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A New Method of Reconstructing the Human

Laryngeal Architecture Using Micro-MRI


*,‡Ting Chen, †Ann M. Chodara, †Alicia J. Sprecher, §Fang Fang, §Wen Song, †Chao Tao, and *,†Jack J. Jiang,
*Shanghai zFuzhou xNanjing, China, yMadison, Wisconsin

Summary: Objectives/Hypothesis. A realistic three-dimentional (3D) model of the larynx could be of value for
the understanding of normal laryngeal motion and for studying pathological changes as well as in modeling potential
therapy outcomes. The objective of this research was to present a new method of creating a computer model of the
human larynx using data obtained through micro-magnetic resonance imaging (MRI) scanning.
Study Design. Prospective study.
Methods. A 7-T micro-MRI scanner was used to scan an excised larynx obtained postmortem from a 68-year-old
woman. MRI data was manually segmented and compiled into 3D images using Mimics12.1 reconstruction software.
Measurements of the reconstructed structures were also calculated using Mimics12.1.
Results. The 3D laryngeal model contained the thyroid, cricoid, and arytenoid cartilages. Nearly all of the intrinsic
muscles could be segmented. Although the cricoarytenoid joint could be visualized, the features of the cricothyroid joint
were not clear. Muscle and cartilage volumes and surface areas were calculated from the 3D model.
Conclusions. The combination of MRI and 3D reconstruction generates promising results in the hopes of creating
a highly realistic and detailed model of the human larynx.
Key Words: Micro-MRI–3D reconstruction–Human larynx–Model.

INTRODUCTION data, yielding voxels with side lengths of 0.35 mm or


A better understanding of the anatomical and physical charac- 0.43 mm. Using the 2D images for segmentation, they created
teristics of the larynx is required to create realistic models with a 3D model using volume rendering; however, the field strength
true potential for research and clinical implementation. These and resolution were low, which led to inaccurate boundaries
features include the shape and relative positions of the laryngeal between both soft tissues and cartilages and within soft tissues
cartilages, intrinsic muscles, and ligaments. There are numer- themselves. Muscle segmentation was difficult and fiber num-
ous studies that report original data on laryngeal anatomy bers and directions could not be collected. Moreover, the clarity
obtained through gross anatomical examination of multiple of the cartilages, specifically the cricoid cartilage, decreased
specimens.1–4 However, it is difficult to combine the data near the edges of the scan.10
from such examinations into a complete three-dimensional The use of high-resolution MRI can generate a more accurate
(3D) model. Histological slicing has been used in other organ understanding of the volume, contours, and location of each
systems to create 3D reconstructions after two-dimensional component of the laryngeal framework. Ultrahigh magnetic
(2D) segmentation5; however, this method is problematic in la- field strengths (above 7 T) can provide submillimeter imaging
ryngeal modeling because different laryngeal tissues have dif- detail,11 approaching a spatial resolution of 0.04 mm and pixel
ferent deformation ratios during the slicing process, resolution of 15 mm at fields above 21 T.12 The signal-to-noise
obscuring the true anatomical shape. Computed tomography ratio increases almost linearly with the magnetic field13 and can
(CT) has also been used for laryngeal imaging and reconstruc- be used to improve resolution or decrease scan time.14,15
tion6–8 and in surgical planning,9 but CT is not able to clearly Ultrahigh-field MRI has great potential in an organ such as
reflect soft tissue. Models created using magnetic resonance im- the larynx with its small size and involved structures. In this
aging (MRI) are more successful because of its superior ability study, we used a 7-T micro-MRI scanner to obtain high-
to image soft tissue. Selbie et al.10 used a 2-T MRI to collect resolution scans of a freshly excised human larynx. Using
3D image processing and editing software, we generated a geo-
Accepted for publication March 29, 2011. metric 3D model for use in laryngeal biomechanical analysis.
Financial Disclosure Information: This research was supported by the Sina-America
Voice Research Center Project from the Ear, Eye, Nose and Throat Hospital of Fudan
University, Shanghai, China.
From the *Department of Otolaryngology, Eye, Ear, Nose and Throat Hospital, Fudan MATERIALS AND METHODS
University, Shanghai, China; yDepartment of Surgery, Division of Otolaryngology—Head
and Neck Surgery, University of Wisconsin School of Medicine and Public Health, Specimen
Madison, Wisconsin; zDepartment of Otolaryngology—Head and Neck Surgery, Fujian
Provincial Clinical College of Fujian Medical University, Fuzhou, China; and the
The Institutional Review Board of the Eye, Ear, Nose and
xKey Laboratory of Molecular and Functional Imaging, School of Medicine, Southeast Throat Hospital affiliated with the Fudan University in
University, Nanjing, China.
Address correspondence and reprint requests to Jack J. Jiang, Department of Surgery,
Shanghai, China approved and oversaw the protocol of this
Division of Otolaryngology, University of Wisconsin School of Medicine and Public investigation. A normal healthy larynx from a 68-year-old
Health, 5745 Medical Sciences Center, 1300 University Avenue, Madison 53706,
Wisconsin. E-mail: jjjiang@wisc.edu
woman was carefully dissected, postmortem. Immediately after
Journal of Voice, Vol. 26, No. 5, pp. 555-562 death, the cadaver was frozen and the tissue was thawed before
0892-1997/$36.00
Ó 2012 The Voice Foundation
excising the larynx. Heavy nylon sutures were used to suspend
doi:10.1016/j.jvoice.2011.03.012 the larynx within an acrylic cylinder for scanning (Figure 1).
556 Journal of Voice, Vol. 26, No. 5, 2012

FIGURE 1. Posterior (A), anterior (B), and lateral (C) views of the excised human larynx after dissection. All cartilages and intrinsic muscles were
maintained intact.

Micro-MRI scanning cricoarytenoid (CA) joint. Using manual segmentation, a 1:1 re-
Scanning was completed with a 7.0-T micro-MRI scanner construction was generated. The framework of the larynx was
(Bruker, Rheinstetten, Germany) with a 16-cm horizontal bore. constructed using surface rendering and Gaussian smoothing.
A volume coil of 61 mm diameter was used. A TurboRARE 3D
T2-weighted scanning sequence was used for axial scanning. In RESULTS
previous studies, we noted severe ghosting near the head and In this study, we found that micro-MRI of the laryngeal frame-
tail of the larynx because of the decreased magnetic signal mov- work provides an excellent anatomical depiction of its architec-
ing away from the isocenter. To remedy this, we scanned the ture. The regional muscles, laryngeal cartilages, and CA joint
specimen twice, once for the top half and once for the bottom were described. The interstitial fluids and spaces were useful in
half. Each scan used an echo time of 43.0 ms, a repetition determining the boundaries of the laryngeal components. We
time of 1000 ms, a flip angle of 180.0 , and a field of view of focused on the structural components known to be important in
4.50 3 4.50 3 3.20 cm with a slice thickness of 0.25 mm, with- phonation and potentially of use in future modeling experiments.
out intervals. The total imaging time for each scan was 2 hours
16 minutes 32 seconds with a number of excitations of 4 and Rigid body reconstruction
a matrix of 256 3 256 3 128. The final resolution was
Cartilages. From the sagittal, coronal, and transverse views,
175 3 175 3 250 mm per voxel. We combined the two sets of
we can clearly observe the features and spatial arrangements
images after scanning using Mimics12.1 software (The Materi-
of the six laryngeal cartilages: the thyroid, cricoid, and
alise Group, Leuven, Belgium).
epiglottis, and the paired arytenoids, corniculates, and cunei-
forms. As the specimen is from an older woman (68 years
3D reconstruction of age), cartilaginous ossification resulted in areas of the
The micro-MRI images were processed with Mimics12.1 to cre- cartilage that appear black in the MRI images. The first step
ate a 3D model of the larynx that included the thyroid, cricoid, in generating a 3D model consisted of manually tracing the
and arytenoid cartilages, internal laryngeal muscles, and the contours of the cartilages as shown in Figure 2. From these

FIGURE 2. MRI images from the sagittal (A), coronal (B), and transverse (C) planes, showing the tracing of cartilage boundaries for compilation
and 3D reconstruction. Outlined in yellow is the thyroid cartilage, in blue the arytenoids, and in lavender the cricoid cartilage.
Ting Chen, et al Micro-MRI and Modeling of the Larynx 557

FIGURE 3. 3D reconstruction of the thyroid (A), cricoid (B), and arytenoid (C) cartilages and their composite framework (D).

traces, we produced 3D reconstructions of the thyroid vex surface of the cricoid (B). Minimal joint space is visible in
cartilage, the arytenoids, and the cricoid cartilage and the MRI image; however, the capsular ligament (C) can be
combined these to create composite images showing the rela- seen to run from the posterior end of the joint through the inner
tive positions of these cartilages (Figure 3). Cartilage volumes surface connecting with the conus elasticus. By displaying the
and surface areas were calculated with Mimics12.1 (Table 1). cricoid and one arytenoid cartilage, we gain an impression of
To simplify our model and because of their limited involve- the joint, which is improved by generating a 3D model of the
ment in phonation, the epiglottis and the corniculate and
cuneiform cartilages were not reconstructed.
Joints. We examined the two of the major joints in the larynx:
the CA and cricothyroid joints. The two articulated cartilages of
the CA joint are shown in Figure 4. Evident are the concave
articular surface of the arytenoid (A) and the corresponding con-

TABLE 1.
Volume and Surface Area of Laryngeal Cartilages and
Conus Elasticus as Calculated by Mimics12.1
Surface Area
Tissues Volume (mm3) (mm2)
Thyroid cartilage 4196.97 3598.23
Cricoid cartilage 3513.53 2134.95
Arytenoid 206.62 (Left)/ 274.93 (Left)/ FIGURE 4. The CA joint shown from a sagittal view. Arrows indi-
cartilage 205.29 (Right) 272.60 (Right)
cate the articular surfaces of the arytenoid (A) and cricoid cartilages
Conus elasticus 2258.19 3254.15
(B). The capsular ligament (C) is shown in a lighter color.
558 Journal of Voice, Vol. 26, No. 5, 2012

FIGURE 5. The relationship of the CA joint and the conus elasticus. The conus elasticus travels around the medial and posterior borders of the joint.

capsular ligament (Figure 5). Unlike the CA joint, the articular ward, where it is contiguous with the inferior margin of the
surfaces, ligaments, and capsule of the cricothyroid joint are vocal ligament (Figure 6). The ligaments of the CA joint can
not readily visible on the MRI images and could not be be seen to join with the elastic membrane of the larynx, which
reconstructed. extends downward through the cricoid cartilage. Loose liga-
Ligaments. The ligaments of the larynx set the boundaries of ments such as the hyoepiglottic ligament were not well defined
the joints’ movement. With the high resolution provided by because of the higher concentration of fat near these ligaments.
micro-MRI, the primary outline of the elastic membrane is
well visualized and easily differentiated from the underlying Control component reconstruction
muscle. The conus elasticus can be traced as it connects the thy- Intrinsic muscles. Our MRI results showed excellent muscle
roid and cricoid cartilages. The lateral portion of the ligament boundaries and gave an estimate of fiber direction when that di-
arises from the inner surface of the cricoid arch and extends up- rection was parallel to the sagittal, coronal, or transverse axis.

FIGURE 6. In (A) arrows indicate the conus elasticus from the sagittal (left), coronal (middle), and a laterally shifted sagittal (right) view. (B) and
(C) show the conus elasticus (teal) in relation to the cartilage framework, the LP (white) and the thyroarytenoid muscle (light blue).
Ting Chen, et al Micro-MRI and Modeling of the Larynx 559

FIGURE 7. Segmentation of the intrinsic laryngeal muscles and LP on the right side. Evident are distinct boundaries between the posterior
CA (brown), lateral CA (salmon), cricothyroid (olive) and thyroarytenoid (light blue) muscles as well as the cartilages.

Figure 7 shows a series of images with laryngeal muscles high- models,16,17 which are created, mathematically speaking, by
lighted. Of note is the ease with which these muscles can be dif- a simplified reduction of the state space of the system to
ferentiated and the muscle fiber structure evident in many of the a finite number with no scientific visualization. Finite element
images. After muscles were traced on the 2D images, analysis, which uses simple geometry to approximately
Mimics12.1 was used to compile the 3D reconstructions shown simulate laryngeal posturing and biomechanics, has been used
in Figure 8. Muscle groups are clearly defined, and manipula- to develop laryngeal models.18,19 A limitation of these studies
tion of these groups and the underlying cartilages is simple. is that data were collected from invasive experiments
The model also provided volume measurements for each of involving individual muscles and layers and thus do not
the reconstructed muscles, shown in Table 2. reflect the true laryngeal architecture. Of course, the more we
know about the architecture of the larynx, the more reliable
Oscillation element reconstruction and valuable a computer model of the larynx will be for
Vocal fold and lamina propria. The micro-MRI images study. Modern imaging technology in combination with
showed a clear boundary between the lamina propria (LP) 3D reconstruction provides the means to produce a highly
and the vocalis muscle, which could be easily segmented realistic dynamic model of the human larynx.20 Models created
(Figure 9). The layers of the LP could not be identified; it using MRI have assisted in medical education,21 demonstrated
appears homogenous in the MRI images. The LP volume was interactions between laryngeal elements,22 and tested model
calculated and reported in Table 2. predictions by scaling an individual larynx to a reference frame-
work.10 Accurate models of the larynx show potential not just
DISCUSSION for research but for eventual clinical application in evaluating
Computer models are useful in exploring and estimating the per- laryngeal pathologies and treatments.
formance of systems too complex for analytical solutions, with In this study, we evaluated the feasibility of creating
one example being the dynamics of the larynx. Previously, com- a computer model of the human larynx. The use of micro-MRI
puter models of laryngeal dynamics have been lumped element provides true architectural information about the rigid body—
560 Journal of Voice, Vol. 26, No. 5, 2012

FIGURE 8. 3D composite images of the intrinsic laryngeal muscles showing their spatial location within the laryngeal framework (same colors as
indicated in Figure 7).

cartilages, joints, and ligaments; the control elements—the images.10 High-field MRI overcomes this limitation and appears
intrinsic muscles; and the oscillation elements—the vocal folds. to be an ideal tool for collecting data to complete a comprehen-
This technology allows visualization of structures not easily sive 3D reconstruction. The 7-T scanner allows a resolution of
evaluated using CT or ultrasound. As compared with traditional 175 3 175 3 250 mm voxels that results in clear enough images
gross anatomical observation or histological slicing, MRI pro- to complete excellent 2D segmentation and 3D reconstruction,
vides more accurate spatial information that can be translated which provide clear geometric data and boundary limitations
into a 3D model. In previous studies, the small details of the lar- for computer modeling.
ynx could not be completely described by low-resolution MRI As for the joint anatomy, the CA joint has been described as
a saddle-shaped synovial joint whose prominent capsule
ligament and articulated surfaces allow for three primary move-
ments: lateral-medial sliding, anteroposterior rocking, and
TABLE 2.
Volumes of Intrinsic Laryngeal Muscles and LP as
rotation. In our data, the conus elasticus wraps around the
Calculated by Mimics12.1 posterior and medial borders of the joint, allowing the lateral-
medial sliding and anteroposterior rocking, but limiting rotation
Left Volume Right Volume of the arytenoids, which is in accordance with previous
Tissues (mm3) (mm3) research.23 It is valuable to know the boundaries of the CA joint
Thyroarytenoid 862.75 851.56 for an accurate laryngeal computer model.
muscle Although the CT joint could not be well visualized in this
Posterior CA muscle 605.10 599.02 study, previous research has indicated that this joint can be di-
Cricothyroid muscle 586.11 566.61 vided into type A, with a well-defined facet, tight capsule, and
Lateral CA muscle 192.16 188.45
ligaments; type B, with no definable facet, only joined by
LP 95.65 92.34
loose soft connective tissue; and type C, with soft tissue facets
Ting Chen, et al Micro-MRI and Modeling of the Larynx 561

FIGURE 9. In (A, sagittal view) and (B, coronal view), arrows indicate the vocal fold LP. The LP was reconstructed in (C) and (D), which show the
relation of this layer (white) to the lateral cricoarytenoid (salmon) and thyroarytenoid muscles (light blue).

and a tiny thin capsular connection.24 This sample appears to Micro-MRI scanning data supply high enough resolution of
be of type B, which would explain the limited visualization of laryngeal components as to permit excellent 2D segmentation
the joint. From the images, the CT joint is evidently subject to for outstanding anatomic architecture reconstruction. More im-
more freedom of movement as compared with the CA joint. portantly, when combined with other MRI technology such as
A higher magnetic field reduces the scanning time needed to diffusion tensor imaging and tractography, it can noninvasively
record high-resolution data; however, for the extremely high- provide biomechanical data such as muscle motor unit anisot-
resolution images recorded in this study, the use of in vivo sam- ropy, tracking of muscle and nerve fiber paths in space, motor
ples is currently prevented by long scanning times, the small unit numbers, and so on.27,28 These technologies have the
core size and the impact of breathing, swallowing, and other potential to greatly change the traditional methodology in
random movements. Use of an excised larynx provides accurate biological computer modeling and supply a whole new style
architectural data while conveniently avoiding these issues. The of laryngeal dynamic computer simulation. Anatomic
larynx used in this study came from a 68-year-old woman. architecture reconstruction as achieved in this study is the
Despite the ossification associated with the individual’s ad- first step in this novel method.
vanced age, cartilage contours remained well defined. Success-
ful 3D reconstruction provides the possibility of computerized
study of variations in laryngeal dynamics because of age, sex, CONCLUSION
and pathology and even among individuals. The present study proposes a new method of creating
Additionally, a limitation observed in this study was in the vi- a computer model of the larynx. High-resolution data from
sualization of the LP. Although the entire LP was easily seg- micro-MRI noninvasively provide a visual representation of
mented from the vocalis muscle, divisions within the LP were the real anatomical structure and spatial relationship of laryn-
not evident. The division of the LP into three layers is based geal components. It supplies true geometric information and
on the distribution and ratio of elastic and collagen fibers.25 boundary limitations for the successful completion of a compa-
At 7 T, the LP appears to be homogenous and cannot be divided rable dynamic model for use in physical and pathophysiological
into layers. In a recent study,26 an 11.7-T micro-MRI was used research. In the future, such a model may also be useful in the
to observe vocal fold tissues in excised ferret and canine laryn- evaluation of possible therapies for laryngeal disorders.
ges. Even with this strong magnetic field and a voxel side length
of 39 mm in the principal plane, the LP layers were not visible.
Although there may be subtle differences in the LP structure be-
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