance between
both porous biomaterials, although some qualitative signs of im-
2. Mechanical properties proved bone tissue regeneration performance were found for the
AM porous biomaterial with lower mechanical properties (Van der
The quasi-static mechanical properties of AM bulk biomaterials as Stok et al., 2013).
well as AM porous biomaterials have been extensively studied during As bone tissue grows into the porous structure of AM bioma-
the last few years using analytical (Zadpoor and Hedayati, 2016), terials, the mechanical properties of bone-tissue complex may
computational (Lin et al., 2007; Barbas et al., 2012; Wieding et al., significantly change. The effects of de novo bone tissue ingrowth
2014), and experimental (Ahmadi et al., 2015; Murr et al., 2010; on the quasi-static mechanical properties of AM porous metallic

Fig. 2. Specimens with different types of micro-architectures used for quasi-static mechanical testing (similar to the ones used in Ahmadi et al. (2015)) (a), fatigue crack
growth specimen made with selective laser melting from Ti-6Al-4V (b).
 A.A. Zadpoor / Journal of the Mechanical Behavior of Biomedical Materials 70 (2017) 1–6 3

In addition to mechanical properties, the failure mechanism of

AM porous biomaterials under quasi-static mechanical testing is
dependent on the type of unit cell. Some general guidelines have
been suggested in a few studies that distinguish the unit cells in
which stretching is the dominant loading mode from bending-
dominate unit cells (Kadkhodapour et al., 2015). Whereas shear
band formation at 45° angle has been found to be the typical
failure mechanism of bending-dominated unit cells, layer-by-layer
failure characterizes the failure mechanism of stretch-dominated
unit cells (Kadkhodapour et al., 2015).
Many computational and analytical studies of the quasi-static
mechanical behavior consider the unit cell geometry of the actual
AM porous biomaterial to perfectly match the designed geometry of
the unit cell. In practice, however, substantial deviations from the
designed unit cell geometry might exist in the actual morphology of
AM micro-architecture (Bagheri et al., 2017; Campoli et al., 2013). The
effects of the imperfections caused by the AM process on the quasi-
static mechanical behavior of AM porous biomaterials with different
types of unit cells were studied using stochastic finite element (FE)
models (Campoli et al., 2013). The study found that the weak spots in
the geometry of AM porous structure generally result in significantly
reduced quasi-static mechanical properties as compared to what is
predicted by analytical and computational models (Campoli et al.,
2013). It is important to realize that the imperfections in the geo-
metry of the AM porous structure as well as the quality of the struts
(as characterized by the continuity of the bulk material from which
the struts are made) are dependent not only on the parameters of
the AM process (Sallica-Leva et al., 2013) but also on the orientation
of the struts with respect to the powder bed (in powder bed fusion
AM processes) (Wauthle et al., 2015). Similar type of dependency on
the build orientation was found for the fatigue behavior of AM por-
ous biomaterials (Kajima et al., 2016). In general, horizontal struts are
found to be the most difficult ones to additively manufacture with-
out any defects (Wauthle et al., 2015) possibly due to the complex
heat transfer process in the powder bed. Heat treatment may be
needed as a post-processing step after fabrication of AM porous
biomaterials to either release residual stresses or to improve the
microstructure and, thus, the mechanical properties of the resulting
biomaterials. It has been, for example, shown that the relatively
brittle behavior of selective laser melted Ti–6Al–4V porous bioma-
terials resulting from “acicular α’ martensitic microstructure” could
be remedied through post-manufacturing heat treatments that
transform the microstructure of the biomaterial to a “fine α þ β mi-
crostructure” (Sallica-Leva et al., 2016). Heat treatments have been
Fig. 3. The range of normalized elastic modulus (a) and yield stress (b) vs. relative
density determined for porous structures with different types of repeating unit also shown to influence the fatigue resistance of AM porous bio-
cells (Zadpoor and Hedayati, 2016) as well as the normalized S-N curves obtained materials (and not necessarily positively) (Lipinski et al., 2013).
for a few types of unit cells (Amin Yavari et al., 2015). Chemical and electrochemical surface treatments are often
applied either to remove the remaining (loose) powder from AM
porous biomaterials or to induce bio-functionalities such as im-
biomaterials with different porosities were recently studied using
proved bone tissue regeneration performance. Since most of such
polymeric fillers with elastic moduli in the range of 0.7 and 1.5 GPa
surface treatments are associated with certain levels of mass loss
(Hedayati et al., 2016). The quasi-static mechanical properties of
and strut thinning, it is important to understand how the me-
fully-filled AM porous biomaterials were found to increase 2–7
times (Hedayati et al., 2016). This is the upper limit of stiffness chanical properties of AM porous biomaterials are affected as a
increase, given the assumption that the entire pore space is filled result of such treatments. One study that compared the effects of
with newly formed tissue. In addition, the relative increase in two different types of bio-functionalizing chemical surface treat-
mechanical properties was generally much higher for more porous ments on the mechanical behavior of AM porous titanium found
structures presumably due to the more pronounced effects of that the effects of surface treatment are very much dependent on
manufacturing weak spots in more porous structures that could be the severity of the treatment (Amin Yavari et al., 2014). While no
remedied by addition of a second supporting material (Hedayati notable difference in the mechanical properties was found for one
et al., 2016). The fatigue behavior of the bone-tissue complex in type of treatment, the other type significantly reduced the quasi-
terms of the number of cycles that it can tolerate before fatigue static mechanical properties of AM porous titanium (Amin Yavari
failure was also notably influenced by tissue ingrowth perhaps et al., 2014). Similar results were found for the effect of the same
even more than the quasi-static mechanical properties (Hedayati surface treatments on the fatigue resistance of AM porous bio-
et al., 2016). materials (Amin Yavari et al., 2014).
4 A.A. Zadpoor / Journal of the Mechanical Behavior of Biomedical Materials 70 (2017) 1–6

3. Fatigue behavior of their yield stress (Amin Yavari et al., 2015). This basically means
that AM porous biomaterials based on the cubic unit cell probably
AM porous biomaterials particularly the ones used for treat- do not experience fatigue failure under compression-compression
ment of load-bearing bony defects or as parts of load-bearing or- loading. On the other hand, the other types of unit cells show
thopedic implants will experience may loading cycles during their significantly different S-N curves depending on their geometry
service life. A study puts the estimate on around 2 million cycles of (Amin Yavari et al., 2015) (Fig. 3c), meaning that the normalized
loading as a consequence of patient walking (Silva et al., 2002). It S-N curve has to be determined at least for one porosity from each
is therefore important to study the fatigue behavior of AM bio- type of unit cell. Given the high cost associated with experimental
materials in general and AM porous biomaterials in particular. determination of the S-N curve for every new type of unit cell
Bone is primarily loaded in compression. Bone-substituting geometry, computational techniques could be of much value. A
biomaterials and orthopedic implants are also chiefly loaded in recent study has shown that it is, indeed, possible to predict the
compression. The most relevant mode of loading to study the fa- S-N curves of AM porous biomaterials using computational tech-
tigue behavior of bone-substituting materials and orthopedic im- niques and damage mechanics (Hedayati et al., 2016).
plants is therefore compression. Pure compressive loading does The endurance limit of a material is defined as the stress level for
not usually result in fatigue failure in most continuous materials, which the fatigue life of the material is indefinite for all practically
because compressive loads have some sort of crack-closure effect relevant purposes. Since indefinite fatigue testing is not possible in
that suppresses crack growth and, thus, prevents fatigue failure practice, a threshold, e.g. one million or ten million cycles, is used to
from happening. The above-mentioned crack-closure effect is, determine the endurance limit. The endurance limits of AM porous
nevertheless, not always present in AM porous biomaterial. Even biomaterials for compression-compression fatigue loading have been
when the porous biomaterials are subjected to fully compressive determined in a number of studies. A summary of some of the en-
fatigue loads at the macro-scale, tensile stresses may develop in durance limit values can be found in (Li et al., 2017). Endurance limits
the individual struts that make up the porous structure. The between 20% and 35% of the yield (plateau) stress are, however, not
amount and distribution of tensile stresses is dependent on the unusual (Amin Yavari et al., 2015; Amin Yavari et al., 2013; Li et al.,
type of unit cell, as some unit cell designs results in much more 2017). These are relatively low values of endurance limit, which
tensile stresses than others. suggest AM porous biomaterials need to be further optimized to
Although some studies of the fatigue behavior of AM porous achieve improved fatigue resistance. The relatively low fatigue re-
biomaterials have used tensile loading of the porous structures sistance of AM porous biomaterials has been attributed to various
(Lipinski et al., 2013), for the reasons mentioned above, many factors among which manufacturing imperfections that could act as
more studies have focused on the compression-compression fati- sites of stress concertation and crack initiation are the most
gue resistance of such materials (Hrabe et al., 2011; Amin Yavari notable (Amin Yavari et al., 2014; Amin Yavari et al., 2015; Amin
et al., 2015; Amin Yavari et al., 2013). When cyclically loaded under Yavari et al., 2013). A number of ways for improving the fatigue re-
compression, the curves depicting strain accumulation vs. cycle sistance of AM porous biomaterials have been also proposed (Van
number show a characteristic three-stage behavior (Amin Yavari Hooreweder et al., 2017).
et al., 2013). The increase in strain is relatively slow in the first two S-N curve is normally determined only for one (or a few)
stages, while the third stage is associated with a fast increase in loading condition(s) characterized by such parameters as the
strain that results in specimen failure (Amin Yavari et al., 2013). minimum and maximum stresses and loading frequency. The S-N
Compression-compression S-N curves have been established for curves of the material for any other loading condition is then ob-
AM porous biomaterials with different porosities and with differ- tained from the already determined S-N curves using certain
ent types of unit cells to study how the type and dimensions of (empirical) relationships such as the Goodman law. One important
repeating unit cells influence the S-N curve of AM porous bio- question about AM porous biomaterials is whether the empirical
materials (Amin Yavari et al., 2015; Amin Yavari et al., 2013). It has relationships derived for continuous materials also apply to this
been observed that for the same level of applied load, the number new type of materials. There has been very limited research in this
of loading cycles a porous structure can sustain before failure direction. One of the papers appearing in the current special issue
generally increases as the relative density increases (Amin Yavari studies the dependency of the S-N curve of AM porous bioma-
et al., 2015; Amin Yavari et al., 2013). This is expected, as less terials on the applied stress ratio (i.e. ratio of minimum and
porous structures are stronger and therefore capable of tolerating maximum stresses) and compares the relationship to that of
higher levels of absolute stress without plastic or fatigue failure. continuous materials (De Krijger et al., 2017). The study finds the
Somewhat more interesting results could be obtained when the relationship to be both qualitatively and quantitatively different
absolute S-N curves are normalized with respect to the yield or from that of continuous materials (De Krijger et al., 2017), meaning
plateau stress of the porous structures to obtain the so-called that new empirical relationships need to be established for AM
normalized S-N curves. A number of studies have shown that, for porous biomaterials. The study cites the highly notched micro-
the same type of repeating unit cells, the normalized S-N curves of architecture of the AM porous biomaterials as a probable cause of
AM porous biomaterials with different porosities are very similar such a different behavior (De Krijger et al., 2017).
and practically indistinguishable (Amin Yavari et al., 2015; Amin
Yavari et al., 2013). This is an important finding, because it allows
for limiting the tedious, time-consuming, and expensive job of 4. Discussion and future directions
determining S-N curves to one single porosity (or a few porosities).
For any other porosity of the same AM porous biomaterial, one The results reviewed in the previous sections show that the de-
simply needs to perform quasi-static mechanical testing and use sign freedom offered by AM porous biomaterials could be used to
the obtained yield (plateau) stress to convert the normalized S-N achieve very different mechanical properties simply by changing the
curve obtained using other porosities back to an absolute S-N geometry and dimensions of the repeating unit cells that make up
curve for the specific porosity at hand. The normalized S-N curve, the micro-architecture of the materials. This is also related to the
however, has been shown to be dependent on the type of unit cell emerging concept of mechanical meta-materials where materials
(Fig. 3c). For the cubic unit cell in which no tensile forces are in- with unusual, rare, or unprecedented mechanical properties can be
duced in the structure, the AM porous structures did not fail after manufactured through the rational design of the micro-architecture
more than one million cycles of loading at stress levels up to 80% (Zadpoor, 2016). In this context, a natural question to ask would be
 A.A. Zadpoor / Journal of the Mechanical Behavior of Biomedical Materials 70 (2017) 1–6 5

‘what are the micro-architectures that give rise to the best me- law is used to transform the S-N curve obtained for one loading
chanical properties for AM porous biomaterials?’ This is basically an condition to other types of loading conditions including other stress
inverse problem that needs to be solved using computational or ratios. Since recent research has shown the currently available em-
analytical tool such as topology optimization (Wang et al., 2016), pirical relationships do not necessarily hold for AM porous bioma-
assuming that one knows what the best mechanical properties for terials (De Krijger et al., 2017), a systematic study of how different
bone tissue regeneration and/or implant osseointegration are. AM parameters of the loading profile influence the S-N curve of AM
can take this one step further and allow for patient-specific dis- porous biomaterials is required. Based on the result of such type of
tribution of mechanical properties within the implant so as to opti- systematic studies, new empirical relationships may need to be de-
mize stress and strain distribution. A natural route to take would be veloped for the case of AM porous biomaterials. Finally, except for a
to run bone tissue adaptation algorithms that predict the most few studies that use shell-based micro-architectures (e.g. structures
sensible distribution of mechanical properties for the local loading based on triply periodic minimal surfaces (Kadkhodapour et al.,
conditions experienced by the implant in the body of a particular 2017; Yan et al., 2015)), the vast majority of studies on the fatigue
patient. The local loading condition are, of course, dependent not behavior of AM porous biomaterials have been focused on beam-
only on the anatomy of the patient but also on the musculoskeletal based micro-architectures (e.g. structures based on lattices and
loading conditions experienced by the patient during physical ac- space-filling polyhedral (Zadpoor and Hedayati, 2016)). More study
tivities. An additional layer of complexity is the fact that mechanical of the fatigue behavior of shell-based porous structures is therefore
properties are not the only properties important for bone tissue re- needed, because the structures based on continuous shells may be
generation and osseointegration. Physical properties such as per- less sensitive to the irregularities caused by the AM process and may
meability and other mass transport properties as well as the topol- therefore show higher levels of endurance limit.
ogy of the AM porous biomaterials may be also important for bone
tissue regeneration and implant fixation. One may therefore needs to
use multi-physics models for predicting the optimal distribution of 5. Conclusions
mechanical and physical properties within any particular implant.
Although limited research has so far been performed in the above- The current special issue presents studies reporting some of the
mentioned directions, utilizing the full potential of AM porous bio- latest developments in our pursuit of understating the mechanical
materials would not be possible without computational and/or behavior of AM biomaterials. Although papers covering the dif-
analytical tools that allow for the rational design of the micro-ar- ferent types of materials including polymeric materials appear in
chitectures of such biomaterials. the issue, the emphasis is on AM porous metallic biomaterials. To
Several other aspects of the mechanical behavior of AM porous sketch the research landscape and lay the ground for the papers
biomaterials have not been sufficiently explored in the past and need appearing in this special issue, this editorial briefly reviewed the
more attention. In particular, there has been limited systematic re- most important aspects in the study of the mechanical behavior of
search on the mechanical behavior of non-metallic AM porous bio- AM porous metallic biomaterials covering both quasi-static and
materials. Although numerous studies have characterized some as- fatigue behavior of such biomaterials.
pects of the mechanical behavior of polymeric and ceramic-based
biomaterials, there has been little systematic research to relate the
topology of non-metallic AM porous biomaterials to their quasi-static References
mechanical properties and fatigue behavior (i.e. S-N curves). It is also
not clear whether the results obtained for metals are directly ap-
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Amir A. Zadpoor n
Behav. Biomed. Mater. 26, 98–108. Additive Manufacturing Laboratory, Department of Biomechanical
Sallica-Leva, E., Caram, R., Jardini, A., Fogagnolo, J., 2016. Ductility improvement due to Engineering, Delft University of Technology (TU Delft), Mekelweg 2,
martensite α′ decomposition in porous Ti–6Al–4V parts produced by selective
laser melting for orthopedic implants. J. Mech. Behav. Biomed. Mater. 54, 149–158.
Delft 2628 CD, The Netherlands
Schouman, T., Schmitt, M., Adam, C., Dubois, G., Rouch, P., 2016. Influence of the E-mail address: [email protected]
overall stiffness of a load-bearing porous titanium implant on bone ingrowth in
critical-size mandibular bone defects in sheep. J. Mech. Behav. Biomed. Mater.
59, 484–496.

n
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