1. April 2018Volume 44, Issue 4, Pages 536–
Dario Di Nardo, DDS,* Gianluca Gambarini, MD,* Silvia Capuani, PhD,†
and Luca Testarelli, DDS, PhD*
2. Significance of this study
Potentially, MRI can reproduce not only hard and soft dental
and periodontal tissues, but it can also differentiate their
peculiar attributes in pathological and nonpathological
conditions. Peculiar anatomical aspects, such as the presence
of lateral canals or microcracks, can be visualized.
3. Introduction
Theimages of the
human skull are
currently
acquired by,
computed tomographic
(CT)
cone-beam computed
tomo- graphic (CBCT)
magnetic resonance
imaging (MRI) devices
4. MRI Originally called 'NMRI' (nuclear magnetic resonance imaging)
and is a form of NMR.
The use of 'nuclear' in the acronym was dropped to avoid negative
associations with the word.
Isnoninvasive andhelp indiagnosingofsofttissue diseases withoutusing
ionizingradiation.
It is almost comparable withCBCTimagingin termsofspatialresolution
-offersthepossibilitytovisualizedata in cross-sectionaland panoramic views
more familiar to dentists.
5. This review
Analyzes the increasing role of magnetic resonance imaging (MRI) in
dentistry and its relevance in endodontics.
•
Assess the Limits and new strategies to develop MRI protocols for
endodontic purposes are reported and discussed
•
7. Materials and Methods
A search for original articles on dental MRI was performed using
PubMed electronic databases.
322 articles were screened
Only 38 studies were included
8. Only articles on the
following,
investigated by the
use of
in vitro and in vivo
MRIwere included.
dental
anatomy,
endodontics
dental
structures,
Articles on joint disorders, orthodontics, and prosthetics
not concerning dental and root anatomy
9. Results
Dental MRI is capable of obtaining a well-defined image of
dental structures like enamel, dentin, pulp, and periodontal tissues.
Dental MRI can also recognize pathologIcal conditions such
as decay, microcracks, and necrotic pulp tissues,
It can differentiate solid like periapical periodontitis from a cystic
lesion because of its capacity to discriminate hydrated tissues.
10. Discussion
MRI is based on nuclear magnetic resonance (NMR) spectroscopy whereby
an electromagnetic field in the radiofrequency (RF) range is used to
stimulate the spins of hydrogen nuclei that are immersed in a strong
magnetic field (B0).
The resonance refers to the change in energy states of the nuclei
in response to a specific radio frequency.
Resonance can also occur in external magnetic field.
Only criteria : must have odd number of protons or neutrons
Main resonating body in humans is H
11. Because of nuclear paramagnetism, these spins align themselves parallel and
antiparallel to the B0 direction.
The most numerous spin population with the same orientation to the B0
generates the macroscopic magnetization(M0).
12. The Radio Frequency stimulation moves the magnetization M0 from the
direction parallel to B0 to the direction perpendicular to B0.
13.
14. Whenthe spins of the hydrogen nuclei are no longer
stimulated
theyreturn to theirinitialposition
creating signals that are received by the RFprobe
as electromotiveforce.
Theacquired signal decaysexponentiallyin
time
are quantified bythe parametersT2(spin-spin
relaxation)and T1(spin-latticerelaxation)
15. • the signal is characterized by a
unique frequency response that
provides physical-chemical
information about the investigated
tissues.
• Superimposing over the main
magnetic field time-dependent and
controlled magnetic field gradients,
images are obtained similarly to
computed tomographic scanners.
16. • By manipulating the length and shape of the RF pulses that
excite the nuclear spins---
the direction and strength of the field gradients,
a specific plane
volume of interest can be selected in differentorientations.
17. • 3DMRIscan is composedofseveral 2-dimensionalimages ofa selected thickness.
• NMR signals are processed by a computer that constructs the MRI images
(essentially a map of the spatial distribution of hydrogen nuclei) using algorithms
based on the Fourier transform .
18. Theimage resolution is quantified bythe image voxelsize.
The provides the in-plane resolution of the image,
The is determined by theslice thickness of each bidimensional image.
Image resolution depends on magnetic gradients’strength of imaging gradients.
Image Resolution
19. Signal-to-noise Ratio (SNR) and Image Resolution
SNR is measured by calculating the ratio between the signal intensity in an area of interest
and the standard deviation of the signal from the background (in an area chosen from the
object).
SNR volume of the voxel
the square root of the number of averages (NA).SNR
20. In MRI, SNRcan be improved by
increasing the voxelsize,
reducing the bandwidth using surface coils,
using an echo time (TE) of spin-echo sequence as short as possible, and
increasing the number of signal acquisitions(NA).
In particular, the voxelsize can be increased by
increasing the field of view(FOV),
decreasing the matrix size, and
increasing the slice thickness.
21. Radiation Frequency (RF) and Imaging Gradient Coils
Agood strategy to reduce FOVfor increasing the image resolution without lowering the
SNRis to use dedicated RF coils.
Head or neck coils cannot reach the resolution needed for practical dental applications.
Extraoral placement of the coil can result in images that will contain more signals from
less important tissues such as the fat of the cheek..
RF
coils
22. Intraoral positioning of the RFcoil mayincrease both resolution and SNR,
but it can be difficult to implement because of anatomic structures such as tori and
frenula that will prevent the most distal elements or root tips of the teeth from appearing
in the acquired volume.
One of the most comfortable coil positions was proposed by Idiyatullin et al (8), who
explained the advantages of using a loop coil in the occlusal position for
dental applications.
Thecoil’s shape is similar to an impression tray,
it can be kept in the mouth between dental arches .
Thehigh patient comfort
The increased signal sensitivity
23. Artifacts
Astudy on the affection of dental materials on the NMRsignal showed that
composites, amalgam, gold, and nickel-titanium alloys can produce relatively strong
artifacts;
stainless steel brackets or wires can produce voids in the signal.
Glass ionomer cement, gutta-percha, zirconium dioxide, and some composites appear
to be fully compatible with MRI because they can be present even in the tooth of
interest without creating significant artifacts.
Polycarboxylate, zinc phosphate–based cement, and some modified di- methacrylates
can also produce small image artifacts(7).
24. Technical Issues
TheNMRsignal decays over time because of the
spin-spin relaxation, quantified by the parameter T2, indicating how quickly
the signal is canceled (goes to 0).
the spin-lattice relaxation, quantified by the time constant T1, indicating
how quickly the system returns to the initial equilibrium state (ie, the one it had before
absorbing RF).
Conventional MRI performed with clinical scanners is characterized by hardware and
software to acquire signals withT2higher than 2 milliseconds.
Because T2 relaxation time of human enamel runs from about 14 to 61
microseconds and in mineralized dentin
25. PULP AND PERIODONTAL TISSUES, which are
soft tissues and therefore more hydrated, will be
acquired properly and appear white or gray in the
NMRimage.
Mineralized tissues such as DENTIN AND
ENAMEL will result in a black zone because of the
impossibility of capturing their signals bythe device.
cortical bone can be identified as a black
zone outlined by a moderate signal from
external soft tissues.
26. MRI Diagnosis of Dental Caries
Microscopic MRI seems to be well suited to studying the development of dental
caries;
It is nondestructive and noninvasive,
Does not use ionizing radiation, and
Leaves tissues available for further investigations
the enlargement of
mineralized tissue
porosity, which extends
the T2 of spin protons
contained in the carious
lesion
local acid accumulation
caused by bacterial
inflammation
tissue
demineralization
penetration of saliva
breakdown of the
mineral structure
results in an increased
local proton density
27. Figure 1.Axial (A–D) MRI and (E–G) CBCTimages of a decayed extracted tooth. NMRimages are T2-weighted images obtained by
using a 9.4-T magnetic field, a multislice multiecho sequence with TE = 3 milliseconds, a repetition time = 5000 milliseconds, a slice
thickness of each image slice = 0.5 mm, and an in-plane resolution of 62 × 62 mm2
. Red arrows indicate a carious
lesion affecting the interproximal surface. The transition zone (Tz) between the sound dentin
(D) and the carious lesion (C) is visible (green arrows). The shape of the endodontic canal
(Ec) and the periodontal remains (P) are also clearlyrecognizable.
28. The high-intensity signal from water in solution and the lack of signal from
mineralized tissues produce contrast that allows recognition of the dental crown and
the outline of the carious lesion, pulp chamber, and root canals.
Carious tissues provide an intense NMRsignal image can be readily distinguishable
fromother dental tissues
Whenthe decay is extended to the pulp
chamber, pulp cavityand the carious tissues
can appear as a single structure
It is also possible to determine the presence of
a transition zone of increasing demineralization
between a very high-intensity area of
demineralized tissue and the zero intensity zone
of the sound tissue.
29. MRI Evaluation of Endodontic Anatomy
. Nasel et al, by using a 1.0 Tmagnetic resonance scanner, showed that the pulp chamber
of vital teeth is always well represented because structures gave a very clear hyperintense
signal in T2-weightedimages .
Witha resolution of about 100–300 mm,NMRI could lead to a better understanding of :-
Processes that occur inside the teeth during inflammation or in cases of narrowing and
obstruction of the root canal during repairing processes from secondary and tertiary
dentin .
Enables optimal assessment of relations between the tooth and a lesion;
The periodontal space is well-defined.
showed a high sensitivity for edema and neurovascular bundle.
In contrast with computed tomographic imaging, dental MRI can give insight into
chemical, vascular, and edematous properties of a lesion; soft tissue processes like
inflammations could be accurately visualized .
30. Theroot of a nonvital tooth produces a different signal when compared with a
vital one.
The general pulp dehydration with aging and root canal fillings such as gutta- percha
could incapacitate the identification of the root canal and the apical foramen.
. Dr˘agan et al obtained accurate images of a human endodontically treated wisdom
tooth using a 7.04 T device with a true free induction with steady-state procession
sequence protocol;
The external morphology of mesial and distal roots as well as the correspondingly shaped
root canals, root canal curvatures, the furcal region, the inter radicular root grooves, and
details of the apical finishing of the root canal treatment can be clearly seen in the 3D
reconstruction.
Where vital nerves in the root showed
a bright MRI signal. & could be easily
assessed byMRI.
Thesignal is attenuated or absent because
of the presence of necrotic tissues that
are not more perfused or the presence of
root canal obturation.
31. Newlydeveloped MRItechniques allow imaging of porous solids within minutes;
ex vivo UTEand ZTEMRIclearly surpass the resolution and information of
conventional MRIand CBCTimaging.
Byan order of magnitude of ~150-mmisotropic resolution, fine structures like
lateral canals are readily detected, and fine segmentation of the pulp is possible.
In vivo ZTEis still not available, and actually it ispossible to afford a resolution of
~600 mmwithin minutes using standard modern equipment and conventional MRI
sequences.
32. Figure 2. (A–C) T2-weighted MRI and (D–F) CBCT axial section of a tooth presenting a lateral canal (Lc). (A) The Lc in the
apical third originating from the principal root canal is visible in the NMRimage,
but it is not visible in CBCT scans. The lateral canal disappears in the immediately (B) coronal and (C) apical
sections.Theacquisition instrument, modality, and acquisition parameters are the same reported in Figure 1.
33. MRI Assessment of Periapical Lesions
In order to be radiographically visible, a periapical radiolucency should reach ~30%–
50% of bone mineral loss.
MRI could show periapical lesions in an earlier stage and with smaller bone mineral loss
because of its sensitivity to the changes in the T2 relaxation time of water molecules between
the constrained environment in healthy dentin and the less hindered and interacting status in
a pathologicalone.
A periapical abnormal area appears gray or white, and it can be distinguished from the
bone marrow.
When a periapical lesion reached and thinned cortical bone, the latter can be visualized as
a thin black line narrowing the lesion orallyand buccally.
• it can present a black area representing bone sclerosis.
34. Candifferentiate the nature of the substances
contained in the lesion;
the presence of blood or a high protein or high
cellular content can be recognized.
could differentiate a simple fluid-filled cavityfrom
an encapsulated cyst;
identification of the cyst’s core and wall or distinguishing a radicular cyst
from a chronic apical granuloma or other solid odontogenic
neo-formations (multicontrast MRI)
can also be reconstructed bysoftware that allows
measurements to define the volumetric evolution of
the lesion over time .
35. Figure 3. (A) Sagittal and (B–E) axial T1-weighted NMRimages and (F) sagittal, (G) frontal, and (H, I, J, K) axial CBCTscans of a tooth
presenting microcracks are shown. Microcracks affecting the middle third (yellow arrows) and
the coronal third projecting to the endodontic space (green arrows) are well represented in NMR
slices. Apulpal calcification (blue arrows) surrounded by hydrated tissues (white arrows) is
visible.Thehypointense area in the pulpal chamber is visible in NMR
but not as well in CBCT imaging, probably because of a lower density of the calcification when
compared withsound dentin. NMRimageswere obtained by usinga multislicemultiecho .2
36. Figure 4.(A–F) Endodontically treated tooth. The presence of 2 gutta-percha cones (yellow
arrows) surrounded by a clearly hydrated area (green arrow) is well-defined. An
incomplete 3D filling allowed infiltration of water from the apical foramen (white arrow).
None of this information is immediately deducible from (H–N)
CBCTimages obtained from the same tooth (G).
37. Future Trends in Endodontics
.
To visualize soft pulp tissue
To evaluate the presence of remnants of pulp tissue after canal
preparation and obturation and distinguish these tissues from voids
As an adjunct diagnostic device
Can show not only soft dental and periapical tissues but also differentiate
them (eg, vessels and nerves)
Assess perfusion and vitality
38. In vitro studies can reach better performance in terms of resolution
because of
• the higher SNR provided by a high magnetic field (higher than 7
T),
• a higher magnetic field gradient (higher than 300 mT/m),
• reduced FOV,
• the possibility of carrying out many of the signal averages (NA) ,
• the possibility of using MRI acquiring sequences with very short
echo times (TE) .
For these reasons, the development of in vitro studies is highly
desirable in the future.
39. In Vitro Micro-MRI in Endodontics
By using a NMR Avance-400 Bruker spectrometer (Bruker, Biller- ica, MA) at a 9.4-T
magnetic field with a microimaging probe characterized by an RF coil of 1 cm in diameter
and magnetic field gradients strength up to 1200 mT/m, they obtained images of extracted
teeth immersed in an NMRtube filled of water.
Theyhave exploited the ability of water to fill all tooth spaces to highlight the endodontic
canal and periodontal remains, lateral canals and microcracks and to evaluate the results
and the effectiveness of endodontic treatment.
40.
41. Conclusion
MRI could become a more common investigating tool both in research and clinical
endodontics. MRI provides the possibility to evaluate decay extensions, vitality and
vascularization of the pulp, presence of soft tissue remnants after endodontic procedures,
early detection, and precise follow-up of periapical lesions, with the great advantage of
avoiding the risk of ionizing radiation. Although some companies are currently developing RF
coils located in a narrow area around the teeth, ‘‘localized and tooth dedicated’’magnetic field
gradient coils for clinical use have not been developed yet.
42. 29. TuttonLM,GoddardPR.MRIoftheteeth. BrJRadiol2002;75:552–62.
30. GeibelMA,SchreiberES,BracherAK,etal.Assessmentofapicalperiodontitisby MRI:
afeasibilitystudy.Rofo 2015;187:269–75.
31. Dr˘aganOC,F˘arc˘as¸anuAS¸,C^ampianRS,TurcuRV.Humantoothandroot canal
morphologyreconstructionusingmagneticresonanceimaging.ClujulMed2016;
89:137–42.
32. AssafAT,Zrnc TA,Remus CC,et al. Evaluation of four different optimized magnetic-
resonance-imaging sequences for visualization of dental and maxillo-mandibular
structuresat3T.JCraniomaxillofacSurg 2014;42:1356–63.
33. Idiyatullin D,CorumC,MoellerS,etal.Dentalmagneticresonanceimaging:making
theinvisiblevisible.JEndod2011;37:745–52.
34. Idiyatullin D,GarwoodM,GaalaasL,NixdorfDR.RoleofMRIfordetectingmicro
cracksinteeth. DentomaxillofacRadiol2016;45:20160150.
35. Kress B, Buhl Y,H€ahnelS, et al. Age- and tooth-related pulp cavity signal intensity
changes in healthy teeth: a comparative magnetic resonance imaging analysis. Oral
Surg Oral MedOral Pathol Oral RadiolEndod2007;103:134–7.
36. KressB,BuhlY,AndersL,etal.QuantitativeanalysisofMRIsignalintensityasa tool
forevaluatingtoothpulpvitality.DentomaxillofacRadiol2004;33:241–4.
37. Ploder O,Partik B,RandT,et al. Reperfusion ofautotransplanted teeth–comparison
ofclinical measurementsbymeansofdental magnetic resonance imaging. OralSurg
OralMedOralPatholOralRadiolEndod2001;92:335–40.
38. AssafAT,ZrncTA,RemusCC,etal.Earlydetectionofpulpnecrosisanddental vi-
talityaftertraumaticdentalinjuriesinchildrenandadolescentsby3-Teslamagnetic
resonanceimaging.JCraniomaxillofacSurg 2015;43:1088–93.
39. PintoAS,CostaAL,Galv~aoND,etal.Valueofmagneticresonanceimagingfordiag-
nosisofdentigerouscyst.CaseRepDent 2016;2016:2806235.
References
1. BaumannMA,DollGM.Spatialreproductionoftheroot canalsystembymagnetic
resonancemicroscopy. JEndod1997;23:49–51.
2. Idiyatullin D,SuddarthS,CorumCA,etal.ContinuousSWIFT.JMagnReson 2012;
220:26–31.
3. OltS,JakobPM.Contrast-enhanceddentalMRIforvisualizationoftheteethandjaw.
MagnResonMed2004;52:174–6.
4. vanLuijkJA.NMR:dentalimagingwithoutx-rays?OralSurgOralMedOralPathol
1981;52:321–4.
5. WhiteSC,PharoahMJ.Theevolutionandapplicationofdentalmaxillofacialimaging
modalities. DentClinNorthAm2008;52:689–705.
6. NirajLK,PatthiB,SinglaA,etal.MRIindentistry-a futuretowards radiation free
imaging-systematicreview.JClinDiagnRes2016;10:ZE14–9.
7. Tymofiyeva O, Proff PC, Rottner K, et al. Diagnosis of dental abnormalities in chil-
dren using 3-dimensional magnetic resonance imaging. J Oral Maxillofac Surg
2013;71:1159–69.
8. Idiyatullin D, Corum CA,Nixdorf DR, Garwood M. Intraoral approach for imaging
teeth using the transverse B1 field components of an occlusally oriented loop coil.
MagnResonMed2014;72:160–5.
9. SedlacikJ,KutznerD,KhokaleA,etal.Optimized14+1 receivecoilarrayandpo-
sitionsystemfor3Dhigh-resolutionMRIofdentalandmaxillomandibular struc-
tures.DentomaxillofacRadiol2016;45:20150177.
10. TymofiyevaO,VaeglerS,RottnerK,etal.Influence ofdentalmaterialsondental
MRI.DentomaxillofacRadiol2013;42:20120271.
11. GrosseU,SyhaR,Papanikolaou D,et al. Magneticresonance imagingofsolid dental
restoration materials using 3D UTE sequences: visualization and relaxometry of
variouscompounds.MAGMA2013;26:555–64.
12. ShafieiF,HondaE,TakahashiH,SasakiT.Artifactsfromdentalcastingalloys in
magneticresonanceimaging.JDentRes2003;82:602–6.
13. Funduk N,KydonDW,Schreiner LJ,et al. Composition and relaxation of the proton
magnetization ofhuman enamel and its contribution to the tooth NMRimage. Magn
ResonMed1984;1:66–75.
14. SchreinerLJ,CameronIG,FundukN,etal.Proton NMRspingroupingandexchange
indentin.BiophysJ1991;59:629–39.
15. Zanolli C, Bondioli L, Coppa A, et al. The late early pleistocene human dental re-
mains from Uadi Aaladand Mulhuli-Amo (Buia), Eritrean Danakil: macromorphol-
ogyandmicrostructure.JHumEvol 2014;74:96–113.
16. SinibaldiR,ContiA,SinjariB,etal.Multimodal-3Dimagingbasedon mMRI
and mCTtechniques bridges the gap with histology in visualization of the bone
regeneration process. J Tissue Eng Regen Med 2017 Jun 7. http://
doi.org/10.1002/term.2494[Epubaheadof print].
17. WeigerM,BrunnerDO,DietrichBE,etal.ZTEimaginginhumans.MagnResonMed
2013;70:328–32.
18. LloydCH,ScrimgeourSN,ChudekJA,etal.Applicationofmagneticresonance mi-
croimagingtothestudyofdentalcaries.CariesRes2000;34:53–8.
19. BracherAK,HofmannC,BornstedtA,etal. Ultrashort echotime(UTE)MRIforthe
assessment ofcarieslesions. DentomaxillofacRadiol2013;42:20120321.
20. AppelTR,BaumannMA.Solid-state nuclearmagnetic resonance microscopy
demonstratinghumandentalanatomy.OralSurgOralMedOralPatholOralRadiol
Endod2002;94:256–61.
21. WeigerM,BrunnerDO,TabbertM,etal.ExploringthebandwidthlimitsofZTEim-
aging:spatialresponse,out-of-bandsignals,andnoisepropagation.MagnReson
Med2015;74:1236–47.
22. H€ovenerJB,ZwickS,LeupoldJ,etal.DentalMRI:imagingofsoftand solid
componentswithoutionizingradiation.JMagnResonImaging2012;36: 841–6.
23.BracherAK,HofmannC,Bornstedt A,etal. Feasibilityofultra-
short echotime(UTE) magneticresonance imagingfor
identificationofcariouslesions. MagnResonMed
2011;66:538–45.
24.LloydCH,ScrimgeourSN,ChudekJA,etal. Magneticresonance
microimagingof cariousteeth. QuintessenceInt 1997;28:349–
55.
25.WeglarzWP,TanasiewiczM,KupkaT,etal. 3DMRimagingof
dentalcavities-an
in vitro study.SolidStateNuclMagnReson2004;25:84–7.
26.BaumannMA,SchwebelT,KrieteA.Dentalanatomyportrayed
withmicroscopicvol- umeinvestigations. ComputMedImaging
Graph1993;17:221–8.
27.BaumannMA,DollGM,ZickK.Stray-fieldimaging(STRAFI)of
teeth. OralSurgOral
MedOralPathol 1993;75:517–22.
28.NaselC,GahleitnerA,BreitenseherM,etal. DentalMR
tomographyofthemandible. JComputAssistTomogr
1998;22:498–502.