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The International Journal of Advanced Manufacturing Technology

https://doi.org/10.1007/s00170-023-11268-6

ORIGINAL ARTICLE

3D printing from micro‑CT images of the trochlea of the superior


oblique muscle and its future applications
Hyunkyoo Kang1   · Guk Bae Kim2 · Minje Lim2 · Wonhee Lee2 · Wu‑Chul Song3 · Kang‑Jae Shin4 · Hyun Jin Shin5 ·
Andrew G. Lee6,7,8,9,10,11,12,13

Received: 3 September 2022 / Accepted: 13 March 2023


© The Author(s), under exclusive licence to Springer-Verlag London Ltd., part of Springer Nature 2023

Abstract
This study investigated the determination of detailed microstructure modeling of the trochlea of the superior oblique muscle
(SOM) using micro-computed tomography (micro-CT) and modeling of a potential prototype for a trochlea implant using
three-dimensional (3D) printing.
We dissected 15 intact orbits of 15 embalmed cadavers. The trochleae of the SOM were detached from the periosteum. The
specimens were stained by immersion in a 15% Lugol’s solution. Images were reconstructed using conventional scanner
software. Measurement points were determined for the middle cross section. Points P1 and P2 were selected where the SOM
adjoined the curvature of the inner trochlea. They defined the inner contact points of the SOM in the inner part of the trochlea
curvature. On the back of the trochlea, points P3 and P4 were selected at the uppermost and lowest points in the inner parts
of the straight trochlea, respectively. Origin O was defined on the arcuate line of P1P2
̂ to generate the smallest-diameter
circle consisting of P1, O, and P2. We then measured the angle from OP1toOP2 , and from OP3toOP4. We also measured the
distances OP1, OP2, OP3, andOP4 for the design of a potential trochlea implant prototype using 3D-printing and micro-CT-
based modeling. The distances OP1, OP2, OP3, andOP4 were − 2.2 ± 0.7, 1.4 ± 0.5, 2.7 ± 0.9, and 2.5 ± 0.4 mm (mean ± SD),
respectively. The angles from OP1toOP2 , from OP2to OP4, and from OP3toOP4 were 100.7 ± 14.4, 66.3 ± 18.0, and
98.9 ± 24.9 degrees, respectively. The present investigation demonstrates that the high-resolution CT is a powerful imaging
technique for defining the true 3D geometry of a specimen and can potentially be used to create a 3D-printed trochlea implant.

Keywords  Implant · Micro-computed tomography · Trochlea · Superior oblique muscle · Three-dimensional printing

6
* Hyun Jin Shin Department of Ophthalmology, Blanton Eye Institute,
shineye@kuh.ac.kr Houston Methodist Hospital, Houston, TX, USA
7
Kang‑Jae Shin Department of Ophthalmology, Neurology, Neurosurgery,
shinkj@dau.ac.kr Weill Cornell Medicine, New York, NY, USA
8
1 Department of Ophthalmology, University of Texas Medical
Department of Mechatronics Engineering, Konkuk
Branch, Galveston, TX, USA
University Glocal Campus, Chungcheongbuk‑Do,
9
Republic of Korea Department of Ophthalmology, UT MD Anderson Cancer
2 Center, Houston, TX, USA
Anymedi Inc, Seoul, Republic of Korea
10
3 Department of Ophthalmology, Texas A and M College
Department of Oral Anatomy and Developmental Biology,
of Medicine, College Station, TX, USA
College of Dentistry, Kyung Hee University, Seoul,
11
Republic of Korea Department of Ophthalmology, University of Iowa Hospitals
4 and Clinics, Iowa City, IA, USA
Department of Anatomy and Cell Biology, Dong-A
12
University College of Medicine, Busan, Republic of Korea Department of Ophthalmology, Baylor College of Medicine
5 and the Center for Space Medicine, Houston, TX, USA
Department of Ophthalmology, Research Institute of Medical
13
Science, Konkuk University Medical Center, Konkuk Department of Ophthalmology, University of Buffalo,
University School of Medicine, 120 Neungdong‑Ro, Buffalo, NY, USA
Gwangjin‑Gu, Seoul 05030, Republic of Korea

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The International Journal of Advanced Manufacturing Technology

1 Introduction 2 Materials and methods

The trochlea of the superior oblique muscle (SOM) is We dissected 15 intact orbits of 15 embalmed adult Asian
attached to the anteromedial orbital roof. The SOM tendon cadavers (7 male and 8 female orbits, 8 right and 7 left
passes through the trochlea, which redirects it to become orbits), aged 41–86 years at death (mean, 71.7 years). None
the functional origin of the SOM for ocular movement of the cadaveric specimens had eyelid or orbital abnor-
[1]. Because of the characteristic location of the trochlea malities. This study was performed in accordance with the
at the anterior margin of the orbital roof, trochlea injury principles outlined in the Declaration of Helsinki. Appro-
can occur during blepharoplasty [2, 3], orbital surgery [4], priate consent and approval were obtained before using the
and following traumatic eyelid injuries [5, 6]. Injury to the specimens.
trochlea occurs infrequently, but it can result in devastat-
ing complications such as diplopia, abnormal head posture,
and ocular motility disturbances [7, 8]. Understanding the 2.1 Trochlea specimen sampling
detailed anatomy of the trochlea is therefore important to
plan the comprehensive therapeutic management of injury The medial corner between the external eyelid surface and
to this structure. orbit was dissected meticulously. Fibrous septae connecting
Previous studies have mostly focused on the intracra- the SOM tendon with the globe and those connecting the
nial course of the trochlear nerve (in fourth nerve palsy) SOM belly with the adjacent periorbita were cut. The troch-
and SOM damage in the orbit, with inadequate considera- lea and the SOM were detached from the periosteum, and
tion of damage to the trochlea itself. Its morphology has the connective tissue inside the trochlea was then carefully
been described previously as a U-shaped piece of cartilage removed. Special care was taken to ensure that the cartilagi-
attached to the orbital plate of the frontal bone. However, nous trochlear saddle was not disturbed (Fig. 1).
our study group previously reported the anatomic location of
the trochlea with reference to soft landmarks and found that
the trochlea has a complex three-dimensional (3D) structure 2.2 Image acquisition using micro‑CT
and that its morphology varies between individuals [9]. The
3D structure and morphology of the trochlea observed using Before performing micro-CT scanning, the specimens were
high-resolution imaging may therefore be helpful in defining stained by immersion in 15% Lugol’s solution (10  g of
individual variations in trochlear anatomy. potassium iodide and 5 g of iodine in 100 ml of water) for
Micro-computed tomography (micro-CT) imaging is an 24 h. The trochlea was then washed with alcohol to remove
emerging tool within the biomedical field, which was devel- free iodine, blotted dry, and scanned (SkyScan 1176, Bruker,
oped to scan small samples at a high resolution. Micro-CT Kontich, Belgium). The micro-CT scanning was conducted
allows the noninvasive visualization of structure morphol- under the conditions: 0.01188  mm of layer thickness,
ogy (e.g., shape and size) with a high degree of precision and
accuracy [10]. Micro-CT is also able to provide quantified
data sets of the structure to allow precise anatomic models
for 3D printing. 3D printing based on micro-CT-imaged
specimens can provide a better understanding of these struc-
tures, new insights into craniofacial surgical applications T
including possible prosthetics, and can be used in anatomy
education [11].
This study used cadaveric dissection with the purpose
of determining the detailed microstructure modeling of the
trochlea using micro-CT. We attempted to design a trochlea
implant prototype using 3D printing. Such information may
provide a comprehensive overview to the learner and also
assist clinicians to develop new concepts such as trochlea
replacement for the treatment of strabismus caused by troch-
lea injury.
Fig. 1  Cadaveric dissection demonstrating the location and shape of
the trochlea (T). The trochlea is attached to the anteromedial orbital
roof. The tendon of the superior oblique muscle (SOM) passes
through the inside of the trochlea

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The International Journal of Advanced Manufacturing Technology

0.01188 × 0.01188 ­mm2 of resolution, 70 kV of voltage, and and the part that is attached to the orbital plate of the
141 mA of X-ray tube current. frontal bone as posterior. In order to design a general-
For image segmentation, the Hounsfield unit (HU) val- ized trochlea model, extracted STL files were loaded into
ues for the localized area were determined using the local Materialise 3-matic software (version 15, Materialise) to
thresholding method. The segmentation of trochlea was be measured. Measurement points were determined using
carried out using region glow and split mask. Images were the middle cross section of the trochlea model as shown
reconstructed using the scanner software (NRecon 1.6.6.0, in Fig. 3A. Firstly, points P1 and P2 were selected where
SkyScan) and converted to Digital Imaging and Communi- the SOM adjoined the curvature of the inner trochlea of
cations in Medicine (DICOM) format for analysis (Fig. 2, anterior part. Point O located on the trochlea curvature was
Supplementary Video 1). Images were imported in com- then determined for generating the smallest-diameter cir-
mercial software (Mimics version 21, Materialise, Leuven, cle consisting of P1, O, and P2. Point O was the origin in
Belgium) and reconstructed following the steps of threshold- the proposed trochlea model. These points of the trochlea
ing, region growing, and semiautomatic image segmentation and the circle were the muscle path, and were designated
with manual editing where required, and the final volume as P1 and P2, respectively (Fig. 3A). OP1, OP2, and the
meshes were exported as stereolithography (STL) files. angle from OP1toOP2(∠P1OP2 ) were measured based on
point O. Among the parts corresponding to the posterior
2.3 Measured parameters part of trochlea, the uppermost part was set as P3, and the
lowest part was set as P4;OP3, OP4, and the angles from
We defined the part of trochlea that is close to the eye and OP2toOP4(∠P2OP4) and from OP3toOP4(∠P3OP4) were
in contact with superior oblique muscle as the anterior then measured.

Fig. 2  Three-dimensional modeling of the trochlea generated from micro-computed tomography data; SOM was removed from the trochlea

Fig. 3  (A) Set points for the


model. P1 and P2 are the
contact points between the
trochlea tendon and trochlea,
indicated by a circle, and the
red arrow is the direction of
the muscle. Each point was
connected and the dimensions
OP1, OP2, OP3, OP4, ∠P1OP2, ∠P2OP4,
and ∠P3OP4 were measured.
(B) Coordinate settings and sec-
tion design based on measured
dimensions

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The International Journal of Advanced Manufacturing Technology

3 Results The trochlea is hollow and cylindrical in shape, but an


artificial trochlea implant will probably have to be longer
Table  1 lists the averaged values obtained among 15 and accommodate an internal groove for the SOM. As
trochlea models. The distances OP1, OP2, OP3, andOP4 shown in Fig. 3B, points S1 and S2 were set by draw-
were 2.2 ± 0.7, 1.4 ± 0.5, 2.7 ± 0.9, and 2.5 ± 0.4  mm ing a line perpendicular to the tangents at points P1 and
(mean ± SD), respectively, while angles ∠P1OP2  , P2, respectively. A passage connecting points P1–P4, S1,
∠P2OP4  , and ∠P3OP4 were 100.7 ± 14.4, 66.3 ± 18.0, and S2 was made (blue line in the figure). Based on the
and 98.9 ± 24.9°, respectively. Based on the averages of standardized cross-sectional design, the trochlea implant
the measured data, a generalized trochlea middle cross- was 1.5 mm thick.
section model was plotted on the coordinates using the The plate to fix the trochlea implant into the orbit is
analytical geometry method as shown in Fig. 3B (green shown in Fig. 4A. The implant was designed with a thick-
line). OP2 was positioned on the y-axis, and the curvature ness of 1 mm and a micro screw diameter of 1.5 mm. For
connecting P1, O, and P2 was implemented by calculating the robust equipping on the curvature of the orbit, the plate
the equation of the circle. was bent into a right angle rather than a straight line. The
generalized trochlea models with the plate are shown in
Fig. 4B–D. The averaged value for 15 trochleae in Table 1

Table 1  Measured data and Case no OP1(mm) OP2(mm) OP3(mm) OP4(mm) ∠P1OP2(◦ ) ∠P2OP4(◦ ) ∠P3OP4(◦ )
averaged values for the 15
trochleae 1 2.0 2.2 2.4 2.9 102.6 59.7 118.5
2 2.6 1.8 2.7 3.0 117.9 62.8 100.9
3 2.0 1.7 1.7 2.2 110.5 34.8 123.7
4 3.7 1.3 4.8 2.7 118.3 70.9 97.7
5 2.9 2.1 3.6 3.1 132.0 54.6 103.0
6 2.5 0.9 3.6 2.7 100.0 93.8 59.7
7 1.7 1.9 1.3 2.3 85.6 67.5 108.4
8 1.8 1.1 2.0 2.4 83.8 72.5 83.6
9 2.0 1.3 2.9 2.4 98.4 91.1 70.8
10 3.1 1.0 3.5 1.9 99.4 68.4 121.7
11 2.5 1.4 2.7 2.7 103.7 90.2 56.4
12 1.2 0.7 1.9 1.8 98.5 74.2 82.3
13 1.5 1.3 1.9 2.2 92.6 37.0 136.3
14 1.3 0.7 3.0 2.4 80.1 46.0 128.0
15 2.3 1.8 3.1 2.8 87.0 71.6 86.0
Mean ± SD 2.2 ± 0.7 1.4 ± 0.5 2.7 ± 0.9 2.5 ± 0.4 100.7 ± 14.4 66.3 ± 18.0 98.5 ± 24.9

Fig. 4  Three-dimensional (3D) printed model for trochlea and plate model. (A) Plate design to fix the trochlea model. Rendered images of the
trochlea model: (B) isometric view, (C) upper view, and (D) frontal view. (E) Design parameters for trochlea prototype

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The International Journal of Advanced Manufacturing Technology

was matched for the implant as shown in Fig. 4E. The pic- oblique tenectomy [12], superior oblique tenotomy [13], and
tures of the 3D printed trochlea were in Supplementary a superior oblique tendon silicone expander [14]. Manipulat-
Fig. S1. ing the trochlea has generally been avoided due to the fear
of postoperative complications. However, Mombaerts et al.
[15] shifted the surgical target from the SOM tendon to the
4 Discussion trochlea. They introduced trochlear luxation surgery through
the upper eyelid crease incision. Kokubo et al. [16] per-
The primary role of the trochlea is to change the vector of formed trochlea reconstruction surgery using a step-cut and
the movements produced by the SOM and to act as a pulley. resuturing technique. In this regard, we considered expand-
When the eye moves upward and inward, the SOM normally ing the surgical concept from reconstruction to replacement
relaxes and the tendon passes smoothly through the trochlea. of the trochlea.
Any restriction in this passage will impair the elevation in The aim of the present study was to design a general-
adduction. Mechanical restriction of the trochlea has been ized trochlea model using a conventional micro-CT system
treated using various surgical procedures, including superior for future application in trochlea replacement therapy. The
most notable characteristic of the model is a posterolater-
ally directed flange that guides the reflected tendon of the
SOM (Fig. 5). We quantitatively assessed the inner and outer
radii of the trochlea after dividing it into its anterior and
posterior regions, and estimated the encountered angles of
O. We found that the trochlea has a unilateral asymmetric
shape: anterior part of trochlea always had a smaller anterior
radius than the posterior part of trochlea. We hypothesize
that there was no significant difference between the sizes of
the posterior radii of the medial and lateral part of trochlea,
indicating a bilateral symmetric shape.
The trochlea is located along the superomedial margin
of the orbit and is firmly attached to the bone. Our study
group previously demonstrated that the detailed location of
the trochlea is in the superomedial orbit. The results of that
study indicated that the superolateral tip of the trochlea was
located 15.8 mm superior and 1.6 mm lateral to the apex
of the lacrimal caruncle. It was also located 11.4 mm infe-
rior to the top of the supraorbital notch/foramen (Fig. 6).
Fig. 5  Illustration of the trochlea replacement in a cadaver (troch- These data of the exact location of the trochlea could be used
lea model was produced by replicating it to make it stand out). The together with the information of the structure of the trochlea
3D-printed trochlea was fixed to the superomedial orbit using the for future trochlea replacement surgery.
plate. The SOM passed through the inside of the trochlea and was
attached to the eyeball (a slit-like gap was made at the lateral portion The trochlea can only be palpated along the superome-
of the 3D printed trochlea so that the SOM could be inserted) dial margin of the orbit by highly skilled experts, because

Fig. 6  Trochlea location in the


superomedial orbit (reprinted
with permission).1 MCL, medial
canthal ligament; SOF, superior
orbital fissure; SON, superior
orbital notch

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The International Journal of Advanced Manufacturing Technology

it is small cartilaginous tissue. For this reason, its anat- 5 Conclusion


omy is not familiar to even strabismus surgeons. Virtual
and printed models are currently used for didactic and In this study, detailed 3D microstructure modeling of the
research purposes in other areas of medicine. These data trochlea was carried out using high-resolution CT scan-
and 3D-printed models can therefore potentially a valuable ning which is a powerful imaging technique. Fifteen
resource for teaching trochlea anatomy to medical students trochleae detached from periosteum of fifteen embalmed
and trainees, and for illustrating its 3D complexity [17]. cadavers were scanned by micro-CT, then segmentation
Tissue replacement has gradually become a common and image reconstruction were performed to obtain a final
operation, especially in orthopedic surgery. The increas- volume mesh in STL file. Five specified points for quan-
ing number of reports about 3D printing technology such tifying the scanned trochlea were suggested in the middle
as patient-specific implants play important roles in sup- cross section of trochlea to determine the generalized mod-
porting operations, especially in complex cases [18–20]. eling. The trochlea implant prototype was designed and
Although it is still at the primary stage, our novel mod- 3D printed for validation. The quantitative data presented
eling of a 3D-printed trochlea introduces a new concept of herein can potentially be used to create a 3D-printed troch-
trochlear surgery to clinicians and will expand our ability lea implant for patients with iatrogenic or posttraumatic
to understand structures. trochlear damage. Further studies are needed to determine
Even if a trochlea implant is constructed, in order for if these techniques will be safe and efficacious in clinical
the SOMs to move without damage after long periods, applications.
the material must be biocompatible and sufficient hard to
reduce friction. In this regard, 3D bioprinting is a promis- Supplementary Information  The online version contains supplemen-
tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 00170-0​ 23-1​ 1268-6.
ing approach for repairing cartilage tissue after damage
due to injury or disease, or to construct load-bearing con- Author contribution  HKK designed the study and wrote the manu-
nective tissue such as cartilage [21]. Therefore, in order for script. GBK and WL analyzed the data. WS and KS collect the data.
this technology to be realized in the future, development HJS designed the study and wrote the manuscript. AGL revised the
manuscript.
of cartilage tissue engineering needs to be followed based
on the availability of bioinks. Funding  This work was supported by the Konkuk University Medical
We have demonstrated that a standard 3D X-ray micro- Center Research Grant 2019 (No. 201911). This sponsor had no role
CT imaging technique can be used to measure human car- in the design or conduct of this research.
tilage with high precision and few accuracy errors. This is Data availability  Raw data table.
consistent with the study of Kim et al. [22], in which his-
tological grading systems for evaluating structures, cells, Declarations 
safranin-O staining, and tidemark integrity were compared
with 3D measurements of cartilage volume and thickness Conflict of interest  The authors declare no competing interests.
using micro-CT to provide complementary information.
One potential obstacle to using micro-CT is the high water
content of cartilage. Particularly in smaller samples, the
evaporation rate can be very high, and the subsequent References
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