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bioengineering
Technical Note
Computer-Guided Bone Biopsy: A Technical Note with the
Description of a Clinical Case
Federica Altieri 1, * , Giovanna Iezzi 2, Valeria Luzzi 1, Gianni Di Giorgio 1, Antonella Polimeni 1
and Michele Cassetta 1
Citation: Altieri, F.; Iezzi, G.; Luzzi,
V.; Di Giorgio, G.; Polimeni, A.;
Cassetta, M. Computer-Guided Bone
Biopsy: A Technical Note with the
Description of a Clinical Case.
Bioengineering 2021,8, 214.
https://doi.org/10.3390/
bioengineering8120214
Received: 19 November 2021
Accepted: 11 December 2021
Published: 15 December 2021
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1Department of Oral and Maxillofacial Sciences, School of Dentistry, “Sapienza” University of Rome,
00100 Rome, Italy; valeria.luzzi@uniroma1.it (V.L.); gianni.digiorgio@uniroma1.it (G.D.G.);
antonella.polimeni@uniroma1.it (A.P.); michele.cassetta@uniroma1.it (M.C.)
2Department of Medical, Oral, Biotechnological Sciences, University “G. d’Annunzio” of Chieti-Pescara,
66100 Chieti, Italy; giovanna.iezzi@unich.it
*Correspondence: federica.altieri@uniroma1.it; Fax: +39-06-501-6612
Abstract:
Aim: The aim of this technical note is to present a computer-aided design–computer-aided
manufacturing (CAD–CAM) surgical guide to perform a computer-guided bone biopsy. Traditionally,
to diagnose abnormal conditions affecting jawbone, a bone biopsy is performed with the use of a
trephine bur. The positioning of the bur, during the biopsy, is based on the skill of the surgeon;
therefore, an inaccurate placement of a trephine bur may occur. The use of a guide, however, can
minimize this risk and achieve a better result. Materials and Methods: To determine the site and the
extension of bone sampling, the stereolithography file (STL) file of cone–beam computed tomography
(CBCT) images is acquired using a specific planning software and superimposed with the STL file
of a dental cast; a virtual surgical guide is designed, using the same software that allows a 3D
(three-dimensional) view of the guide from different perspectives and planes. The number and site
of guide tubes are determined on the basis of the width and the extension of the sampling; thanks to
a 3D printer, the surgical guide is manufactured. Results: The use of a customized surgical guide
realized with CAD–CAM technology allows a precise and minimally invasive approach, with an
accurate three-dimensional localization of the biopsy site. Conclusions: The high precision, great
predictability, time-effectiveness and versatility of the present guide should encourage the clinician
to use this minimally invasive surgical approach, but controlled clinical trials should be conducted to
evaluate the advantages as well as any possible complications.
Keywords: biopsy; computer-assisted surgery; CAD-CAM; CBCT; oral surgery; digital planning
1. Introduction
An accurate diagnosis and treatment of oral disease is an essential component of the
patient’s comprehensive dental care and the foundation of high-quality dentistry. Few
bony abnormalities can be accurately diagnosed based on their radiographic features [
1
].
Confirmatory diagnosis may require a biopsy and microscopic examination [
2
]. In current
dental practice, the reconstruction of cranial and maxillofacial defects is made through the
use of bone grafting. This is a surgical procedure that replaces missing bone with autolo-
gous bone, or with an artificial, synthetic, or natural substitute [
3
]. The most common use
of bone grafting is in implant-supported rehabilitation, in order to restore the edentulous
area of a missing tooth [
3
]. Once the transplanted bone is secured into its new location,
the blood supply is generally restored to the bone on which it is attached. To evaluate
the graft histology characteristics a bone biopsy is necessary [
2
]. Today, the most precise
imaging to perform a thorough evaluation of the maxillary bone structure is cone-beam
computed tomography (CBCT), which provides high spatial resolution, accessibility and a
lower radiation dosage compared to computed tomography (CT) [4,5].
Bioengineering 2021,8, 214. https://doi.org/10.3390/bioengineering8120214 https://www.mdpi.com/journal/bioengineering
Bioengineering 2021,8, 214 2 of 9
The aim of the present technical note is to describe a computer-aided design–computer-
aided manufacturing (CAD-CAM) surgical-guide procedure used to perform a bone biopsy
after a previous bone graft; a single case of guided bone biopsy with subsequent implant
insertion is described.
2. Materials and Methods
The present procedure, used at the Department of Oral and Maxillo-Facial Sciences
of “Sapienza” University of Rome, allows jawbone biopsy employing a surgical guide
realized with at least one tube that guides a trephine bur to enable accurate bone sam-
pling of the maxillary and/or mandibular bone. The realization of the present surgical
template requires:
•
The determining of bone sampling site and extension. For this purpose, DICOM
(Digital Imaging and Communications in Medicine) files of CBCT are acquired using
specific planning software and a superimposition of a 3D (three-dimensional) scan
of the cast model (Easy Optical3D Scanner, Open Technologies, Rezzato, BS, Italy) is
performed after uploading the corresponding STL file (stereolithography file);
•
The design of a virtual surgical guide through CAD software that allows a view of the
3D guide from different perspectives and planes; the number and site of guide tubes
are determined on the basis of the width and the extension of the sampling;
•
The surgical guide printing, thanks to a 3D printer (Stratasys OrhoDesktop, Eden
Praire, MN, USA).
3. Description of a Computer-Guided Biopsy
3.1. Manufacturing the Surgical Guide
In a young adult patient with the need for prosthetic rehabilitation of the maxillary
arch, due to multiple dental agenesis, the initial phase of treatment involved a split crest
procedure using autologous bone grafting. In order to achieve an adequate implant,
osseointegration and a successful treatment outcome from both functional and aesthetic
points of view are required, as is a good dental emergence profile. Equally, to obtain a
correct prosthetic rehabilitation [
6
] it is important to have at least 2 mm of width around
the implant bone crest at the buccal and palatal planes. Intra-oral tissues (mandibular
branch) or the extra-oral tissues (e.g., iliac crest bone) grafts usually led to good results,
but they are invasive and complications cannot be excluded, such as additional surgical
procedures [
6
]. To find an alternative solution in such cases, techniques for crest expansion
using bone expanders or osteotomes, or “split-crest” (SCT) performed with an ultrasound
device or with conventional surgery have been proposed [
7
]. The “split-crest” technique
consists of splitting the vestibular and oral cortical bones, displacing the vestibular cortical
bone in either the maxillary or mandible bone and separating it from the bone marrow and
creating a middle gap, which is usually occupied mostly by the inserted implants. The
space unoccupied by the implants can be filled with biomaterials such as autologous bone
grafts, particulate bone, or plasma derivatives, such as platelet-rich plasma [7].
The surgical sites were assessed by a clinical intraoral examination, panoramic and
periapical radiographs. The split crest criteria were used for the patient’s evaluation: (1) a
minimal horizontal bone width of 2 mm; (2) a minimal vertical bone height of 10 mm; (3) no
concavity in alveolar bone profile; and (4) the horizontal osteotomies had to end at least
1 mm distance from the neighboring teeth [
8
]. A CT was requested for a 3D pre-operative
evaluation to determine the presence of an alveolar width of at least 2 mm and the absence
of a concavity. A staged rehabilitation approach was planned given that the two-stage
ridge split usually has a higher implant success rate when the ridge width is lower than
5 mm after splitting [
9
]. After local anesthesia (Optocain
®
-Molteni Dental-Italia), a full
thickness crestal incision extended buccally and palatally was made with vertical divergent
releasing incisions extended into the vestibule. A mucoperiosteal flap was elevated, and
the bone ridge was exposed. The cortical bone was initially curetted, to remove all residual
connective tissue and periosteum, then, using a piezoelectric scalpel, a horizontal incision
Bioengineering 2021,8, 214 3 of 9
was made in the middle of the ridge with two releasing incisions, one mesial and one
distal. The horizontal osteotomies were performed at a distance of at least 1 mm from the
neighboring teeth. The alveolar ridge was split longitudinally in two parts, provoking a
greenstick fracture using a 4 mm straight osteotome (Hu-Friedy Mfg. Co., Chicago, IL,
USA). The straight osteotome was gently tapped on with a hammer to create a fine cut
longitudinal to the crest. The osteotome was then used as a lever to spread apart the two
cortical plates. The surgical fracture was extended to a depth of 10 mm. Many attempts
were made to avoid sharp and complete vertical or horizontal fractures of the buccal and
palatal bone plates. After a crestal incision, bone from the retromolar trigone was harvested
using a trephine (4
×
6 mm) and then fragmented into particles (bone chips). The bone
defect obtained by the separation of the bone segments was filled with bone chips, which
were condensed in the space between the buccal and palatal bone plates with the aim
of completely filling the space (Figure 1). The mucoperiosteal flap was sutured using
tension-free single sutures (GORE–TEX, W.L.Gore and Associates, Inc., Flagstaff, AZ, USA).
Suture removal was performed 10 days after the surgical procedure. A reduced implant
placement time approach in the staged rehabilitation was used [
10
]. After a healing period
of 2 months, a computer-guided implant surgery was carried out. During the computer-
guided procedure a bone graft sample was harvested thanks to a computer-guided biopsy
(Figure 2). A dedicated CAD software ( 3Shape Implant Studio
®
, Srl Milam, Italy ) was
used to plan the number, the length and the diameter of dental implants as well as the
dimensions of trephine bur to be used (Figure 3). A software application allowed the design
of the surgical guide (3Shape Implant Studio
®
) printed with a 3D printer (3D Stratasys
OrthoDesktop) (Figure 2A). In the present case two surgical guides were realized with
a total of 5 tubes. Since the diameter of the tubes is larger than that of the drills and the
implant, in some cases it is necessary to utilize two guides to hold two contiguous pipes.
Bioengineering 2021, 8, x FOR PEER REVIEW 3 of 9
connective tissue and periosteum, then, using a piezoelectric scalpel, a horizontal incision
was made in the middle of the ridge with two releasing incisions, one mesial and one
distal. The horizontal osteotomies were performed at a distance of at least 1 mm from the
neighboring teeth. The alveolar ridge was split longitudinally in two parts, provoking a
greenstick fracture using a 4 mm straight osteotome (Hu-Friedy Mfg. Co., Chicago, IL,
USA). The straight osteotome was gently tapped on with a hammer to create a fine cut
longitudinal to the crest. The osteotome was then used as a lever to spread apart the two
cortical plates. The surgical fracture was extended to a depth of 10 mm. Many attempts
were made to avoid sharp and complete vertical or horizontal fractures of the buccal and
palatal bone plates. After a crestal incision, bone from the retromolar trigone was har-
vested using a trephine (4 × 6 mm) and then fragmented into particles (bone chips). The
bone defect obtained by the separation of the bone segments was filled with bone chips,
which were condensed in the space between the buccal and palatal bone plates with the
aim of completely filling the space (Figure 1). The mucoperiosteal flap was sutured using
tension-free single sutures (GORE–TEX, W.L.Gore and Associates, Inc., Flagstaff, AZ,
USA). Suture removal was performed 10 days after the surgical procedure. A reduced
implant placement time approach in the staged rehabilitation was used [10]. After a heal-
ing period of 2 months, a computer-guided implant surgery was carried out. During the
computer-guided procedure a bone graft sample was harvested thanks to a computer-
guided biopsy (Figure 2). A dedicated CAD software ( 3Shape Implant Studio®, Srl Milam,
Italy ) was used to plan the number, the length and the diameter of dental implants as
well as the dimensions of trephine bur to be used (Figure 3). A software application al-
lowed the design of the surgical guide (3Shape Implant Studio®) printed with a 3D printer
(3D Stratasys OrthoDesktop) (Figure 2A). In the present case two surgical guides were
realized with a total of 5 tubes. Since the diameter of the tubes is larger than that of the
drills and the implant, in some cases it is necessary to utilize two guides to hold two con-
tiguous pipes.
Figure 1. (A) Bone harvest from the retromolar trigone with the use of a trephine (4 × 6 mm) bur;
(B) a detail of the bone sampling site; (C) the bone defect obtained by the separation of the bone
segments is filled with bone chips, which were condensed in the space between the buccal and pal-
atal bone plates with the aim of completely filling the space; (D) a detail of the bone graft.
Figure 1.
(
A
) Bone harvest from the retromolar trigone with the use of a trephine (4
×
6 mm) bur;
(
B
) a detail of the bone sampling site; (
C
) the bone defect obtained by the separation of the bone
segments is filled with bone chips, which were condensed in the space between the buccal and palatal
bone plates with the aim of completely filling the space; (D) a detail of the bone graft.
Bioengineering 2021,8, 214 4 of 9
Bioengineering 2021, 8, x FOR PEER REVIEW 4 of 9
It was not possible to design a single surgical guide due to the limited space in the
dental arch and the size of the tubes. The tubes guided the trephine bur as well as the
implants into their planned positions. Using dedicated sleeves of different diameters, it
was possible to guide, first, the trephine bur and then the implant drills and the implant
mounting devices. Bone cores were harvested using a 3.5 × 10 mm diameter trephine bur
under saline solution irrigation and processed for histology. Every guide had different
tubes called “master tubes” embedded within the acrylic resin surgical guide; the master
tubes had cylindrical walls and wings to prevent their rotation and to provide greater
mechanical strength. To adapt the master tube to the trephine bur, to the implant drills
and also to the mounting devices, removable sleeves were used. The removable sleeves
have a variable inner diameter that permits the accommodation of the biopsy trephine
bur, the implant drills, and the implant mounting devices.
The tooth-supported surgical guide was constructed with a 3D printer (3D Stratasys
OrthoDesktop).
Figure 2. (A) The tooth-supported surgical guide positioned in the upper arch; (B) a detail of the
biopsy trephine bur.
Figure 2.
(
A
) The tooth-supported surgical guide positioned in the upper arch; (
B
) a detail of the
biopsy trephine bur.
It was not possible to design a single surgical guide due to the limited space in the
dental arch and the size of the tubes. The tubes guided the trephine bur as well as the
implants into their planned positions. Using dedicated sleeves of different diameters, it
was possible to guide, first, the trephine bur and then the implant drills and the implant
mounting devices. Bone cores were harvested using a 3.5
×
10 mm diameter trephine bur
under saline solution irrigation and processed for histology. Every guide had different
tubes called “master tubes” embedded within the acrylic resin surgical guide; the master
tubes had cylindrical walls and wings to prevent their rotation and to provide greater
mechanical strength. To adapt the master tube to the trephine bur, to the implant drills and
also to the mounting devices, removable sleeves were used. The removable sleeves have a
variable inner diameter that permits the accommodation of the biopsy trephine bur, the
implant drills, and the implant mounting devices.
The tooth-supported surgical guide was constructed with a 3D printer (3D Stratasys
OrthoDesktop).
Bioengineering 2021,8, 214 5 of 9
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Figure 3. (A) Virtual implant planning of 1.2 on the 3-Shape Implant Studio software; (B) planning
of implant position in the canine area [1.3].
3.2. Specimen Processing
A total of four bone cores, corresponding to the four implant sites planned in the
grafted bone tissue, were retrieved and immediately stored in 10% buffered formalin. The
specimens were processed using the Precise 1 Automated System (Assing, Rome, Italy).
The specimens were dehydrated in a graded series of ethanol rinses and embedded in a
glycolmethacrylate resin (Technovit, Kulzer, Wehrheim, Germany). After polymerization,
the specimens were sectioned, along their longitudinal axis, with a high-precision dia-
mond disk at about 150 lm and ground down to about 30 lm with a specially-designed
grinding machine. Two slides were obtained from each specimen. These slides were
stained with acid fuchsin and toluidine blue and examined with transmitted light Leitz
Laborlux microscope (Leitz, Wetzlar, Germany). Histomorphometry of the percentages of
newly formed bone, residual grafted material, and marrow spaces was carried out using
a light microscope (Leitz) connected to a high-resolution video camera (3CCD, JVC KY-
F55B, JVC, Yokohama, Japan) which interfaced with a monitor and PC (Intel Pentium III
1200 MMX, Intel, Santa Clara, CA, USA). This optical system was associated with a digit-
izing pad (Matrix Vision GmbH, Oppenweiler, Germany) and a histometry software pack-
age with image capturing capabilities (Image-Pro Plus 4.5; Media Cybernetics Inc., Im-
magini & Computer SncMilano, Italy).
Figure 3.
(
A
) Virtual implant planning of 1.2 on the 3-Shape Implant Studio software; (
B
) planning
of implant position in the canine area [1.3].
3.2. Specimen Processing
A total of four bone cores, corresponding to the four implant sites planned in the
grafted bone tissue, were retrieved and immediately stored in 10% buffered formalin. The
specimens were processed using the Precise 1 Automated System (Assing, Rome, Italy).
The specimens were dehydrated in a graded series of ethanol rinses and embedded in a
glycolmethacrylate resin (Technovit, Kulzer, Wehrheim, Germany). After polymerization,
the specimens were sectioned, along their longitudinal axis, with a high-precision diamond
disk at about 150 lm and ground down to about 30 lm with a specially-designed grind-
ing machine. Two slides were obtained from each specimen. These slides were stained
with acid fuchsin and toluidine blue and examined with transmitted light Leitz Laborlux
microscope (Leitz, Wetzlar, Germany). Histomorphometry of the percentages of newly
formed bone, residual grafted material, and marrow spaces was carried out using a light
microscope (Leitz) connected to a high-resolution video camera (3CCD, JVC KY-F55B, JVC,
Yokohama, Japan) which interfaced with a monitor and PC (Intel Pentium III 1200 MMX,
Intel, Santa Clara, CA, USA). This optical system was associated with a digitizing pad
(Matrix Vision GmbH, Oppenweiler, Germany) and a histometry software package with
image capturing capabilities (Image-Pro Plus 4.5; Media Cybernetics Inc., Immagini &
Computer SncMilano, Italy).
Bioengineering 2021,8, 214 6 of 9
3.3. Histological Results
At low magnification, trabecular bone with small and large marrow spaces was
observed (Figure 4). The coronal portion of the alveolar bone, after split crest, was evident.
In this portion the preexisting trabecular bone with small marrow spaces was in contact
to many remodeling and new bone formation areas. Moreover, some residual autologous
bone particles, which probably underwent a process of remodeling ending up in their
replacement with new bone, could be detected (Figure 5). Instead, the apical portion of the
bone core was characterized by newly trabecular bone and residual grafted particles, lined
by newly formed bone, which showed the features of a recently formed tissue, such as
wide osteocyte lacunae, high staining affinity, the presence of osteoblasts and the osteoid
matrix’s undergoing mineralization. In many areas the collagen matrix undergoing a
remodeling process was present. In the marrow spaces there were some blood vessels
close to the newly formed bone and the biomaterial particles (Figure 6). Inflammation and
multinucleated giant cells were absent. Histomorphometrical analysis showed that the
percentage of newly formed bone was 22.8%, marrow spaces 60.1% and residual grafted
material 17.1%.
Bioengineering 2021, 8, x FOR PEER REVIEW 6 of 9
3.3. Histological Results
At low magnification, trabecular bone with small and large marrow spaces was ob-
served (Figure 4). The coronal portion of the alveolar bone, after split crest, was evident.
In this portion the preexisting trabecular bone with small marrow spaces was in contact
to many remodeling and new bone formation areas. Moreover, some residual autologous
bone particles, which probably underwent a process of remodeling ending up in their
replacement with new bone, could be detected (Figure 5). Instead, the apical portion of
the bone core was characterized by newly trabecular bone and residual grafted particles,
lined by newly formed bone, which showed the features of a recently formed tissue, such
as wide osteocyte lacunae, high staining affinity, the presence of osteoblasts and the oste-
oid matrix's undergoing mineralization. In many areas the collagen matrix undergoing a
remodeling process was present. In the marrow spaces there were some blood vessels
close to the newly formed bone and the biomaterial particles (Figure 6). Inflammation and
multinucleated giant cells were absent. Histomorphometrical analysis showed that the
percentage of newly formed bone was 22.8%, marrow spaces 60.1% and residual grafted
material 17.1%.
Figure 4. At low magnification, two areas with different features are observed: the coronal one,
characterized by trabecular bone with small marrow spaces; and the apical, where autologous bone
particles surrounded by new bone can be seen (toluidine blue and acid fuchsin 9×).
Figure 4.
At low magnification, two areas with different features are observed: the coronal one,
characterized by trabecular bone with small marrow spaces; and the apical, where autologous bone
particles surrounded by new bone can be seen (toluidine blue and acid fuchsin 9×).
Bioengineering 2021,8, 214 7 of 9
Bioengineering 2021, 8, x FOR PEER REVIEW 7 of 9
Figure 5. Trabecular bone with small marrow spaces. In some areas bone particles undergoing remodeling process were
detected (toluidine blue and acid fuchsin 40×).
Figure 6. In the apical portion several residual biomaterial particles lined by new bone are found.
In the marrow spaces there are many blood vessels close to the newly formed bone and the bio-
material particles (toluidine blue and acid fuchsin 100×).
Figure 5.
Trabecular bone with small marrow spaces. In some areas bone particles undergoing
remodeling process were detected (toluidine blue and acid fuchsin 40×).
Bioengineering 2021, 8, x FOR PEER REVIEW 7 of 9
Figure 5. Trabecular bone with small marrow spaces. In some areas bone particles undergoing remodeling process were
detected (toluidine blue and acid fuchsin 40×).
Figure 6. In the apical portion several residual biomaterial particles lined by new bone are found.
In the marrow spaces there are many blood vessels close to the newly formed bone and the bio-
material particles (toluidine blue and acid fuchsin 100×).
Figure 6.
In the apical portion several residual biomaterial particles lined by new bone are found. In
the marrow spaces there are many blood vessels close to the newly formed bone and the biomaterial
particles (toluidine blue and acid fuchsin 100×).
Bioengineering 2021,8, 214 8 of 9
4. Discussion
Given the differences in treatment and prognosis for many bony entities, the iden-
tification of these lesions mandates biopsy. When radiological findings in the maxillary
and mandible bones require a histopathological examination for the correct diagnosis,
computer-guided biopsy can be used. Further treatment, if necessary, will then be dictated
by the definitive histopathologic diagnosis. The guide described in this note can be used for
many purposes: not only to guide the bone biopsy but also the implant site preparation and
the implant insertion [
11
]. This new technique allows both bone harvesting and implant
insertion to be performed at the same time. Bone sampling and subsequent histological
analysis allow us to evaluate the results obtained following bone regeneration. This tech-
nique can also be extremely useful in case of research aimed at comparing the images of a
CT or CBCT with the corresponding anatomical structure, allowing the clinician to obtain
a match between the radiological and the histological images. This technique can be used
even if no implants have to be inserted, i.e., it can be used to perform solely the biopsy. The
surgical guide can be tooth-, bone- or mucosa-supported.
The present computer-guided biopsy seems to have many advantages: a precise and
reliable biopsy sampling, a reduced surgical time, and safety of the anatomical structures.
As this procedure is flapless and minimally invasive, it reduces the post-operative discom-
fort; in addition, it is a safe method to prevent neurological damage in complex anatomical
regions with proximity to nerve branches. On the other hand, this procedure requires the
use of dedicated software and the construction of a surgical guide is expensive.
Moreover, considering the results of a recent study aimed to determine the presence
of a learning curve in static computer-assisted surgery (s-CAS), it would seem possible to
obtain predictable results in terms of accuracy from the beginning, using a CAD–CAM
surgical template. In fact, s-CAS it is not characterized by a typical “learning curve” [12].
5. Conclusions
In conclusion, the high precision, great predictability, time-effectiveness and versatility
of the present guide should encourage the clinical use of this minimally invasive surgical
approach, but controlled clinical trials should be conducted to evaluate the advantages of
the current method concerning treatment time and patient discomfort, as well as possible
complications.
Author Contributions:
F.A.: conception and design, acquisition of data, drafting and revising of
the manuscript; G.I.: performed the histological and manuscript final approval; V.L.: acquisition
of data, drafting and revising of the manuscript; G.D.G.: drafting and revising of the manuscript;
A.P.: revising of the manuscript and manuscript final approval; M.C.: conception and design
and manuscript final approval. All authors have read and agreed to the published version of
the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement:
The study was examined and approved by the Ethics Com-
mittee of the “Umberto I” Universital Hospital of Rome, Italy (protocol code: #4871 date of approval
05/02/2018).
Informed Consent Statement:
Patient consent was obtained to the treatment and to publish the
clinical intraoral photographs.
Data Availability Statement: The study did not report any data.
Conflicts of Interest: No conflict of interest.
Bioengineering 2021,8, 214 9 of 9
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