ActaActa

Biomaterialia 99 (2019)
Biomaterialia 479–494
xxx (xxxx) xxx

Contents lists available at ScienceDirect

Acta Biomaterialia
journal homepage: www.elsevier.com/locate/actabiomat

Full length article

A manufacturing and annealing protocol to develop a cold-sprayed

Fe-316L stainless steel biodegradable stenting material
Jennifer Frattolin a, Ranjan Roy b, Sriraman Rajagopalan c, Michael Walsh d, Stephen Yue c,
Olivier F. Bertrand a,e, Rosaire Mongrain a,f,⇑
a
Department of Mechanical Engineering, McGill University, Macdonald Engineering Building, Montreal, Quebec H3A 0C3, Canada
b
Department of Chemical Engineering, McGill University, M.H. Wong Building, Montreal, Quebec H3A 0C5, Canada
c
Department of Mining and Materials Engineering, McGill University, M.H. Wong Building, Montreal, Quebec H3A 0C5, Canada
d
Biomaterials Cluster, Bernal Institute, School of Engineering, Health Research Institute, University of Limerick, Ireland
e
Interventional Cardiology Laboratories, Quebec Heart and Lung Institute, Laval University, Quebec City, Quebec G1V 4G5, Canada
f
Montreal Heart Institute, Montreal, Quebec H1T 1C8, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Biodegradable stents show promise to revolutionize coronary artery disease treatment. Its successful
Received 23 March 2019 implementation in the global market remains limited due to the constraints of current generation
Received in revised form 20 August 2019 biodegradable materials. Cold gas dynamic spraying (CGDS) has been proposed as a manufacturing
Accepted 21 August 2019
approach to fabricate a metallic biodegradable amalgamate for stent application. Iron and 316L stainless
Available online 23 August 2019
xxxx
steel powders are combined in a 4:1 ratio to create a novel biomaterial through cold spray. Cold spray
processing however, produces a coating in a work hardened state, with limited ductility, which is a crit-
Keywords:
ical mechanical property in stent design. To this end, the influence of annealing temperature on the
Biodegradable stent
Cold spray
mechanical and corrosion performances of the proposed Fe-316L amalgamate is investigated. It was
Bioresorbable scaffold found that annealing at 1300 C yielded a complex material microstructure, with an ultimate tensile
Biomaterials strength of approximately 280 MPa and ductility of 23%. The static corrosion rate determined at this
Coronary artery disease annealing temperature was equal to 0.22 mg cm2 day1, with multiple corrosion species identified
within the degradation layers. Precipitates were observed throughout the microstructure, which
appeared to accelerate the overall corrosion behaviour. It was shown that cold-sprayed Fe-316L has sig-
nificant potential to be implemented in a clinical setting.

Statement of Significance

Biodegradable stents have potential to significantly improve treatment of coronary artery disease by
decreasing or potentially eliminating late-term complications, including stent fracture and in-stent
restenosis. Current generation polymer biodegradable stents have led to poorer patient outcomes in com-
parison to drug-eluting stents, however, and it is evident that metallic biomaterials are required, which
have increased strength. To this end, a novel iron and stainless steel 316L biomaterial is proposed, fabri-
cated through cold-gas dynamic spraying. This study analyses the effect of annealing on the Fe-316L bio-
material through corrosion, mechanical, and microstructural investigations. The quantitative data
presented in this work suggests that Fe-316L, in its annealed condition, has the mechanical and corrosion
properties necessary for biodegradable stent application.
 2019 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

1. Introduction conventional thermal powder deposition methods. Cold spray

Cold-gas dynamic spraying (CGDS) has emerged as an
alternative powder processing technique to other more
⇑ Corresponding author at: Macdonald Engineering Building, 817 Sherbrooke St.
West, Room 270, Montreal, QC H3A 0C3, Canada.
E-mail address: rosaire.mongrain@mcgill.ca (R. Mongrain).
allows for the deposition of pure metals, metallic alloys, and com-
posite powders, creating a wide range of possible materials with
varied properties. It is a high-pressure powder processing tech-
nique, utilizing compressed gas (nitrogen or helium) at a pressure
of 1–5 MPa. The high-pressure gas is heated to 100–800 C and
travels to the gun nozzle, where it is mixed with the powder
carried by the gas jet stream from the powder feeder [1]. A

https://doi.org/10.1016/j.actbio.2019.08.034
1742-7061/ 2019 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
480
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converging/diverging nozzle is implemented to generate gas flow
with high velocities, propelling the powder particles from 300 to
1200 m s1. Since the powder impacts the substrate at a high
velocity, the particles deform, adhere to the substrate and form a
coating [2]. The temperature of the powder remains low (below
typical solid-state powder sintering temperatures), and effects nor-
mally associated with high temperature powder processing tech-
niques, such as casting or sintering, including oxidation, thermal
stresses, and grain growth, are avoided. This is advantageous for
biomaterial applications as oxygen-sensitive powders can be
sprayed. Furthermore, no melting is observed, and the particles
are able to yield and mix under very high strain rates, producing
a complex microstructure [1]. The resulting microstructure has
grain sizes in the micron to submicron range, resulting in high
strength, as well as improved fatigue resistance and wear proper-
ties [3].
The application of cold spray to the development of biomateri-
als is an interesting alternative for the fabrication of coronary
stents, a scaffolding device used to treat coronary artery disease.
Traditional manufacturing techniques, such as casting or sintering,
utilize elevated temperatures to form the materials, operating
above the transformation temperature of the material. This is
avoided in cold spray due to its low operating temperature. In
addition, the refined microstructure obtained through cold spray
would allow for a thinner stent strut profile, without sacrificing
the scaffolding performance of the stent. This is of considerable
importance since strut thickness is an independent predictor of
restenosis risk [4]. Cold spray has already been demonstrated as
a potential fabrication technique for permanent stents through
the work of Al-Mangour et al. [5].
The application of CGDS to biodegradable stent fabrication may
help address some of the deficiencies of current generation
biodegradable stents. Biodegradable stents provide temporary
scaffolding support to prevent acute recoil post-implantation but
degrade fully to avoid late-term complications like late stent
thrombosis and stent fracture. The potential advantages of
biodegradable stents over traditional drug-eluting stents include
decreased incidence or potential elimination of in-stent restenosis
and stent fracture, restoration of more native tissue behaviour,
including cyclic strain and vessel pulsatility, as well as physiolog-
ical shear stress, among other benefits [6–9]. Polymers were the
material of choice for biodegradable stent application, due to their
known bioresorbable properties in clinical applications, such as
biodegradable sutures. However, polymer stents pose a significant
number of challenges. The comparatively poor mechanical proper-
ties of polymer stents have required thicker and wider struts than
traditional DES to increase scaffolding strength and stiffness. This
leads to reduced deliverability due to a larger catheter profile, in
addition to established precision constraints due to the poor radio-
graphic visualization of polymers [10,11]. The reduced stiffness of
polymer stents also results in greater scaffold recoil in complex
lesions. From a clinical perspective, there are several factors
revealed by the recent clinical trials of polymer stents that are con-
cerning, including the relatively high target lesion failure, the pres-
ence of late-stent thrombosis, and poor outcomes in smaller calibre
and tortuous vessels [12,13]. Furthermore, due to the poor
mechanical properties of polymer stents, attaining firm strut appo-
sition against the vessel wall is problematic. This has resulted in a
phenomenon referred to as intraluminal scaffold dismantling,
where stent struts protrude into the arterial lumen as they
degrade. This is of significant clinical concern as the protruding
struts are highly thrombogenic, increasing the risk of late scaffold
thrombosis [14].
These limitations may be resolved with the implementation of
biodegradable metallic materials. Currently, the only metallic
biodegradable stent approved for clinical use is BioTronik’s Mag-
Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
Biomaterialia (2019) 479–494
(xxxx) xxx
maris stent, though it has been recently associated with rapid
degradation, resulting in poor stent scaffolding [15]. The use of
cold spray presents an alternative means to fabricate metallic
biodegradable stents. Cold spray allows for the deposition of reac-
tive powders without oxidation, resulting in a biodegradable coat-
ing. Multiple metallic powders can be sprayed to create an
intermixed metal–metal composite with a controlled corrosion
rate, by modifying the relative weight percentages of the powders.
In addition, by utilizing dissimilar metals with a large electropo-
tential gap, galvanic corrosion can be used to further accelerate
the corrosion behaviour of the material. One of the remaining chal-
lenges associated with CGDS is the work-hardened coatings. Since
cold spray is a deformation-based technique, the available defor-
mation existing within the metallic particles is used during depo-
sition. Furthermore, the particle–particle interface is weak, where
particles are largely only mechanically interlocked. This results in
overall poor ductility, with brittle fracture commonly occurring
[16]. Ductility is a critical property in stent application, in order
to facilitate stent expansion and resist deformation under heart
pulsation.
Frattolin et al. [17] previously studied the effect of different
powder mixtures of iron and 316L stainless steel on the corrosion
and mechanical properties, including 20% Fe and 80% 316L, 50% Fe
and 50% 316L, and 80% Fe and 20% 316L. It was evident from this
study that the combination of 80% Fe and 20% 316L had the most
suitable degradation properties of the different mixtures. However,
the particle interfaces were weakly bonded, and the overall mate-
rial ductility was insufficient for stent application. Therefore, the
objective of this work was to develop a manufacturing and anneal-
ing protocol that would improve the ductility of the cold-sprayed
Fe-316L material, validating its potential for biodegradable stent
application.
2. Materials and methods
2.1. Cold-gas dynamic spraying and sample fabrication
Commercially available iron and 316L stainless steel powders
were utilized for cold spray. Pure iron powder (ATOMET 195SP
classification) was obtained from Quebec Metal Powders (Sorel,
Canada) and 316L stainless steel powder was purchased from
SandVik Osprey (Neath, United Kingdom). The iron and 316L stain-
less steel powders were characterized using multiple techniques.
First, X-ray diffraction (XRD), coupled with quantitative phase
analysis, was used to confirm the composition of the powders. Sec-
ond, inductively coupled plasma optical emission spectrometry
(ICP-OES) was utilized to determine the element composition of
the powders. Third, to examine the morphology of the powder, a
scanning electron microscope (SEM) was used to image the pow-
ders at 2000 magnification. Lastly, the particle size and distribu-
tion were measured with a LA-920 laser diffraction analyzer
(HORIBA Scientific, France).
The powders were prepared in a 4:1 ratio, by weight, of iron to
316L stainless steel. To ensure a homogeneous particle distribu-
tion, the powders were then mixed utilizing a rolling mixer, with
2 mill balls, for 1 h. The Plasma Giken PCS-800 cold spray system
(Plasma Giken Co., Ltd., Japan) was used to fabricate flat samples of
Fe-316L. Prepared powder was preheated in a vacuum furnace as
humidity may affect coating adhesion to the substrate when spray-
ing [18]. Two 1018 carbon steel sheets, 15 cm in length and width
and approximately 0.6 cm thick, were utilized as substrates. Nitro-
gen (N2) was used as the propellant gas at a pressure of 4.0 MPa
and a temperature of 700 C. The substrates were grit-blasted prior
to spraying, as well as heated with 2 passes of nitrogen gas, to
improve powder deposition efficiency. The deposition efficiency,
DE, of the coating was determined utilizing the following equation:
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DE ¼ Dms =mp;total
where Dms, in grams, is the difference between the initial and final
mass of the substrate and mp,total, in grams, is the total mass of the
sprayed particles, which is obtained directly from the CGDS system.
After cold spraying, the samples were cut into the dog-bone
tensile specimens, according to the dimensions outlined of the sub-
size sample in ASTM E8/E8M-16a [19], with a gauge length of
25 mm and a width of 6 mm. Electrical discharge machining
(EDM) was used to remove the steel substrate from the Fe-316L
coating.
The prepared samples were then vacuum annealed at 1100 C,
1200 C, or 1300 C. The vacuum annealing setup employed a Type
46100 high temperature furnace (Thermolyne Corporation, USA),
with the samples contained in an alumina tube insert. The furnace
temperature was increased at a rate of 250 C h-1 until the required
temperature was reached, after which it was held at temperature
for 2 h. Samples were then allowed to cool at a controlled rate to
room temperature. After annealing, all samples were subsequently
ground and polished to improve surface finish.
2.2. Coating characterization
The chemical composition and microstructure of the Fe-316L
amalgamates exposed to different annealing conditions were
assessed and subsequently compared to as-sprayed Fe-316L. Sam-
ples (10 mm � 10 mm) were ground with up to 1200 silicon car-
bide paper and subsequently polished with 3 mm and 1 mm
diamond paste, according to standard metallographic preparation
procedures. Prior to microscopic observation, samples were
cleaned in an ultrasonic bath with isopropanol for 10 min.
2.2.1. X-ray diffraction
Phase analysis was performed by XRD on a D8 DISCOVER X-ray
Diffractometer (Bruker Corporation, Madison, WI, USA), with a Co
Ka source. Scans were conducted at a voltage and current of
35 kV and 45 mA, respectively, with a 0.02 s�1 scan rate. The back-
ground noise was subtracted from the original scan directly within
the DIFFRAC.SUITE EVA software (Bruker Corporation, Billerica,
MA, USA). The quantitative composition of the detected austenite
and ferrite phases of each annealing condition was determined
by Rietveld refinement. In addition, the full width at half maximum
(FWHM) of the (1 1 0) peak was determined to assess peak broad-
ening, which was computed within the DIFFRAC.SUITE EVA
software.
2.2.2. Optical and scanning electron microscopy
Specimens were characterized by optical microscopy with a
Nikon Epiphot 200 microscope (Nikon Instruments Inc., Melvile,
NY, USA), with Clemex Vision software (Clemex Technologies
Inc., Longueuil, QC, Canada) at 200� magnification. The polished
samples were also observed utilizing a Hitachi SU3500 SEM (Hita-
chi, Ltd., Tokyo, Japan) at an accelerating voltage of 15 kV. The ele-
ment distribution of the samples was assessed by energy-
dispersive X-ray spectroscopy (EDS) utilizing AZtec software
(Oxford Instruments Ltd., Abingdon, United Kingdom) at 500�
magnification.
2.3. Mechanical testing
Uniaxial tensile tests were conducted on an MTS hydraulic test-
ing machine with an extensometer. Tensile tests were performed
with the prepared dog-bone specimens at room temperature
according to ASTM E8/E8M-16a, at a strain rate of 0.001 s�1 [19].
For each annealing condition, three specimens were tested. Sample
width and thickness were re-measured after testing to assess neck-
Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
/ Acta
/ ActaBiomaterialia 99xxx
Biomaterialia (2019) 479–494
(xxxx) xxx 481
3
ð1Þ ing. Engineering ultimate tensile strength (UTS), yield stress, and
elongation at fracture were determined. Yield stress was calculated
using the 0.2% offset method. After testing, the morphology of the
fractured surface was characterized using SEM.
2.4. Corrosion testing
Static and galvanic corrosion tests were implemented to quan-
tify the impact of annealing on the corrosion behaviour of Fe-316L.
Samples were 10 mm � 10 mm, with an approximate thickness of
1 mm. Prior to corrosion testing, samples were progressively
ground with 400, 600, 800, and 1200 grit SiC paper. First, baseline
static immersion tests were conducted to calculate the corrosion
rate of each sample, followed by galvanic corrosion tests to quan-
tify the impact of heat treatment on the galvanic corrosion reaction
between iron and 316L stainless steel. Both tests were completed
in triplicate.
2.4.1. Static corrosion testing
Static corrosion tests were conducted of each sample following
ASTM standard G31-12a [20]. Physiological test conditions were
implemented, with modified HyCloneTM Hanks’ Balanced Salt Solu-
tion (HBSS) (Fisher Scientific, Canada) used as the corrosive media,
which was changed every 24 h. Modified HBSS is used as its ionic
composition is similar to that of blood plasma [21]. The solution
was buffered with HEPES to maintain a physiological pH of 7.4.
The solution was held at physiological temperature of 37 C, by
means of an ISOTEMP 202 hot water bath (Fisher Scientific,
Canada). As outlined by ASTM G31-12a, the solution volume to
sample surface area ratio (V/S) was maintained between 20 and
40 mL cm�2. The test duration was 7 days, and the samples were
removed from the test bench every 24 h, cleaned and weighed.
The corrosion rate of each sample, CRstatic, in mg cm�2 day�1, was
then calculated according to the following equation [20]:
CRstatic ¼ W=At ð2Þ
where W is the total mass loss in mg, A is the surface area in cm2,
and t is the total exposure time in days.
2.4.2. Galvanic corrosion testing
Galvanic corrosion tests were conducted in compliance with
ASTM standard G71-81 (2014) [22]. To induce a galvanic couple,
a VersaStat3 potentiostat (Princeton Applied Research, TN, USA)
was utilized. The annealed and as-sprayed samples were used as
the working electrode, with the other electrode defined as pure
316L stainless steel, with a 1:1 surface area ratio implemented. A
saturated calomel electrode was used as the reference electrode.
Samples were immersed for 6 h at 37 C within a jacketed reaction
beaker with 700 mL of buffered modified HBSS. Samples were sus-
pended on wires and were exposed to agitation through magnetic
mixing. Galvanic current and potential were measured with
respect to time.
The galvanic corrosion rate (CRgalv), in mg cm�2 day�1, was cal-
culated by the following equation:
CRgalv ¼ W=At ð3Þ
where A is the surface area in cm2, t is the elapsed time in days, and
W is the mass loss, in mg, equal to:
W ¼ MIt=zF ð4Þ
where M is the molar mass of iron in mg mol�1, I is the stabilized
galvanic current in Ampere, t is the total time in seconds, z is ion
valence (z = 2), and F is Faraday’s constant, 96 485.34 C mol�1.
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2.5. Corrosion product characterization
The corrosion products were analyzed utilizing five different
techniques, four of which specifically analyzed the corrosion pro-
duct layer on the sample, including XRD, X-ray photoelectron spec-
troscopy (XPS), SEM, and EDS. The final characterization technique,
ICP-OES, analyzed the composition of the loosed corrosion prod-
ucts in the testing solution.
2.5.1. X-ray diffraction and scanning electron microscopy
X-ray diffraction was used to assess the composition of the cor-
rosion products, following a similar procedure outlined in Sec-
tion 2.2.1. SEM was used to assess the morphology of the
degradation product layer, and the element distribution of the cor-
rosion products on the specimen surface was evaluated through
EDS. Analysis was conducted at 100 magnification and at an
accelerating voltage of 20 kV.
2.5.2. X-ray photoelectron spectroscopy
X-ray photoelectron spectroscopy of the accumulated corrosion
products was performed using a ThermoScientific K-Alpha XPS. X-
ray photoelectron spectroscopy is a surface characterization tech-
nique, which allows for depth profiling through etching to under-
stand the degree of oxidation or change in structures, which is
not possible with XRD. First, survey spectra were recorded from 0
to 1400 eV, implementing an aluminum K-alpha source with a
beam width of 400 mm. High-resolution scans of O1s, Fe2p, C1s,
Cl2p, P2p, and Ca2p, were then performed. For all samples, the sur-
face was etched for 225 s to analyze the corrosion products in
depth with an argon ion gun at an emission angle of 30. The ref-
erence binding energies used for identification are presented in
Table 1.
2.5.3. Inductively coupled plasma optical emission spectrometry
The testing solution from the static corrosion tests was col-
lected every 24 h for the duration of the 7-day test. To prepare
the solution for testing, each 100-mL sample was split into two
50-mL tubes and weighed. Each sample was centrifuged for one
hour at 1000 RPM and 25 C. The supernatant was removed, and
any remaining solution was evaporated at 65 C prior to re-
weighing. Nitric acid (5 mL) was added to each sample, followed
by a digestion period of 4 h at 95 C. After digestion, all samples
were completed to volume with deionized water and re-weighed.
A total of 14 samples were tested, two samples per day, for each
annealing condition. Testing standards for transitional metals (Fe,
Ni, and Cr) were made at concentrations of 100, 10, and 1 mg L-1.
The average element percentage, per day, was determined (n = 2).
Table 1
Reference binding energies in eV for Fe2p, O1s, C1s, P2p, Cl2p, and Ca2p.
Element Compound Binding Energy
Fe2p Fe3O4 710.6
724
O1s Fe-O 530.2
Fe-OH/Fe-OOH/Fe-PO4 531.5–531.6
C1s Hydrocarbons 284.6/284.8
C-O bonds 286.6
288.3
P2p Ca3(PO4)2 133.6
Cl2p FeCl2 201.0
199.3
Ca2p Ca3(PO4)2 347.8–347.9
350.6
Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
al.al.
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2.6. Statistical analysis
Mean values were determined for relevant data sets. Statistical
analysis was completed in GraphPad Prism 7.04 (GraphPad Soft-
ware Inc., La Jolla, CA, USA). A one-way ANOVA was used to com-
pare data sets. Tukey’s multiple comparisons test was selected as
a post-hoc test, with all possible pairwise combinations tested. A
p-value of < 0.05 was considered significant for both tests.
3. Results
3.1. Cold-gas dynamic spraying and sample fabrication
The iron and 316L stainless steel powders were characterized
using SEM, laser diffraction particle size analysis, XRD, and ICP-
OES. The SEM micrographs obtained at 2000 magnification are
presented in Fig. 1a. The morphology of the iron powder was more
irregular in comparison to the 316L stainless steel powders spher-
ical morphology, which could influence cold sprayability. The par-
ticle size analysis indicated a dimension of 33 ± 23 mm for the iron
powder, with a dimension of 21 ± 14 mm for the 316L stainless steel
powder. The corresponding frequency percentage with respect to
diameter is presented in Fig. 1b for both powders. X-ray diffraction
confirmed the chemical composition and crystalline structure of
the powders (Fig. 1c), with a-Fe identified for the pure iron pow-
der, and a-Fe and c-Fe for the 316L stainless steel. Quantitative
phase analysis of the 316L powder indicated a relative phase per-
centage of 19.1% and 80.9% of ferrite and austenite, respectively.
It is presumed that the presence of ferrite in the 316L powder is
a result of strain-induced transformation during powder process-
ing. The element concentrations determined through ICP-OES are
presented in Tables 2 and 3 for iron and 316L stainless steel pow-
ders, respectively.
The deposition efficiency of the two cold-sprayed plates was
equal to 28.9 ± 0.2%. The reduced deposition efficiency was associ-
ated with particle bounce back, due to insufficient deformation. It
was hypothesized that this was a result of the crystalline structure
of pure iron, body-centred cubic (BCC), which has a lower particle
packing density than FCC and HCP materials (0.68 vs 0.74). In addi-
tion, the irregular morphology of the powder particles could
impact deformation kinetics as irregular powders have been
reported to yield less dense coatings with greater porosity [30].
The resulting cold-sprayed coatings were 2.5 mm thick. The dog-
bone subsize specimens were then machine cut and ground, with
an average sample thickness of 1.3 ± 0.2 mm.
3.2. Coating characterization
3.2.1. X-ray diffraction
X-ray diffraction was used to identify the annealed and as-
sprayed samples. As-sprayed Fe-316L was a mixture of a-Fe and
c-Fe. After annealing, the peaks of c-Fe were significantly reduced
in comparison to the as-sprayed Fe-316L and could not be confi-
dently differentiated from the noise of the signal (Fig. 2a). Quanti-
Reference
tative phase analysis indicated that the amount of austenite had
[23]
decreased significantly to trace amounts in comparison to the as-
[24] sprayed sample (Table 4). The decrease in austenite is a result of
[24] a transformation of austenite to ferrite, presumably due to nickel
[24] diffusion from 316L stainless steel to iron during annealing. Iron
[25] transforms to austenite above 900 C, which may have facilitated
[25]
[26,27]
nickel diffusion. Any austenite detected could be a result of incom-
[28] plete nickel diffusion (i.e. not at equilibrium), where local concen-
[28] trations give small amounts of austenite.
[26,27,29] The FWHM was determined for the annealed Fe-316L samples
and compared to the as-sprayed material, as shown in Fig. 2b.
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5

Fig. 1. Characterization of iron (top) and 316L stainless steel (bottom) powders with (a) SEM; (b) laser diffraction particle size analysis; and (c) XRD.

Table 2
Element concentrations of the iron powder determined through ICP-OES. Elements denoted with an (*) indicate that a concentrated solution was used for ICP testing (dilute
solutions were used for all non-marked elements).

Element Fe P* Ti* S* Pb* Total

Weight Percentage (%) 99.3 0.00966 0.693 0.00670 0.00391 100

Table 3
Element concentrations of the 316L powder determined through ICP-OES. Elements denoted with an (*) indicate that a concentrated solution was used for ICP testing (dilute
solutions were used for all non-marked elements).

Element Fe Cr Ni Mo Mn Si* P* S* Total

Weight Percentage (%) 67.4 16.7 12.5 2.44 0.550 0.370 0.0277 0.00641 100

The FWHM is typically sensitive to variation in microstructure,
such as grain refinement, as well as residual stress and plastic
deformation within the material [31,32]. Peak broadening, and
therefore an increase in FWHM, can be attributed to an accumula-
tion of stacking faults and structural disorders, as well as increased
stress. Overall, there was a decrease in the FWHM of the (1 1 0)
peak between the annealed and as-sprayed samples. This reduc-
tion is attributed to the release of internal stress within the
microstructure and recrystallization during annealing. An increase
in annealing temperature resulted in a decrease in FWHM, though
the FWHM did not change significantly between 1200 C and
1300 C. Moravej et al. [33] observed a similar relationship
between annealing temperature and FWHM for electroformed iron,
where an increase in the former resulted in a decrease of the latter.
3.2.2. Optical and scanning electron microscopy
The optical micrographs of annealed and as-sprayed Fe-316L
are presented in Fig. 3a. In the optical image of the as-sprayed
specimen, the darker matrix is composed of iron and the lighter
dispersed particles are 316L stainless steel. The most significant
observation of the annealed samples, in comparison to the as-
sprayed, is the absence of the lighter phase, i.e. the stainless-
steel particles. This confirms the XRD analysis that indicated a
transformation of austenitic stainless steel to ferritic low-alloyed
steel. In addition, a decrease in porosity was observed between
all annealed and as-sprayed samples. A scanning electron micro-
scope was utilized to further assess the transformation of 316L
stainless steel by EDS (Fig. 3b). Distinct particles of 316L stainless
steel can be observed within the iron matrix of the as-sprayed

Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
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sample, indicated by the bright areas of nickel and chromium. In

contrast, atomic diffusion is evident in all annealed samples and
confirms the transformation of the stainless steel observed in the
optical micrographs. The degree of diffusion across particle bound-
aries was not uniform for all annealed samples, however, and clus-
ters of chromium and nickel could still be observed when
annealing at 1100 C.
Precipitates were observed in the optical micrographs of the
annealed specimens. Formation of precipitates and intermetallic
phases are a result of sensitization, defined as long term exposure
at high temperatures; for 316L stainless steel, the sensitization
temperature range is between 600 and 950 C [34]. In 316L stain-
less steel, an intermetallic phase precipitates at grain boundaries,
where a chromium rich region develops, resulting in chromium
depletion surrounding the precipitate [35]. EDS images confirmed
the presence of a chromium rich precipitate within the annealed
samples, particularly for samples annealed at 1300 C.

3.3. Mechanical testing

Uniaxial tensile tests were conducted to assess the impact of

annealing temperature on the mechanical behaviour of cold-
sprayed Fe-316L. Engineering stress–strain curves were generated
for all annealed Fe-316L samples. A representative stress–strain
curve of a sample from each annealing condition is presented in
Fig. 5. As the annealing temperature increased, the allowable
deformation prior to fracture increased, and visible necking was
detected for samples annealed at higher temperatures, particularly
at 1300 C. The mechanical behaviour of the as-sprayed coupons
was brittle, with limited deformation occurring prior to failure.
One of the three as-sprayed samples tested failed during pre-load
and no data was recorded for this sample.
The fracture surfaces of the differently annealed samples were
analyzed under SEM at 2000 magnifications (Fig. 4b–e). Both
ductile and brittle fracture (cleavage) were observed on the surface
of the heat-treated samples. Substantial microvoid coalescence
(MVC) were observed for all annealed samples, evident by the net-
work of spherical ‘‘dimples” in the microstructure. These micro-
voids are the mechanism of ductile fracture, which initiates crack
formation under loading. In contrast, the surface of the as-
sprayed sample indicated a complete brittle failure mode, with
no MVC observed.
Engineering UTS, elongation, and yield stress were determined
for each annealing condition; the mean values are presented in
Fig. 5 with standard deviation and relevant p-values. The engineer-
ing UTS was highest for the samples annealed at 1300 C (Fig. 5a).
Multiple comparisons testing showed that the tensile strengths of
the differently annealed specimens were all significantly different
from the as-sprayed condition, p = 0.0001 for samples annealed
at 1100 C and p < 0.0001 for samples annealed at 1200 C and
1300 C. Specimens annealed at 1300 C had the greatest elonga-
Fig. 2. (a) XRD patterns of the annealed and as-sprayed samples; (b) FWHM of the tion at fracture, with significant differences found between the dif-
(1 1 0) peak of the as-sprayed and annealed samples. ferently annealed specimens, as shown in Fig. 5b. In addition, the
elongation fractures determined for all annealed samples were sig-
nificantly higher than that of the as-sprayed, with p = 0.0011 for
samples annealed at 1100 C and p < 0.0001 for samples annealed
Table 4
Quantitative phase composition of ferrite and austenite in the annealed and as-
at 1200 C and 1300 C. One-way ANOVA tests found no significant
sprayed samples. difference between the yield strengths of the annealed samples
with p = 0.1314.
Sample Ferrite (%) Austenite (%)
Due to the deposition process of cold-spray, which yields work-
1100 C 99.8 0.2 hardened coatings and poor particle–particle bonds, limited ductil-
1200 C 99.9 0.1
ity was determined for the as-sprayed condition (0.047%). Low
1300 C 99.8 0.2
As-Sprayed 91.1 8.9 strength was observed for the as-sprayed tensile samples, due to
limited ductility (i.e. premature fracture), with a UTS of 84 MPa.

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Fig. 3. (a) Optical micrographs of representative polished annealed and as-sprayed specimens at 200 magnification; (b) Concentration of select elements by EDS of as-
sprayed and annealed samples at 1100 C, 1200 C, 1300 C.

The combination of low strength and low ductility was associated
with incomplete bonding at particle–particle interfaces, which was
confirmed by the as-sprayed optical and SEM images. Incomplete
particle bonding results in fracture at low forces, with limited
deformation. During the annealing process, recrystallization
occurs, which removes dislocations existing within the crystalline
structure, softening the material and improving ductility. More
importantly for a cold-sprayed material, annealing also improves
interparticle bonding through ‘sintering’, which is accompanied
by atom diffusion across particle boundaries (Fig. 3) [5,36].
Improved interparticle bonding results in greater tensile strength
despite increased material softening as ductility (i.e. fracture resis-
tance) is increased.
3.4. Corrosion testing
3.4.1. Static corrosion testing
The average static corrosion rate, CRaverage, was calculated in mg
cm2 day1. The relationship between corrosion rate and time is
presented in Fig. 6a with standard deviation. Elevated degradation
rates were observed during the first 24–48 h of immersion, due to
the exposure of the fresh sample surface to the testing solution. A

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Fig. 4. (a) Engineering stress–strain curves of representative annealed and as-sprayed specimens. The fracture surface at 2000 magnification using SEM for representative
samples annealed at (b) 1100 C; (c) 1200 C; (d) 1300 C; as well as (e) as-sprayed condition.

Fig. 5. The engineering UTS, elongation at fracture, and yield stress, with standard deviation, of the differently annealed samples (n = 3), as compared to the as-sprayed
condition (n = 2). A statistically significant increase in both UTS and ductility was observed after heat treatment at all temperatures. NS signifies a non-significant difference.

one-way ANOVA test found that the average corrosion rates of all
samples, after 7 days of immersion time, were significantly differ-
ent, p < 0.0001. Tukey’s multiple comparisons test indicated that
the corrosion rates of the annealed samples were all significantly
less from that of the as-sprayed sample. Similarly, the corrosion
rate of samples annealed at 1200 C and 1300 C were found to
be significantly different from that of specimens heat treated at
1100 C (p = 0.0393 and p = 0.0399, respectively). There was no sig-
nificant difference between samples annealed at 1200 C and
1300 C, p > 0.9999.
The highest corrosion rate observed was 0.22 mg cm2 day1
(0.10 mm year1), determined for samples annealed at 1200 C
and 1300 C. This corrosion rate is approximately 43% less than
that of the as-sprayed sample. This decrease in corrosion rate is
attributed to several factors. Increased porosity and poor interpar-
ticle bonding of the as-sprayed samples allowed for preferential
corrosion to occur at the particle boundaries and surface pores.
Choi et al. [37] observed similar behaviour when analysing
cold-sprayed ferrous alloy coatings degraded in 3.5% NaCl solution,
where corrosion products were first observed around interparticle
boundaries and micro-pores. In contrast, the sintering that
occurred at the particles boundaries of the annealed samples
would slow the rate of the corrosion reaction, due to decreased
corrosion initiation sites. This difference between the annealed
and as-sprayed samples was clearly observed when analyzing the
corroded surface under SEM (Fig. 6b-e). From a biodegradable stent
application perspective, the severe corrosion at the boundaries of
the as-sprayed specimen is problematic as it could lead to a severe
reduction of the radial strength and stiffness of the stent. This may
result in premature failure of the device before complete vessel
remodelling can occur [38]. Decreased corrosion around particle
boundaries of the annealed samples is advantageous in this regard.
3.4.2. Galvanic corrosion testing
The galvanic potential of the as-sprayed sample was measured
at approximately 700 mV, consistent to that of pure iron. In con-

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Fig. 6. (a) Average static corrosion rate versus time for the annealed and as-sprayed samples (n = 3); SEM images at 500 magnification of the corroded sample surfaces after
cleaning annealed at (b) 1100 C; (c) 1200 C; (d) 1300 C; and (e) as-sprayed specimens.
trast, the potential range of the annealed samples was between
550 and 600 mV, which is similar to that of mild steel on the
galvanic potential series chart [39]. This discrepancy between the
potentials of the heat treated and as-sprayed samples confirms a
material transformation due to Ni and Cr diffusion during anneal-
ing. Despite this, there was no discernable influence of heat treat-
ment on the determined galvanic corrosion rate (Table 5).
Statistical significance testing indicated that there was no signifi-
cant difference between the galvanic corrosion rates of the tested
samples (One-way ANOVA, p = 0.9856).
3.5. Corrosion product characterization
3.5.1. Scanning electron microscopy and X-ray diffraction
The corrosion products were analyzed with multiple character-
ization techniques, including XRD, SEM, EDS, XPS, and ICP-OES. The
accumulated corrosion products on the sample surface were pre-
served and dried. All samples were covered in an orange-brown
layer, which was prone to flaking and had poor surface adherence.
This is typically associated with the formation of ferrous
hydroxides/oxide-hydroxides [24]. The morphology of the layer
was analyzed with SEM at 3000 magnification (Fig. 7). The
mineral-like structure observed is similar to that observed by Her-
mawan et al. [40], when conducting corrosion tests of Fe-35Mn
specimens in modified HBSS. These agglomerates were found to
contain higher concentrations of calcium and phosphorus, which
was similarly observed when analysing the Fe-316L samples by
EDS. The EDS images illustrated the heterogeneous phenomena
occurring on the sample surface during corrosion. All samples were
densely covered in oxygen, with chlorine, sodium, phosphorus,
Table 5
Galvanic corrosion rates, in mg cm2 day1, determined for the annealed and as-
sprayed specimens.
Sample Galvanic Corrosion Rate (mg cm2 day1)
1100 C 2.14 ± 0.22
1200 C 2.17 ± 0.31
1300 C 2.16 ± 0.36
As-Sprayed 2.09 ± 0.16
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calcium, and sulfur all found in varying concentrations (refer to
Supplementary Figs. 1–4). Decreased iron density was observed
in highly concentrated areas of chlorine, indicative of an active cor-
rosion reaction occurring on the sample surface (pitting corrosion).
Overlapping areas of concentrated phosphorous and calcium were
observed in the EDS maps, which coincided with the agglomerate
structure on the corrosion sample surface. The concentration of
this layer was higher for the annealed samples than the as-
sprayed sample but was not homogeneous across the entire sur-
face. This could be attributed to the propensity of the as-sprayed
sample to actively corrode in the presence of chlorine, due to its
poor interparticle bonding and high porosity, which act as initia-
tion sites for chlorine attack.
The corrosion products on the sample surface were analyzed
using XRD. The resulting XRD patterns were plotted for represen-
tative samples (Fig. 8). The XRD patterns had low intensity counts,
which was attributed to the decreased thickness of the corrosion
product layer that was prone to flaking and poorly adherent to
the specimen surface. The predominant compound identified was
iron phosphate, which was observed for the heat treated and as-
sprayed specimens. In addition, iron oxide (Fe2O3) was detected
in samples annealed at 1200 C and 1300 C. The presence of
Fe2O3 in the 1300 C specimen was identified after depositing some
of the corrosion products onto carbon tape and reanalysing with
XRD. The identification of iron phosphates and iron oxides are con-
sistent to that reported by Tolouei et al. [24], which investigated
corrosion products of pure iron in different pseudo-physiological
solutions.
3.5.2. X-ray photoelectron spectroscopy
A survey spectral scan was completed for each annealing condi-
tion, which positively identified elements Fe, O, C, Cr, Na, Ca, Cl, P,
and K. As expected, many of these elements are associated with the
components of the testing solution, modified HBSS. The identifica-
tion of these elements was consistent with EDS mapping analysis
of the corrosion product layer. High-resolution scans of Fe2p,
O1s, C1s, Cl2p, Ca2p, and P2p were conducted of the surface and
after 225 s etching (Supplementary Figs. 5–8). Some minor shifting
was observed in the peak binding energies after etching, which
was anticipated as oxygen disappears in depth profile and the sur-
rounding atoms differ. Overall, good agreement was found
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Fig. 7. SEM micrograph at 3000 of the corrosion products of samples annealed at (a) 1100 C; (b) 1200 C; (c) 1300 C; as well as the (d) as-sprayed sample.

Fig. 8. X-ray diffraction pattern of corroded samples annealed at (a) 1100 C; (b) 1200 C; (c) 1300 C; as well as the (d) as-sprayed condition. The primary corrosion product
identified was iron phosphate, with iron oxides detected in two of the four samples analysed (specimens annealed at 1200 C and 1300 C).

between the selected reference binding energies and peak binding
energies determined for the samples, with some limited variation
occurring between different specimens.
Since the corrosion product layer was dried in air, surface
hydrocarbons and C-O compounds (carbon dioxide and glucose)
were observed for all samples on the surface, which were signifi-
cantly reduced after etching for 225 s, as shown in Table 6. In con-
trast, the intensity of all other analyzed elements increased after
etching, emphasizing the importance of depth analysis when iden-
tifying corrosion products. Analysis of the Fe2p spectra identified
the presence of Fe3O4 at the Fe2p3/2 and Fe2p1/2 peaks, though
the Fe2p3/2 peak is also associated with FeCl2 at a binding energy
of 710.6 eV according to Grosvenor et al. [28]. The O1s spectra anal-
ysis indicated the presence of both Fe-O and Fe-OH/Fe-OOH on the

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Table 6
The percent change in counts s1 on the sample surface and after etching for 225 s, as determined by high-resolution XPS, for the annealed and as-sprayed specimens. The raw
intensity data, in counts s1, is provided in parentheses, where the counts on the surface is listed first, followed by the counts after etching.
Element Reference Binding Energy (eV) 1100 C
Fe2p 710.6 37.2% (17890/24550)
724 27.3% (15823/20135)
O1s 530.2 9.7% (21216/23278)
531.6 14.2% (23605/26957)
C1s 284.4/284.6 40.5% (5797/3447)
286.6 26.1% (4495/3320)
288.3 15.4% (3273/2770)
Cl2p 199.3 22.2% (4922/6017)
201 20.2% (3712/4463)
P2p 133.6–133.6 18.0% (3502/4133)
Ca2p 347.8 – 63.4% (8009/13086)
350.6 – 40.1% (6322/8857)
surface for all samples. The peak intensity was higher for the Fe-
OH/Fe-OOH species than Fe-O, where Fe-OH and Fe-OOH are inter-
mediate compounds formed in the corrosion reaction pathway,
which lead to the formation of Fe3O4. High resolution scans of
Cl2p revealed the presence of FeCl2 (rokuhnite), which is a precur-
sor compound to c-FeOOH and Fe3O4. This species forms when
conducting corrosion tests in HBSS, which has a high concentration
of Cl- ions [41].
Analysis of the Ca2p spectra identified the composition of the
agglomerates observed under SEM and EDS as Ca3(PO4)2. The pres-
ence of Ca3(PO4)2 is a result of the reactivity of the material when
exposed to simulated body fluid, such as HBSS, and not necessarily
due to the corrosion of Fe-316L. Other studies conducting immer-
sion tests with Fe-based materials, including Fe-35Mn and 316L
stainless steel, have identified calcium phosphates on the surface
after testing in HBSS [40,42]. Variation in binding energies for Ca3(-
PO4)2 was found in the literature, particularly when identifying
Ca2p3/2 peak [26,29]. The peak binding energies identified in the
tested samples matched well with studies conducted by França
et al. [26], with a binding energy of 347.8 eV for the Ca2p3/2 peak.
However, the binding energy the Ca2p1/2 peak was not reported.
An investigation by Chusuei et al. [29] reported binding energies
for both Ca2p3/2 and Ca2p1/2, but shifts in the peak binding ener-
gies of Ca2p3/2 and Ca2p1/2 were observed of the tested samples
in comparison. It is possible that the Ca2p1/2 peak may be associ-
ated with CaCO3, which has a more similar binding energy
(351.5 eV) to that observed in the samples tested [43]; CaCO3 can
precipitate due to the bicarbonate ions present in modified HBSS.
However, it has been shown by Kirkland et al. [44] that the use
of HEPES buffer in HBSS may decrease or inhibit the formation of
CaCO3 in vitro. Due to the low intensity of Ca2p spectra, it was
not possible to conclude whether both Ca3(PO4)2 and CaCO3 were
present. Analysis of the P2p spectra further suggested the presence
of Ca3(PO4)2, with tested samples matching well to reference bind-
ing energies of calcium phosphate in literature, with minor varia-
tion [26,27]. This P2p peak may also be associated with iron
phosphates, which were identified in the XRD analysis [27,45].
3.5.3. Inductively coupled plasma optical emission spectrometry
The change in concentration of Fe, Ni, and Cr in the corrosion
solution as measured by ICP-OES are presented in Fig. 9. Overall,
the iron concentration decreased with time for all samples, which
reflects a similar trend when plotting the corrosion rate with time.
This was attributed to the formation of a stable degradation layer
on the sample surface, which would have slowed ion diffusion at
the surface, as well as to the development of the calcium-
phosphate passive film. Interestingly, the concentration of Ni for
all annealed samples followed the same trend as that of iron; such
a pattern was not observed for the as-sprayed data. Furthermore, a
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1200 C 1300 C As-Sprayed
86.4% (20123/37512) 119.8% (16086/35362) 92.3% (7733/14871)
36.2% (29658/21769) 90.0% (15634/29701) 152.7% (3225/8149)
6.6% (47920/44759) 56.5% (22759/35620) 13.8% (24631/28019)
28.0% (50158/64209) 5.9% (38096/35841) 14.0% (26183/29841)
60.0% (11060/4428) 60.6% (13091/5160) 54.8% (11229/5074)
46.30% (7688/4129) 36.6% (9799/6217) 37.0% (7677/4834)
– 19.8% (5865/4706) 15.7% (4413/3718)
5.27% (3927/4134) 61.8% (5627/9105) 42.6% (5480/7816)
– 71.5% (4031/6912) 35.1% (3818/5159)
25.0% (7075/8843) 60.6% (2968/4766) 65.8% (2199/3646)
17.9% (5029/5930) 31.9% (3619/4774)
15.0% (4776/5494) 37.4% (4322/5937)
tenfold increase in concentration in comparison to the as-sprayed
data was found. This is a further indication of the transformation of
the Fe-316L amalgamate after annealing, due to atomic diffusion.
More specifically, it suggests that both the iron and nickel are
degrading concurrently in the annealed specimens, whereas the
iron matrix is only degrading in the as-sprayed sample. However,
the change in chromium concentration with time did not follow
the same trend as nickel and iron for the annealed samples, and
the reported concentration was often lower than the value deter-
mined in HBSS. While both nickel and chromium are substitutional
atoms during atomic diffusion, the atomic radius of chromium is
larger than that of nickel (166 vs. 149 pm), which could slow the
diffusion rate of chromium across particle boundaries during
annealing [46]. Furthermore, EDS mapping of the annealed sam-
ples revealed chromium-rich precipitates throughout the matrix,
rather than a uniform distribution like that observed with nickel.
This may explain why chromium was not observed in the corrosion
products within the testing solution.
4. Discussion
Microstructural, mechanical, and corrosion investigations were
conducted to assess the impact of annealing on the overall material
behaviour of Fe-316L, with heat treatment at 1100 C, 1200 C, and
1300 C. Annealing resulted in substantial atomic diffusion
between the Fe and 316L particles, and ultimately the transforma-
tion of austenitic stainless steel to low-alloyed ferrite, which was
confirmed by EDS and XRD. Precipitates with a high element con-
centration of chromium were observed with increasing concentra-
tion as the annealing temperature increased. Interestingly, the
presence of precipitates within the microstructure, which tradi-
tionally have embrittling characteristics, did not have an impact
on the mechanical behaviour of annealed Fe-316L [47,48]. In com-
parison to the as-sprayed condition, the mechanical properties of
Fe-316L significantly improved after heat treatment. This was
attributed to two primary factors: an increase in particle–particle
bonding due to sintering at the boundaries and recrystallization,
which removed residual stress, and work hardening induced by
powder deposition. A statistically significant increase was
observed in the ductility between the annealed samples. It is inter-
esting to note, however, that the austenite levels were very similar
between the annealed specimens and significantly lower than the
as-sprayed sample. Since austenite is stabilized by Ni, then exten-
sive Ni diffusion had occurred at all annealing conditions, which
should lead to strong interparticle bonds [49]. The ductility is
low when annealed at 1100 C, however, and high at 1300 C. This
suggests that large scale diffusion and particle sintering are not the
only influence on elongation and perhaps atomic diffusion is not
the sole indicator of effective sintering for cold-sprayed coatings.
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Fig. 9. Change in percent of iron, nickel, and chromium within the testing solution for the static corrosion tests for samples annealed at (a) 1100 C; (b) 1200 C; (c) 1300 C;
and (d) as-sprayed samples. The dotted line represents the concentration of iron, nickel, and chromium determined within the Hanks’ Balanced Salt Solution and HEPES buffer
only, which was equal to 0.0042%, 0.00002%, and 0.0006%, respectively.

This suggests that annealing of cold sprayed mixed metal powders
could provide an interesting rapid prototyping technique for bio-
material fabrication. This could be used to generate a new series
of low alloy steels with incremental changes of Ni and Cr to control
material properties. From the perspective of manufacturing
biodegradable stents, this would allow for the modification and
control of the corrosion rate of the material, potentially creating
a more patient-specific treatment approach to reflect disease
severity.
A peak corrosion rate of 0.22 mg cm2 day1 (0.10 mm year-1)
was determined for the samples annealed at 1300 C, in contrast
to the corrosion rate of the as-sprayed material, equal to
0.39 mg cm2 day1 (0.18 mm year-1). Interestingly, the corrosion
rate increased with higher annealing temperatures, where the
opposite would necessarily be expected due to improved particle
bonding [50]. The increase in corrosion rate observed between
samples annealed at 1100 C and 1200/1300 C may be attributed
to microgalvanic corrosion, due to increased precipitate concentra-
tion in samples annealed at 1200/1300 C. The intermetallic phase
observed in the microstructure can act as a cathode in an anodic
Fe-based matrix. It has been documented within literature that
intermetallic particles, such as those observed in this work, as well

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as inclusions and secondary phases, act as micro-cathodes to initi-
ate galvanic corrosion in an anodic matrix [48,51–53]. The imple-
mentation of intermetallic phases has been used to accelerate the
behaviour of iron-based biomaterials [51,52]. Schinhammer et al.
[51] introduced manganese and palladium to an iron matrix, which
produced Pd-based intermetallic phases that acted as cathodic
sites resulting in microgalvanic corrosion, increasing the overall
corrosion rate of the Fe-Mn-Pd alloy. In low-alloy steels, MnS inclu-
sions have been shown to act as cathodes to preferentially degrade
the nearby steel matrix [54–56]. In addition, microgalvanic corro-
sion has been observed between Cr-rich secondary phases and a
steel matrix, which promotes the Fe degradation within the steel
[57]. M secondary phase has also been shown to act as a cathode
in low carbon bainitic steel, resulting in accelerated corrosion in
NaCl solution [58]. Similar behaviour has been observed with
sigma phase in stainless steels, where preferential corrosion occurs
of c-austenite [48]. Such secondary phases are typically a result of
sensitization due to heat treatment. Therefore, the precipitates
formed during annealing may have acted as cathodic sites to accel-
erate the overall corrosion behaviour of the annealed Fe-316L sam-
ples. This may explain why the static corrosion rate was highest for
samples annealed at 1300 C as microstructural observation indi-
cated that it had the highest concentration of such precipitates.
EDS mapping of a sample annealed at 1300 C revealed an
increased oxygen concentration around the precipitates (Fig. 10),
suggestive of a corrosion reaction. Point identification by EDS
revealed that the precipitates had a higher concentration of Cr than
the surrounding matrix, the majority of which had Cr content of
27–32%. Microvoids were also identified within the Fe-316L
matrix.
From a more global perspective, the material properties of Fe-
316L annealed at 1300 C are consistent with or better than other
Fig. 10. Element concentration by EDS mapping of a sample annealed at 1300 C at
3000 magnification. Chromium-rich precipitates, as well as microvoids, were
observed within the surrounding Fe-316L matrix. Increased concentration of
oxygen was found around the precipitates.
Table 7
Comparison of the mechanical properties of Fe-316L, annealed at 1300 C for two hours, with other biodegradable stent material properties reported within literature.
Material UTSeng (MPa) Yield Stress (MPa)
Fe-316L (Annealed: 1300 C, 2 h) 280 140
316L Stainless Steel 490 190
Pure Iron 210 150
Mg-Zn 280 250
WE43 magnesium alloy 250 150
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developing biodegradable stents (Table 7). It has good tensile
strength for biodegradable stent application, and the UTS deter-
mined is higher than magnesium-based biodegradable materials.
While the ductility is less than that of pure iron or 316L stainless
steel, the elongation at fracture determined for Fe-316L is suffi-
cient for coronary stents and is considerably improved from its
as-sprayed state. Interestingly, the yield stress of Fe-316L was
the lowest of all compared materials, which is an important prop-
erty in stent design as decreased yield stress will lower the balloon
pressure required for stent expansion [59].
The corrosion rate of Fe-316L annealed at 1300 C is less than
other developing biodegradable stents [62]. The reduced corrosion
rate of annealed Fe-316L can be viewed as a compromise to
achieve the mechanical properties required for biodegradable stent
application. Recent clinical studies suggest that a reduced corro-
sion rate may be advantageous, however, to maintain device integ-
rity and scaffolding support in vivo over a longer duration of time
[15]. In particular, a recent case report indicated that the rapid
degradation of the BioTronik’s Magmaris stent after only
4 months led to inadequate stent scaffolding, resulting in severe
restenosis [15].
The identification of the corrosion products in this work allows
for an important understanding of the chemical reactions occur-
ring on the sample surface during degradation. By understanding
how and why the corrosion products form, the change in corrosion
behaviour over time can be explained. Furthermore, the accumula-
tion of corrosion products can influence the local pH environment
of the surrounding tissues in vivo [64]. To identify the corrosion
products formed on the sample surface, various characterization
techniques were used, including SEM, EDS, XRD, XPS, and ICP-
OES. A mixture of iron oxides/oxyhydroxides and phosphates were
found, as well as FeCl2, which form a multi-layer structure, typi-
cally composed of three layers [65,66]:
(1) Iron (II) oxide (FeOnH2O) or iron hydroxide (Fe(OH)2)
(2) Magnetite (Fe3O4)
(3) Iron (III) oxide (Fe2O3nH2O)
This is consistent with the corrosion products of other iron-
based biomaterials reported in literature [24,33,40]. It has been
documented within literature that the accumulation of these cor-
rosion products in vivo has not led to local or systemic toxicity
[67–70].
While an in-depth approach was used to analyze the corrosion
products of Fe-316L, identification of the species was challenging,
which was associated with the decreased thickness of the corro-
sion product layer. Furthermore, despite the increased resolution
of XPS in comparison to XRD, it was not possible to confidently
identify multiple species within the Fe2p high resolution scan,
which was attributed to the broad spectra and relatively undefined
satellite structures. Furthermore, the overlapping binding energies
of iron species, as well as substantial variation in binding energies
reported within literature, make interpretation difficult [71]. For
instance, the Fe2p3/2 peak, identified as Fe3O4, may also be associ-
ated with FeCl2 at a similar binding energy, which was identified
within the chlorine spectra. There was an indication of multiple
Elongation (%) Corrosion Rate (mm year1) Reference
23 0.10 (0.22 mg cm2 day1) –
40 – [60]
40 0.2 [61]
22 0.92 [62]
4 1.35 [63]
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species within the Fe2p spectra, which was established by the O1s
high resolution analysis, but the reduced intensity of the Fe2p
spectra made this interpretation less reliable. The limitations of
the analysis outlined here could be addressed through additional
analysis of a thicker corrosion product layer, assessing multiple
locations, for a more precise identification.
Due to the bioactivity of the sample material, the development
and stabilization of a passive Ca3(PO4)2 film was facilitated when
exposed to modified HBSS. The passive layer may be disrupted,
however, by Cl adsorption. This is accomplished by decreasing
its resistance to dissolution, by preventing the amalgamation and
crystallization of the film [24]. Furthermore, the use of HEPES buf-
fer is known to weaken the passive film by influencing the nucle-
ation processes of Ca3(PO4)2, ultimately producing a less dense
corrosion product layer [44]. This may explain why the protective
layer observed in this work was not homogeneous over the entire
surface, ultimately permitting the diffusion of Cl ions.
The results of this investigation are presented in the context of
their limitations. General limitations of the work include the local
nature of microscopy images presented, as well as potential varia-
tion when measuring sample dimensions. More specifically, the
identification of the precipitates observed within the annealed
specimens was challenging, and the techniques presented in this
work were unable to confidently identify its composition. Future
work involves additional microstructural investigations to confi-
dently identify the intermetallic phase observed. Next, the tech-
nique utilized to assess the galvanic corrosion reaction was
limited to a macro-characterization. It cannot directly quantify
the microgalvanic reaction within the Fe-316L coating, only that
of the annealed samples coupled with pure 316L. To quantify
microgalvanic corrosion, future work will develop a protocol to
implement scanning Kelvin probe force microscopy (SKPFM) to
measure potential differences across particle boundaries. This will
confirm the presence of micro-galvanic couples, as well as any
electropotential variations within the structure of annealed Fe-
316L material.
In this work, static corrosion tests were utilized as it is a conve-
nient method to assess the global corrosion behaviour of
biodegradable materials. However, this corrosion environment
has its limitations. Typically, it underestimates the corrosion
occurring on the surface as the convective contribution due to fluid
flow is not considered. Conversely, proteins were not included
within the testing solution, nor was the presence of cells on the
material surface considered, both of which will affect material
degradation [21]. In addition, the atmospheric conditions were
not controlled, i.e. implementing a testing environment with 5%
CO2. Future investigations should incorporate these factors to pro-
vide an improved prediction of the in vivo corrosion environment.
In addition, the use of polarization corrosion tests would comple-
ment the corrosion investigations completed in this work.
The formation of Ca3(PO4)2 on the sample surface due to the
reactivity of Fe-316L in HBSS slowed the overall corrosion beha-
viour. To truly quantify its impact on Fe-316L degradation, as well
as the other environmental conditions mentioned previously, an
in vivo study should be conducted, which would also allow for an
assessment of Fe-316L biocompatibility. The use of cellular tests
would also be beneficial to evaluate the biocompatibility of Fe-
316L, which should be conducted in future investigations.
5. Conclusions
There are numerous challenges associated with the develop-
ment and implementation of biodegradable stents in a clinical set-
ting, particularly when comparing current biodegradable stent
performance to the gold standard treatment of drug-eluting stents.
Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034
Biomaterialia (2019) 479–494
(xxxx) xxx
It is critical that newly developed biomaterials intended for
biodegradable stent application address the limitations of polymer
stents, which have largely underperformed in a clinical setting. It
was demonstrated in this work that cold-gas dynamic spraying is
a viable alternative for biomaterial fabrication and that a cold-
sprayed iron and 316L stainless steel material has potential to be
implemented in a clinical setting. It was found that annealing at
1300 C for 2 h yielded the mechanical and corrosion properties
necessary for biodegradable stent application, with an ultimate
tensile strength of 280 MPa, and a ductility of 23%. The corrosion
rate was equal to 0.22 mg cm2 day1, and a multi-layer structure
of ferrous oxides, hydroxides and oxide hydroxides was observed
after degradation. Ongoing investigations include the effect of
degradation on the mechanical properties of Fe-316L, as well as
in vivo studies to assess device biocompatibility and
biodegradation.
Acknowledgements
The authors wish to acknowledge funding sources from the Natural
Sciences and Engineering Research Council of Canada (Discovery
Grant NSERC RGPIN 217183-13), as well as the McGill University
Engineering Doctoral Award.
Declaration of Competing Interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared to
influence the work reported in this paper.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.actbio.2019.08.034.
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Please cite this article as: J. Frattolin, R. Roy, S. Rajagopalan et al., A manufacturing and annealing protocol to develop a cold-sprayed Fe-316L stainless steel
biodegradable stenting material, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.08.034