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Received: 12 December 1912 Revised: 12 December 1912 Accepted: 12 December 1912

DOI: 10.1002/mp.15987

RESEARCH ARTICLE

Tissue equivalence of 3D printing materials with respect to


attenuation and absorption of X-rays used for diagnostic
and interventional imaging

Patrizia Kunert1 Sebastian Trinkl1 Augusto Giussani1 Detlef Reichert2


Gunnar Brix1

1
Department of Medical and Occupational Abstract
Radiation Protection, Federal Office for
Radiation Protection, Oberschleissheim,
Introduction: Three-dimensional printing is a promising technology to produce
Germany phantoms for quality assurance and dosimetry in X-ray imaging. Crucial to this,
2
Department of Physics, Martin-Luther
however, is the use of tissue equivalent printing materials. It was thus the aim of
University Halle-Wittenberg, Halle, Germany this study to evaluate the properties of a larger number of commercially avail-
able printing filaments with respect to their attenuation and absorption of X-rays.
Correspondence Materials and methods: Apparent kerma attenuation coefficients (AKACs)
Patrizia Kunert, Externe und interne
Dosimetrie, Biokinetik, Abteilung f ür
and absorbed doses for different X-ray spectra (tube voltages, 70–140 kV) were
medizinischen und beruflichen measured and simulated by Monte-Carlo computations for a larger number
Strahlenschutz, Bundesamt f ür of fused-deposition-modeling (FDM) materials. The results were compared
Strahlenschutz, Ingolstädter Landstr. 1,
D-85764 Oberschleissheim, Germany.
with the respective values simulated for reference body tissues. In addition, the
Email: pkunert@bfs.de properties of polylactide acid samples printed with reduced infill densities were
investigated.
Results: Measured and simulated AKACs and absorbed doses agreed well with
each other and in case of AKACs also with attenuation coefficients derived from
the reference database of the National Institute of Standards and Technology
(NIST). For lung, adipose, muscle, and bulk soft tissue as well as for spon-
giosa (cancellous bone), printed materials with equivalent attenuation as well
as absorption properties could be identified. In contrast, none of the considered
printed materials was equivalent to cortical bone.
Conclusion: Several FDM materials have been identified as well-suited sub-
stitutes for body tissues in terms of the investigated material characteristics.
They can therefore be used for in-house production of individualized and task-
specific phantoms for image quality assessment and dose measurements in
X-ray imaging.

KEYWORDS
3D printing materials, anthropomorphic phantoms, fused-deposition-modeling, Monte-Carlo
simulations, tissue equivalence

1 INTRODUCTION have been commonly used in wide areas of science as


well as product development and manufacturing for over
Technologies for 3D printing such as fused-deposition- a decade. For medical radiation physics, it is a promis-
modeling (FDM),stereo lithography,or multi-jet modeling ing technology for the production of individualized

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2022 The Authors. Medical Physics published by Wiley Periodicals LLC on behalf of American Association of Physicists in Medicine.

7766 wileyonlinelibrary.com/journal/mp Med Phys. 2022;49:7766–7778.


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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7767

or task-specific phantoms for radiological imaging and To overcome this limitation, dedicated materials were
dosimetry.1–3 Since the variety and availability of com- developed, in which either metal filaments were mixed
mercial anthropomorphic phantoms are limited not only with PLA16 , or CaTiO3 or bismuth powder to ABS.17,18
regarding their tailored size and stature of mimicked per- However, these materials are not commercially available
sons but also because of their high acquisition costs, the (so far) and special equipment like multi-material printer
production of phantoms or add-ins to commercial phan- or filament-extruder are required for their processing.
toms using 3D printing offers great scientific potentials Although many studies have already addressed the
with the advantage of a fast,cheap,and easy production. issue of tissue equivalence of FDM materials, their
The FDM method is one of the most common additive results can hardly be compared with each other due
manufacturing methods, where a plastic wire, called fila- to different measurement methods used and radiation
ment, is heated into a thermoplastic state and extruded qualities studied. Moreover, to our knowledge, there are
into a 3D shape. A decisive advantage compared to no investigations of the tissue equivalence of FDM
other methods is the broad range of commercially materials regarding the energy deposition for diagnostic
available filament materials and the ability to lower the X-rays, which is crucial for the production of dosimetry
printed object density by increasing the amount of air phantoms. It was thus the aim of the present study to
inside the object using a grid or honeycomb structure.4 characterize a larger number of commercially available
Another advantage is the ability to process multiple thermoplastic polymers and composite materials in
materials, which is offered by modern 3D printers with terms of their attenuation and absorption properties to
more than one print head. This is especially of interest expand the spectrum of materials that are well suited
for the production of heterogeneous anthropomorphic as substitutes for various body tissues. To this purpose,
phantoms. measurements on FDM materials were accompanied
A crucial prerequisite for producing tailored phan- by Monte-Carlo (MC) simulations to characterize the
toms is the selection of materials that are equivalent to physical properties of body tissues under similar expo-
tissues regarding X-ray interactions. Therefore, the char- sure conditions. This is a novel approach that has not
acterization of materials regarding their attenuation and been used in previous studies to quantify the tissue
absorption properties is of great importance. In previ- equivalence of printed materials for photon energies
ous studies, various FDM materials were characterized used in X-ray imaging.
primarily with respect to their attenuation behavior only,
either by an analysis of CT densities given in Hounsfield
units (HU)4-9 or direct measurements of attenuation 2 MATERIALS AND METHODS
coefficients.10–13
It was found that many thermoplastic FDM materials 2.1 Sample production using FDM
have HU values between −80 and 340 HU, which make
them interesting as tissue substitutes.7 By decreasing In total, 20 different commercially available filament
the infill density of printed objects, this range could be types were investigated. They are summarized in
expanded down to −800 HU5 offering the possibility to Table 1. For each material, six plates with dimen-
approximate the CT density of lung tissue.4,9 In gen- sions 40 × 30 × 3.5 mm3 were produced, as shown
eral, there is a linear correlation between the infill and in Figure 1a. For the metal composite filaments, e.g.,
CT density, depending on the infill structure and the stainless steel, and copperfil, the thickness of the slices
used material.4-6,14 On the other hand, the HU range was reduced to 2 mm in view of their higher atten-
of printed materials can be expanded up to 7200 HU uation properties. Beside rigid materials, one flexible
using thermoplastic composite materials, often based material (Polyflex) was investigated. In contrast to other
on polylactic acid (PLA) mixed with metal or stone TPU-based materials, this material can be processed
powders.8 by any kind of FDM printer. For each material, plates
The direct comparison of attenuation coefficients of were printed with an infill density of 100%. To examine
printed materials with reference values for body tissues, the best infill density for the imitation of lung tissue,
like the ones given in the National Institute of Standards an additional series of PLA samples was produced for
and Technology (NIST) xcom database15 , indicated five different infill factors (25%, 30%, 35%, 40%, and
that PLA and chlorinated polyethylene (PE) are suitable 45%) using a grid infill structure. PLA was used, since
muscle equivalents.Furthermore,acrylonitrile butadiene it has been proven as equivalent to skeletal muscle12 ,
styrene (ABS), Nylon, and polyvinyl alcohol (PVA) can which in turn is comparable in its atomic composition
be used as adipose tissue substitutes in the diagnostic to lung tissue.19 However, the boundary of the samples
energy range.11,12 Thermoplastic polyurethane (TPU) with reduced densities must inevitably be printed in
and a wooden composite material proved suitable as full density (as shown in Figure 1b). To assess the
substitute for some soft tissue organs.10 impact of the boundary on the attenuation behavior, two
A core problem of all mentioned studies was that blocks with different thicknesses (11 and 22 mm) were
no suitable equivalent for cortical bone was found.6 produced for this sample series. The orientation during
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7768 TISSUE EQUIVALENT 3D PRINTING MATERIALS

TA B L E 1 Characterization of the fused-deposition-modeling (FDM) materials investigated in this study

Processing Mass density of


Sample Brand name, temperature Chemical the printed
name Material mixture manufacturer (◦ C) formula samples (g/cm3 )

ABS Acrylonitrile butadiene styrene ABS, Avistron 220–250 (C8 H8 C4 H6 C3 H3 N)n 1.01 ± 0.02
Carbonfil Polyethylentherepthalat + Cabronfil, FormFutura 230–265 1.16 ± 0.02
glycole + 20% carbon fibers
Copperfil PLA + high amount of copper Copperfil, ColorFabb 195–220 3.34 ± 0.02
powder
Easywood PLA + 40% wood particles Easywood, FormFutura 200–240 1.16 ± 0.02
HIPS High-impact polystyrene SSU00, 3ntr 220–260 (C8 H8 )n 0.95 ± 0.02
Laybrick Copolymers + chalk Laybrick, Polymaker 165–210 1.19 ± 0.02
Moldlay Unknown Moldlay, Layfilaments 170–180 1.10 ± 0.02
Nylon Nylon Nylon 230, Taulman 3D 225–235 (C12 H22 N2 O2 )n 1.05 ± 0.02
PC Max Polycarbonate PC-Max, Polymaker 250–270 1.16 ± 0.02
PETG Polyethylenterephthalat + PETG, Filamentworld 195–225 1.23 ± 0.02
glycole
PLA Polylactide PLA, Filamentworld 190–220 (C3 H4 O2 )n 1.21 ± 0.02
PMMA Polymethyl methacrylate PMMA, Material4Print 230–250 (C5 O2 H8 )n 1.12 ± 0.02
Polyflex Thermoplastic polyurethan Polyflex, Polymaker 220–235 1.17 ± 0.02
Pure PLA + 60% ecological fibers PURE, Aprinta Pro 190–220 1.21 ± 0.02
PVA Polyvinyl alcohol PVA, FormFutura 180–205 (C2 H4 O)n 1.17 ± 0.02
Concrete PLA + 50% concrete powder Stonefil, Concrete, FormFutura 200–240 1.57 ± 0.03
Potteryclay PLA + 50% clay powder Stonefil Pottery Clay, 200–240 1.51 ± 0.03
FormFutura
Granite PLA + 50% granite powder Stonefil, Granite, FormFutura 200–240 1.54 ± 0.03
Stainless PLA + high amount of steel Composite PLA, ProtoPasta 195–220 2.22 ± 0.06
steel powder
Terracotta PLA + 50% terracotta powder Stonefil, Terracotta, 200–240 1.53 ± 0.03
FormFutura

printing dictates the amount of material in each spatial in Table 1. The layer height was set to 0.1 mm. The
direction of the object since the chosen grid structure printing speeds were adapted to each material individ-
exhibits air ducts as shown in Figure 1c. In this study, the ually, with infill speeds ranging between 20 mm/s (e.g.,
orientation of air ducts was chosen to be perpendicular for Polyflex and Nylon) and 40 mm/s (e.g., for ABS
to the front surface that is perpendicular to the direction and PLA). For a better adhesion during the printing
of irradiation. However, samples printed with a parallel process, some materials [e.g., polymethyl methacrylate
orientation to the front surface were also examined (PMMA)] needed a heated print bed with temperatures
for comparison. For each material and infill density, an up to 100◦ C. The exact printing settings are given in
additional plate was printed with dimensions 40 × 30 Supporting Information (Table S1).
× 3.5 mm3 containing six 7 × 2 × 2 mm3 cavities to The mass density of all 3D printed material samples
accommodate thermoluminescent dosimeters (TLD) as was determined by weighing with a precision balance
also shown in Figure 1a. (Kern PCB; Kern & Sohn GmbH, Balingen, Germany;
All samples were printed on an FDM printer (Ultimaker precision, ±0.01 g) and measuring the dimensions with
2+; Ultimaker B.V., Geldermanser, Utrecht, Netherlands) a vernier calliper (uncertainty, ±0.01 mm). To avoid
using a 0.6 mm nozzle. The geometric information systematic uncertainties, the dimensions were mea-
of objects given in the computer-aided design (CAD) sured on three positions along the same direction and
software (Rhinoceros 5; Robert McNeel & Associates, averaged for volume calculation. The resulting densities
Seattle, WA, USA) was translated into a numerical con- of the printed samples are summarized in Table 1. The
trol language (g-code) using a slicing software (Cura volume of 3D printed objects can slightly vary from
4.3.0; Ultimaker B.V.). The correct processing tempera- the CAD model depending on the filament materials
ture for each material was found using a temperature due to different material behaviors during the heating
tower test20 , targeted on the temperature ranges given and cooling processes. For samples with reduced infill
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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7769

density, the mass density was determined only for the were stacked directly behind the Al filter to have samples
inner structure, by assessing the contribution of the fully with increasing thickness. Backscattering of X-rays on
printed boundaries on mass and volume measurements. the floor was reduced by a lead shield. A calibrated stem
chamber (M2333; PTW-Freiburg, Freiburg, Germany),
connected to a UNIDOS E dosimeter (PTW-Freiburg),
2.2 Experimental setup for the was placed at a distance of 51 cm from the focal point of
measurement of attenuation properties the X-ray tube and 128 cm above the floor. An appropri-
ate distance between source and detector is essential
The experimental setup for the investigation of atten- for the realization of a narrow-beam setup to mini-
uation properties is presented in Figure 2a. For all mize the influence of multiple scattered photons on the
materials investigated, attenuation curves were deter- transmission. The chamber is characterized by a small
mined by measuring the transmission of X-rays through sensitive volume and is suitable for a wide range of
different numbers of plates using a X-ray tube with applications. It was calibrated for air kerma measure-
tungsten anode (ISOVOLT 400/10; Seifert, Ahrensburg, ments with radiation qualities of TH 140, 100, and 70.22
Germany). To adequately calibrate our measurement data, radia-
Five radiation qualities were investigated, correspond- tion quality correction factors were interpolated for the
ing to tube voltages of 70, 80, 100, 120, and 140 kV. used radiation qualities.
X-rays were filtered with 7 mm intrinsic beryllium (Be) The air kerma rate, Ka (d), was measured over an
and additional 2.5 mm aluminium (Al), which corre- exposure time of 3 min at a tube current of 10 mA.
sponds to first Al half value layers of 0.25, 0.28, 0.35, A temperature and pressure correction of the cham-
0.43, and 0.51 cm. The used radiation qualities cover ber was made before each measurement session, as
approximately all RQR radiation qualities21 between well as a zero-point correction to suppress background
RQR 5 and RQR 9. A narrow beam geometry was noise. The mean values computed from three individual
obtained putting a 2.4 mm wide circular collimator in measurements were used for the further evaluation.
front of the opening window of the X-ray tube, between Kerma transmission ratios Ka (d)∕Ka (0) were deter-
the Be and Al filters. The collimator consisted of three mined for different sample thicknesses, d. The resulting
layers [2 mm lead (Pb), 1.8 mm copper (Cu), and 1.2 mm data were approximated by mono-exponential functions,
Al]. For each investigated material type, printed plates according to the Lambert–Beer’s law:

E
Ka (d) ∫E max 𝜑 (d, E) ⋅ 𝛼 (E) dE
= 0
≅ exp (−AKAC ⋅ d) ,
Ka (0) Emax
∫E 𝜑 (0, E) ⋅ 𝛼 (E) dE
0

(1)

where 𝜑(d, E) is the photon fluence, 𝛼(E) the fluence-


to-kerma conversion coefficient, E the photon energy,
and AKAC being the apparent kerma attenuation coef-
ficients. This equation is valid to a good approximation,
since 𝛼(E) depends only slightly on the photon energy
in the considered energy range.23 Curve fitting was
performed by a least-squares algorithm using SciPy24 ,
weighting the values by their inverse standard devia-
tion. For samples with reduced infill density, the influence
of fully printed boundaries was considered and AKACs
were calculated for the infill structure only.

2.3 Experimental setup for the


measurement of absorption properties

Absorption properties of the different materials were


F I G U R E 1 (a) Computer-aided design (CAD) construction of characterized by measuring the absorbed dose directly
samples consisting of six fully printed plates and one additional plate
inside a stack of all printed plates. The dose mea-
with cavities to accommodate thermoluminescent dosimeters (TLDs).
(b) Visualization of a sample block with a 35% infill density with grid surements were performed with lithium fluoride (LiF)
infill style in the slicing software (view from the top of the sample). TLD-rods of 1 × 1 × 6 mm3 (TLD-100; Bicron-Harshaw,
(c) Image of the printed sample block with a 35% infill density. Cleveland, OH, USA) that were placed in the cavities of
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7770 TISSUE EQUIVALENT 3D PRINTING MATERIALS

F I G U R E 2 Experimental setups: (a) Narrow-beam setup for the measurement of X-ray transmission through 3D printed samples of
different thickness d. The image excerpt shows the arrangement of filters used for the narrow-beam collimation. (b) Broad-beam setup for the
measurement of the dose absorbed in the printed material.

the designated plate, which was arranged in the middle in the measurements by using the spectral data of the
of the stack of the printed plates, as shown in Figure 2b. python-based program xpecgen.27 All simulations were
The stack was placed in the center of the beam on a run on a Linux virtual machine with 40 CPUs (Intel Xeon
low-density polystyrene plate at a distance of 127 cm CPU E5-2687 W v3 at 3.10 GHz; Intel, Santa Clara, CA,
to the focal point of the X-ray tube. Irradiations were USA) using the low-energy electromagnetic package
performed with the ISOVOLT 400 X-ray tube, the expo- of Geant4 with a cut-in-range of 0.1 mm.28 Coherent
sure time was 2 min for a tube current of 10 mA. A scattering was neglected.
broad-beam setup was used to ensure a homogeneous The simulations of transmission measurements were
irradiation of the material stack and the TLDs. The same done with 107 primary photons. For an uncertainty
radiation qualities as for the attenuation measurements analysis, the mean values and the standard deviation of
were used. several simulation runs were calculated. The computing
For each measurement, a new set of six TLDs was time for one simulation was about 1 h. The AKACs
used, which were individually calibrated by irradiation derived from the simulated attenuation curves were
with the ISOVOLT 400 X-ray tube at the same radiation computed by exponential fits of the simulated kerma
qualities as used for the experiments. Calibration was transmission ratios according to Equation (1).
assessed with the above-mentioned stem chamber Absorbed doses inside the reference tissues were
and the dosimeter. The chamber was calibrated for simulated in the middle of the tissue block with an
absorbed dose in water for radiation qualities of TH 140 inserted LiF-crystal with a size of 12 × 6 × 1 mm3 . For
and 100. The correction factors were interpolated for comparison with the measured dose in printed materi-
the actual radiation qualities. The individual calibration, als, the thickness of the simulated tissue samples was
annealing, and read-out of the TLDs were performed adjusted to the slightly varying thicknesses of the dif-
with a TLD oven (TLDO 1321; PTW-Freiburg) and a ferent kind of materials. To save computation time, the
TLD reader (Harshaw TLD 5550; Thermo Fischer Sci- opening angle of the broad-beam setup was set to 10◦ .
entific, Waltham, MA, USA) according to a standardized It could be shown that this did not affect the results.
protocol.25 For further evaluations, the mean dose value, Simulations were done with 109 primary photons, which
D, of measured TLD doses was used. corresponds to a simulation time of 4 h per run. The
mean and standard deviation of independent runs was
used for further evaluations. The dose achieved by sim-
2.4 Monte-Carlo-based computation of ulations was scaled using a calibration factor obtained
tissue properties by comparing the experimentally measured dose in a set
of reference TLDs and the dose simulated for the same
Both experimental setups described above were sim- geometrical setup.
ulated by MC computations (Geant4 10.5; Geant4 To enable a cross-validation of measured and sim-
Collaboration26 ). In order to determine reference values ulated AKACs and absorbed doses, simulations were
for different body tissues as characterized in Table 2, also performed for homogeneous PMMA samples with
simulations were run with the 3D sample materials the same dimensions as the printed samples and the
replaced by tissue samples of the same size.The energy density and the atomic composition of PMMA given in
spectra were adjusted to the radiation qualities utilized Table 1.
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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7771

TA B L E 2 Reference tissues used for Monte-Carlo simulations as characterized by their mass densities and atomic compositions

Mass fraction (%)


Mass density
Tissue (g/cm3 ) H C N O Na Mg P S Cl K Ca

Lung tissue19,29 0.38 10.5 8.3 2.3 77.9 0.2 0.1 0.2 0.3 0.2 0.0 0.0
Adipose tissue19 0.95 11.4 59.8 0.7 27.8 0.1 0.0 0.0 0.1 0.1 0.0 0.0
Skeletal muscle19 1.05 10.2 14.3 3.4 71.0 0.1 0.0 0.2 0.3 0.1 0.4 0.0
Bulk soft tissue19 a 1.03 10.5 25.6 2.7 60.2 0.1 0.0 0.2 0.3 0.2 0.2 0.0
Cortical Bone19 1.92 3.4 15.5 4.2 43.5 0.1 0.2 10.3 0.3 0.0 0.0 22.5
Spongiosa29 1.31 7.8 24.8 3.9 52.5 0.1 0.2 3.4 0.3 0.0 0.1 6.8
a 19
Used as substitute for soft tissues, for example, glands, trachea, uterus in ICRP 89.

2.5 Validation of measurement and and simulation methods employed. The cross-validation
simulation methods for simulated and NIST-based AKACs for cortical bone
is shown in Figure 3c. Again, there is a good linear
To validate the methods for measurement and simula- correlation between both data. Yet, the standard devi-
tion of AKACs and absorbed doses, both approaches ations of the simulated AKACs are higher compared
were compared in the case of PMMA at all tube voltages to the data obtained for PMMA due to slight deviations
considered. Additionally, the AKACs obtained by both from the mono-exponential attenuation behavior due to
methodological approaches were compared with refer- beam-hardening effects.
ence data derived from the energy-dependent fluence Absorbed doses measured in PMMA are plotted
attenuation coefficients given in the NIST database. For against the corresponding simulated values in Figure 3d.
this, the X-ray spectra were divided into small energy The differences were within the range of ±5%. On aver-
bins for which the fluence attenuation coefficients can age, simulated dose values were 3% lower than the
be considered as constant. Using this approximation, measured values. This slight systematic deviation was
mean transmission ratios were computed for different taken into account for a fine calibration of all simulation
thicknesses, d, according to Equation (1) (replacing the results.
integrals by sums) and used to estimate NIST-based
AKACs by the mono-exponential fitting procedures
described above. To evaluate the effect of beam hard- 3.2 Physical properties of printed
ening, simulated AKACs were also compared with NIST materials as compared to tissues
data for cortical bone as a high-density tissue by using
the same approach as described above. Figure 4 summarizes the attenuation properties of
the investigated printed materials (measured AKACs)
in comparison with those of body tissues (simulated
3 RESULTS AKACs) for a representative tube voltage of 100 kV. The
investigated printed materials cover a broad range of
3.1 Validation of the used attenuation values. Various materials are comparable
measurement and simulation methods to adipose, bulk soft, and skeletal muscle tissue. Sam-
ples printed with a reduced infill density are in a range
All results for the validation processes are summarized comparable to lung tissue. Stone-containing filaments
in Figure 3a–d. Figure 3a shows that the transmis- show higher attenuation properties and are comparable
sion ratios determined experimentally for PMMA can to spongiosa. In contrast, the attenuation behavior of
be very well approximated by mono-exponential func- cortical bone cannot be adequately reproduced by the
tions in the considered energy range. This justified the printed materials considered, since stone-containing
use of the Lambert–Beer law as in Equation (1) to materials have lower and metal-containing filaments
determine AKACs for the investigated materials and soft markedly higher attenuation coefficients. As high-
tissues, although measurements were performed with density materials are more effective in inducing beam
conventional X-ray spectra and not with mono-energetic hardening, deviations from the Lambert–Beer law are
X-rays. expected; this explains the slightly larger error bars of
The linear relationship between both measured and the AKACs determined for the high-density material in
simulated AKACs and the respective NIST-based coef- comparison to other materials
ficients is shown for PMMA in Figure 3b. Measured and Absorbed doses measured in printed materials and
simulated AKACs were on average 1% lower and 2% simulated for body tissues are summarized in Figure 5
higher than the corresponding NIST data, respectively. for a representative tube voltage of 100 kV. Because
This verifies the high accuracy of the measurement mass densities have per definition no direct impact
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7772 TISSUE EQUIVALENT 3D PRINTING MATERIALS

F I G U R E 3 General validation results for the considered X-ray spectra. (a) Measured transmission ratios for polymethyl methacrylate
(PMMA) samples of different thickness in log-scale. The fitted apparent kerma attenuation coefficients (AKACs) are given in the legend.
(b) Correlation of AKACs determined from attenuation measurements (light gray symbols) and simulations (dark gray symbols) with
NIST-based AKACs for PMMA. (c) Correlation of simulated and NIST-based AKACs for the example of cortical bone. (d) Correlation between
measured and simulated absorbed doses in a PMMA block. Error bars give standard deviations and the lines mono-exponential regressions (a)
and linear regressions through the origin (b–d). The shaded areas represent deviations of less than ±5% from the NIST-based AKACs (b and c)
and from the line of identity (d).

on the absorbed dose, the doses to most printed only a slight energy dependence, with values increasing
non-composite materials and soft tissues are in a com- at higher tube voltages. In contrast, the relative differ-
parable range taking their uncertainties into account. In ences between stone filaments and spongiosa as well
contrast, the dose absorbed in spongiosa and cortical as between stone/metal filaments and cortical bone
bone is significantly lower due to the different elemental decrease with increasing tube voltages (Figure 6e,f ). For
composition of these tissues. While the absorbed dose lung tissue, PLA samples printed with 40% and 45% infill
in Laybrick is very similar to that in spongiosa, the dose densities are within their uncertainties in the range of
in stone-containing materials is much higher than the ±5% difference (Figure 6a). The same holds for ABS
one in cortical bone. and Nylon for adipose tissue (Figure 6b). Easywood,
The tissue equivalence of the investigated printed Moldlay, and PLA show very similar attenuation prop-
materials was quantitatively assessed based on the erties to each other and are within the range of tissue
relative differences, δ, between measured AKACs and equivalence over the whole investigated energy range
absorbed doses and the corresponding simulated tissue for bulk soft tissue and skeletal muscle (Figure 6c,d).
reference values. Materials were assumed to be tissue Additional materials fulfilling the condition for tissue
equivalent if the δ values for both, AKACs and absorbed equivalence are PVA for bulk soft tissue, polyethy-
doses, are less than ±5%. lenterephthalat + glycole (PETG) for skeletal muscle,
The relative differences between AKACs measured and with slight limitations Laybrick for spongiosa. With
for selected printed materials and those simulated for the exception of Laybrick, the relative differences
reference soft tissues, plotted in Figure 6a–d, show are distinctly larger for stone/metal composites and
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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7773

F I G U R E 4 Apparent kerma attenuation coefficients (AKACs) for a representative tube voltage of 100 kV for all printed materials
considered (light gray bars) and body tissues (dark gray bars) determined from measurements and simulations, respectively. The error bars give
the standard deviations.

F I G U R E 5 Absorbed doses for a representative tube voltage of 100 kV in the printed materials considered (light gray bars) and body
tissues (dark gray bars) determined from measurements and simulations, respectively. The error bars give the standard deviations. Doses were
measured in slightly different depths due to slight variations in sample thicknesses after the printing process; simulated tissue data refer to a
mean depth of 13 mm.

spongiosa/cortical bone as compared to polymers is an excellent linear relation between measured mass
and soft tissues due to the considerable differences densities and infill factors. On the contrary, measured
in their mass densities and elemental compositions AKACs are slightly lower than theoretically expected.It is
(Figure 6e,f ). to be presumed that the attenuation behavior is not only
Figure 7 shows the measured mass densities and affected by the average mass density and the atomic
AKACs for PLA samples printed with a reduced infill composition of the samples printed with a reduced infill
density versus the nominal percent infill factors. There factor, but also by the inhomogeneous infill structure
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7774 TISSUE EQUIVALENT 3D PRINTING MATERIALS

F I G U R E 6 (a–f) Relative differences between apparent kerma attenuation coefficients (AKACs) measured for selected printed materials
and simulated for reference tissues for five tube voltages. The error bars were calculated by means of Gaussian error propagation of standard
deviations of measured/simulated values. Measured values are slightly shifted on the x-axis for better visualization. Reference simulations for
polymethyl methacrylate (PMMA), polylactide (PLA), and PLA35 with a mean density corresponding to that of the printed samples are
additionally plotted. The shaded areas represent the range of less than ±5% relative differences, for which tissue equivalence was assumed.

(cf. Figure 1c). This assumption is supported by the materials and those simulated for soft tissues and spon-
fact that AKACs simulated for the PLA35 sample with a giosa do not show a significant energy dependence.
homogeneous material distribution are about 5% higher In contrast, there is a distinct energy dependence for
(averaged over all tube voltages) than the values mea- cortical bone with larger differences for lower tube volt-
sured in the printed sample with the corresponding mass ages (Figure 8f ). Considering the uncertainties of the
density (Figure 6a). Moreover, the direction of the air relative differences, the doses inside all PLA samples
ducts with respect to the X-ray beam affects the atten- with reduced infill densities and fully printed PLA are
uation behavior. Irradiating the samples with the beam identical but do not strictly meet our equivalence cri-
parallel and not orthogonal to the air ducts resulted on terion for lung tissue over the examined energy range
average in 10% lower AKACs. (Figure 8a). Easywood, Moldlay, PETG, PLA, and PVA
As Figure 8a–e demonstrates, the relative differences are in good approximation within the equivalence range
between absorbed doses measured in selected printed for bulk soft tissue for all tube voltages (Figure 8c),
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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7775

performed for X-ray spectra and not for monoenergetic


X-rays, which corresponds to the actual situation in
X-ray imaging. Due to the broad range of investigated
radiation qualities, the results of this study are transfer-
able to other radiation qualities typically used for X-ray
imaging.The fact that the transmission of X-rays through
printed samples was quantified by the kerma, and not by
the photon fluence, does not interfere with the objective
of our study, namely to compare the physical properties
of printed materials with those of body tissues.
Different tissue substitutes could be identified for
lung, adipose, bulk soft, skeletal muscle tissue as well
as for spongiosa. However, none of the investigated
commercial stone or metal filaments was similar to
cortical bone with respect to either their attenuation or
their absorption properties.
Materials which were already known to be appropriate
F I G U R E 7 Correlation of mass densities (light gray symbols, left substitutes for skeletal muscle6,11,14 (PLA) or adipose
axis) and apparent kerma attenuation coefficients (AKACs) (dark
gray symbols, right axis) measured at 100 kV for polylactide (PLA)
tissue11,13 (ABS, Nylon) with respect to their attenuation
samples printed with reduced infill factors. The error bars give the behavior were found to be tissue equivalent also with
standard deviations and the line the theoretically expected respect to their absorption properties. Additional materi-
relationship. als were identified to be suitable substitutes for skeletal
muscle (PETG, Moldlay), bulk soft tissue (PVA, Moldlay,
Easywood), and spongiosa (Laybrick) in both aspects.
whereas the doses in these materials are more than 5% With a decrease of the infill density of PLA to 45% or
higher than in skeletal muscle for tube voltages below 40%, also lung tissue can be mimicked in both proper-
100 kV (Figure 8d). For adipose tissue, the dose inside ties. For some materials the relative differences deter-
ABS, Nylon, and Polyflex is equivalent over the whole mined for specific tube voltages were slightly outside the
investigated energy range (Figure 8b). The same holds ±5% range, for example, for absorbed doses in lung tis-
for Laybrick as a substitute for spongiosa (Figure 8e). sue at 100 and 120 kV (Figure 8a) or skeletal muscle tis-
Comparable to the results reported for AKAC, neither sue for tube voltages below 100 kV (Figure 8d). It should
stone nor metal materials are suitable substitutes for be noted, however, that both the measured and simu-
cortical bone (Figure 8f ). lated values are subject to uncertainties, which results
The deviations between the physical properties in an increased relative uncertainty of their difference δ.
(AKAC, absorbed dose, physical density) of selected Our study thus succeeded not only in expanding the
printed materials and those of the reference soft tissues number of 3D printing materials with tissue equivalent
and spongiosa are summarized in Table 3. The values transmission properties in the diagnostic energy range,
given here represent mean values over all tube voltages. but also in identifying materials with tissue equivalent
This approach was considered appropriate to charac- absorption properties. To the best of our knowledge, the
terize the tissue equivalence of the printed materials latter aspect had not yet been systematically investi-
over the considered energy range due to the only weak gated in previous studies for the energy range relevant
energy dependency of the transmission and absorption for X-ray imaging. Consequently, tissue equivalent fil-
properties observed. ament materials can be used to print individualized or
task-specific tailored body phantoms to determine the
quality of images, for example, in terms of the noise
4 DISCUSSION and contrast, as well as the dose distribution by inserted
TLDs.
In this study, the tissue equivalence of a large number Like in other studies, samples with different infill den-
of commercially available thermoplastic polymers and sities were printed to simulate lung tissues.4,6 For the 3D
composite materials was investigated with respect to printer used in the present study, we could demonstrate
both their attenuation and absorption of X-rays for tube an excellent linear relation between infill factor and
voltages between 70 and 140 kV typically used for X-ray the mass density of printed materials. Nevertheless,
imaging. To this end, extensive measurements and MC measured AKACs slightly deviate from a linear relation
simulations were performed. The results were validated with the percent infill factor. This implies that the atten-
with each other as well as to reference NIST data in uation properties of samples printed with a reduced
the case of attenuation measurements at the example infill density need to be investigated in detail, since they
of PMMA. All measurements and simulations were cannot necessarily be derived from the nominal infill
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7776 TISSUE EQUIVALENT 3D PRINTING MATERIALS

F I G U R E 8 (a–f) Relative differences between absorbed doses measured for selected printed materials and for reference tissues, simulated
for each material (under consideration of individual material thicknesses), for five tube voltages. The error bars were calculated by means of
Gaussian error propagation of standard deviations of measured/simulated values. The curves show the results of reference simulations for
polymethyl methacrylate (PMMA) and polylactide (PLA), which were done with a sufficiently high number of initial particles. Measured values
are slightly shifted on the x-axis for better visualization. The shaded regions indicate the range of less than ±5% relative differences, for which
tissue equivalence was assumed.

factor itself. Moreover, the inhomogeneous structure of attenuation and absorption is especially beneficial since
printed samples, in particular the orientation of air ducts PLA is easily available at low costs. Additionally, many
with respect to the beam direction, has to be considered composite materials are based on PLA, which facilitates
as a relevant factor that may affect the measured atten- their adhesion in the printing process of more complex
uation in a narrow-beam setup. Other infill structures, phantoms. The availability of other similar materials,
for example, a gyroid structure could be a solution for for example, Moldlay and Easywood, allows a certain
this problem.30 As expected, the dose inside all printed flexibility with respect to the processing temperature
PLA samples was not considerably affected by the infill and material adhesion, when using a multi-material
density and structure. FDM printer. With PVA and PETG, there are additionally
The confirmation of PLA as substitute for skeletal bulk soft tissue and skeletal muscle equivalents with
muscle and bulk soft tissue with respect to both X-ray slightly different attenuation properties than PLA. This
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TISSUE EQUIVALENT 3D PRINTING MATERIALS 7777

TA B L E 3 Percent differences (mean ± SD) between selected makes it possible to realize minor differences in imag-
printed materials (measured data) and soft tissues/spongiosa ing contrasts, for example, between different organs
(simulated data) with regard to their relevant material properties
[apparent kerma attenuation coefficient (AKAC), absorbed dose,
in anthropomorphic phantoms. On the other hand, it
mass density] averaged over the considered tube voltages should be noted that printed PMMA did not fulfil the
requirements for tissue equivalence neither for muscle
Relative differences (%)
nor for bulk soft tissue. The analysis of commercially
Adipose tissue AKAC D ρ
available composite filaments yielded that they are not
HIPS −8.9 ± 1.0 −4.5 ± 5.6 −0.1 ± 2.1 suited as substitutes for cortical bone due to the large
ABS −2.7 ± 1.6 0.8 ± 3.0 6.6 ± 1.8 differences in mass densities and atomic compositions.
Nylon 0.6 ± 2.0 0.2 ± 4.0 10.5 ± 1.8 The development of suitable filaments would therefore
Carbonfil 10.4 ± 2.6 −0.7 ± 3.1 22.1 ± 2.1
be very welcome.
There are some limitations to our study: We did not
PMMA 13.4 ± 2.2 −0.2 ± 2.4 17.9 ± 2.0
examine the variation between manufacturers for the
PLA 24.1 ± 3.4 −3.7 ± 2.4 27.4 ± 2.2 same kind of filament materials, nor the influence of
Polyflex 9.9 ± 0.6 −2.8 ± 3.0 22.6 ± 2.2 different types of printers and printing settings. The
Lung tissue AKAC D ρ adhesion between different tissue equivalent materials
was not aim of the present study, and will be inves-
PLA25 −41.6 ± 2.2 −7.8 ± 2.6 −26.3 ± 4.7
tigated in further work focusing on the production of
PLA30 −32.0 ± 1.3 −6.7 ± 3.1 −10.5 ± 4.8 complex structured phantoms by a multi-material FDM
PLA35 −16.8 ± 1.5 −7.7 ± 2.5 7.9 ± 4.7 printer. Finally, possible approaches to match mate-
PLA40 −3.3 ± 2.2 −6.8 ± 2.4 26.3 ± 4.5 rial properties to those of cortical bone, for example,
PLA45 4.0 ± 2.1 −5.8 ± 2.3 36.8 ± 4.5 by reducing the infill density or content of metal in
composite filaments, was not yet investigated.
Bulk soft tissue AKAC D ρ

Carbonfil −10.8 ± 1.8 6.4 ± 4.3 12.6 ± 1.9


PMMA −7.9 ± 1.1 6.3 ± 2.5 8.7 ± 1.8 5 CONCLUSION
PC Max −9.0 ± 1.3 4.9 ± 2.9 12.6 ± 1.8
PLA 0.5 ± 1.0 2.0 ± 2.9 17.5 ± 2.0 In this study, a large number of commercially available
PVA −3.8 ± 1.1 3.5 ± 2.4 13.5 ± 2.1
FDM materials was investigated as possible substitutes
for representative tissues for five different radiation qual-
Polyflex −19.5 ± 1.9 4.1 ± 4.2 13.1 ± 2.0
ities typically used for X-ray imaging. With respect to
Moldlay 0.0 ± 0.9 −0.6 ± 3.2 6.4 ± 1.8 both their attenuation and absorption properties, various
Easywood −1.4 ± 1.1 2.4 ± 1.5 12.6 ± 1.8 substitutes were found to be equivalent to soft tissues
PETG 9.7 ± 0.7 3.2 ± 2.3 19.4 ± 1.9 and spongiosa. These identified thermoplastic polymers
Pure 18.2 ± 4.1 −0.3 ± 2.2 17.5 ± 1.9 and composite materials can be used for in-house 3D
printing of patient- or task-specific phantoms aimed to
Spongiosa AKAC D ρ
improve image quality assessment and dosimetry in
Laybrick −3.7 ± 5.0 −0.9 ± 4.2 −9.1 ± 1.5 X-ray imaging.
Skeletal muscle AKAC D ρ
AC K N OW L E D G M E N T S
Carbonfil −15.6 ± 2.0 8.5 ± 4.9 10.5 ± 1.9
We would like to acknowledge Dr. Patrick Woidy (BfS,
PMMA −12. 9 ± 1.5 7.1 ± 3.2 6.7 ± 1.8
Department of Environmental Radioactivity) for the kind
PC Max −13.9 ± 1.6 7.3 ± 3.8 10.5 ± 1.8 introduction into the topic of FDM 3D printing, as well
PLA −4.8 ± 0.6 5.3 ± 4.8 15.2 ± 2.0 as the group of Oliver Meisenberg (BfS, Department of
PVA −9.1 ± 1.6 6.1 ± 3.4 11.3 ± 2.1 Medical and Occupational Radiation Protection) for the
Polyflex −15.9 ± 2.7 6.9 ± 4.1 11.0 ± 2.0 provision of their 3D printer and our colleague Dr.Helmut
Schlattl for his professional support.
Moldlay −5.5 ± 1.1 3.3 ± 3.8 4.4 ± 1.8
Open Access funding enabled and organized by
Easywood −6.7 ± 0.7 5.0 ± 4.6 10.5 ± 1.8
Projekt DEAL.
PETG 3.6 ± 1.2 6.1 ± 2.7 17.1 ± 1.9
Pure 11.6 ± 3.3 1.1 ± 2.4 15.2 ± 1.9 CONFLICT OF INTEREST
Note: The shaded materials meet or at least come very close to tissue The authors have no conflicts of interest to disclose.
equivalence in terms of both their attenuation and absorption properties.
Abbreviations: ABS, acrylonitrile butadiene styrene; HIPS, high impact
polystyrene; PC, polycarbonate; PETG, polyethylenterephthalat + glycole; PLA, F U N D I N G I N F O R M AT I O N
polylactide; PMMA, polymethyl methacrylate; PVA, polyvinyl alcohol The authors received no specific funding for this work.
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7778 TISSUE EQUIVALENT 3D PRINTING MATERIALS

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