Key words
head/neck - diagnostic radiology - MR imaging - radiography - apical periodontitis - dental MRI - cone beam computed tomography
Introduction
Apical periodontitis (AP) is mainly caused by bacterial inflammation. Through an inflamed root canal (pulpitis) or a deep gingival sulcus, bacteria can penetrate to the apical foramen and cause local infections. Apical periodontitis can be classified as an acute type with pain symptomatology and a chronic type without pain. Several studies have evaluated the type and incidence of periapical lesions in vivo [1]
[2] and in vitro [3]
[4] with different diagnostic methods. Nair et al. investigated 256 extracted teeth for identification of the incidence of abscess, granuloma, and radicular cyst. Their results showed an incidence of granuloma (50 %) and periapical abscess (35 %) and a surprisingly low incidence of cysts (15 %), which could be further categorized into a true apical cyst (acute) and an apical pocket cyst (chronic) building up after healing. In a comparative study between radiographic assessment and histological findings [4], the same group analyzed 114 specimens and revealed an insufficient concurrence of diagnosis between the two modalities, clearly indicating the need for improved in vivo diagnostic tools. Simon et al. [2] investigated the use of CBCT for the classification of periapical lesions. In direct comparison, the CBCT-derived diagnosis compared well with the biopsy-based diagnosis in the majority of the cases (75 %). However, in about 25 % of the cases, CBCT failed to differentiate between cyst and granuloma, indicating the need for advanced in vivo imaging techniques.
In the current clinical routine, X-ray-based imaging is still the gold standard for the diagnosing and progression monitoring of periapical lesions. Chronic apical periodontitis can be identified in the X-ray image by the related root resorption, hypercementosis and osteitis. Acute lesions, however, are difficult to assess by X-ray before substantial bone degeneration occurs.
Some studies have shown that a periapical lesion from endodontic infection might be present without being radiographically visible. In order to be radiographically visible, a periapical radiolucency should reach nearly 30 – 50 % of bone mineral loss [5]
[6]. Furthermore, the size of periapical lesions is often underestimated in periapical radiographs [7]
[8]
[9].
The radiographic image conforms to a 2-dimensional projection of a 3-dimensional structure. The interpretation is known to be limited by complex background patterns such as overlapping roots and anatomic structures like maxillary sinus.
As a first step towards improved in vivo imaging, the increasing availability of cone beam computed tomography (CBCT) imaging systems enables volumetric imaging [10]
[11]. A few recent studies clearly indicate the potential improvement of the diagnosis of periapical lesions by the introduction of CBCT. In a comparison to conventional radiographs, Tsai et al. [12] and Liang et al. [13] proved a higher sensitivity of CBCT especially for smaller lesions and an overall increase in diagnostic fidelity. Estrela et al. [14] reported that only progressed periapical lesions were identified correctly by conventional radiography. In contrast, Balasundaram et al. [15] reported an only insignificant impact of CBCT diagnosis for the treatment of a respective lesion.
Due to the underlying physical principle, all X-ray (XR)-based imaging techniques have limited capabilities in soft tissue characterization and are supposed to be limited in the differentiation between chronic and acute periapical lesions that may have an impact on the treatment strategy. Furthermore, the related ionizing radiation with its well-known risks [16] limits the application of CBCT for longitudinal monitoring especially in young patients.
Magnetic resonance imaging (MRI) has shown excellent results for soft-tissue visualization without any harmful radiation. Already in 1981, the versatile three-dimensional assessment of morphology and function raised the interest of MRI as a generic imaging tool in dental applications [17]
[18].
However, up to now, only a few reports have been published on the application of MRI in dentistry mainly due to the limited access of dentists to MRI and limitations of MRI arising from metal artifacts caused by dental fillings. Without being used widely, reported applications of MRI in dentistry include the assessment of extracranial tumors [18]
[19]
[20]
[21], the assessment of the morphology and function of the temporomandibular joint [22]
[23]
[24]
[25]
[26]
[27], the planning of dental implantation procedures [28]
[29]
[30]
[31]
[32], planning and evaluating orthodontics and orthognathic surgery [33], the assessment of impacted teeth [34] and the mandibular and the trigeminal nerve channel [35]
[36]
[37]
[38]
[39]
[40]
[41], caries diagnosis [42]
[43]
[44]
[45], assessment of dental pulp [46]
[47], or for imaging of the mandible and mandibular for other purposes [48]
[49]
[50]. With the introduction of faster imaging techniques that are less sensitive to dental filling material and the advent of new compounds, the application of MRI for periapical lesion diagnosis and characterization appears increasingly attractive and should be reconsidered.
It is the aim of this study to clinically evaluate the applicability of MRI for the assessment of apical periodontitis in direct comparison with CBCT.
Materials and Methods
19 consecutive patients (average age 43 ± 13 years) with 34 lesions in total (13 molars, 14 premolars and 7 front teeth) were enrolled in this feasibility study. XR findings included minor to severe periapical lesions. All patients had multiple dental fillings (including amalgam, gold, ceramic and composite fillings), crowns and bridges. As ferromagnetic materials containing alloys cause severe image artifacts in MRI, patients with retainers or brackets were excluded from this study. All patients underwent a CBCT scan and an MRI investigation within 16 ± 15 days. Two patients had to be excluded during the MRI scan due to severe claustrophobia.
The local ethics committee of the university approved the study protocol, and written informed consent was obtained from all patients before dental MRI.
Imaging protocol
The CBCT data were obtained on a wide volume imaging system (Galileos, Sirona Dental Systems, Germany) with an in-plane resolution of 0.287 mm, a field of view of 150x150x150 mm³ and an effective average dose of 16 – 90 µSv. All MRI data were acquired on a 3-Tesla whole-body system (Achieva 3 T, Philips Medical, Best, The Netherlands) with a 16-element neurovascular receive coil.
All patients underwent a standardized MRI protocol. After a first initial survey in axial, sagittal and coronal orientation, high-resolution (HR) scans were acquired in parasagittal or paracoronal orientation aligned with the central line of the teeth. The high-resolution diagnostic scans comprised a high-resolution multi-slice TSE acquisition (HR-TSE) with T1- (T1w) and T2-weighted (T2w) contrast. The scan time was 9:06 min (T1w) and 5:43 min (T2w). Relevant acquisition parameters are listed in Table I. Please note that the rather long repetition time of TR = 625 ms will not result in pure T1-weighted images, but the final image contrast will also be slightly impacted by the proton density. However, with average T1 values well above 1000 ms at a field strength of 3 T, T1 relaxation will still govern the resulting image contrast.
Data analysis
For analysis, all data were transferred to a medical workstation (ViewForum, Philips Healthcare, Best, The Netherlands). Periapical lesions were defined as periapical radiolucencies (CBCT) or structural changes in the spongy bone signal (MRI), which were connected with the apical part of a root and with at least twice the width of the periodontal ligament space.
Location and dimension of the lesions were compared between T1w, T2w images and CBCT. The isotropic CBCT data were reformatted in parasagittal direction similar to the MRI acquisition geometry. Lesion dimensions were independently quantified in either modality by their height h, width w and area A in the slice showing maximal extension of the lesion. All data were analyzed in consensus by an experienced dental radiologist (MAG, more than 20 years of dental radiology experience), a dental medical doctorate student (ESS, 1 year after approbation), an oral and maxillofacial surgeon (LKS, more than 10 years of experience), and an experienced MR scientist (VR, more than 20 years of MRI research experience). In this feasibility study, the data were not blinded for evaluation.
The correlation of the dimension measurement between the different approaches was assessed applying a Spearman’s rho test and the significance of differences between measurements was assessed using the two-tailed paired student’s t-test. Normal distribution of the data was tested by applying a Kolmogorov-Smirnov test. P-values below 0.05 were considered significant. All statistical analyses were performed with SPSS 21.0 (IBM Corp, Armonk, NY).
In the case of invasive treatment, the excised material was histologically investigated for inflammation markers.
Results
The imaging protocol was successfully performed in all investigated patients. The average MRI examination time for both sides including patient preparation and scan planning was 50 minutes. Although the patients presented with dental fillings, bridges and crowns, all lesions could be visualized with sufficient image quality. Even though a single acquisition took up to 9 minutes, no motion artifacts introduced by swallowing were observed. A typical example for the resulting image appearance with MRI in direct comparison with CBCT is presented in [Fig. 1]. Where CBCT mainly shows mineralized tissue components such as teeth and bone, MRI provides complimentary information of the soft tissue components.
Fig. 1 Cystic lesion (arrow) – CBCT a and T1- b and T2- weighted MRI images c.
Abb. 1 Zystische Läsion (Pfeile) – DVT a und T1-b und T2 gewichteten MRT Daten c.
The T1w images ([Fig. 1b]) provide sufficient diagnostic detail for the assessment of the main structures of interest. The large lesion visible on CBCT images ([Fig. 1a]) can be clearly seen on the MR image. According to the imaging physics, the contrast between the lesion and the surrounding mineralized material is inverted. Highly mineralized structures, appearing bright on CBCT images, result as signal voids in the respective MRI representation. However, due to the surrounding soft tissue (gingiva, muscle, salivary glands), and the bone marrow (high fat content), the cortical bone and the teeth can be clearly identified. In direct comparison, the lesion appears more homogeneous on the CBCT image. No apparent artifacts from the dental fillings occur in MRI, while some streaks caused by beam hardening can be observed on the CBCT images. Root filling materials, however, are not visible on the MRI images and the apical foramen cannot be directly assessed. The heterogeneous contrast within the lesion is even more obvious in the T2w image ([Fig. 1c]), with clear enhancement close to the apical foramen and the periodontal gap.
All lesions identified with CBCT were clearly visible on T1w as well as in T2w MR images. The lesion dimensions in T1w and T2w MRI corresponded well (R² = 0.98, p < 0.01) to each other and did not show any significant differences (pT1-T2: w> 0.82, h> 0.87, A> 0.84). Compared with CBCT, the lesion dimensions were slightly but significantly overestimated for T1w as well as T2w image contrast (pT1-DVT: w < 0.01, h < 0.01, A < 0.01; pT2-DVT: w < 0.01, h < 0.01, A < 0.01). The correlation between MRI and CBCT data showed reasonably good results with values ranging between R² = 0.73 and 0.89, all highly significant with p-values below 0.01. A heterogeneous lesion appearance on the T2w MR images was observed in several patients and four patients presented with a well circumscribed hyperintense signal in the vicinity of the apical foramen ([Fig. 2]). Only one of five clinically identified chronic lesions (four cysts and one granuloma, all showing inflammation markers in histology) showed a clear heterogeneous signal on T2w images. The dimension of the remaining lesions was too small to allow assessment of heterogeneous contrast.
Fig. 2 Radicular cyst (arrow) – radiograph a, T1w MRI b, and T2w MRI c showing a clear enhancement at the location of the apical foramen (dashed arrow) in the T2w MRI images.
Abb. 2 Radikuläre Zyste (Pfeil) – Zahnfilm a, T1w MRT (B) und T2w MRT c einer apikalen Osteolyse (Pfeil) mit deutlicher Aufhellung in der Region des apikalen Foramens (gestrichelter Pfeil) in den T2w MRT Daten.
In several cases, MRI could provide additional information not directly available from XR–based imaging. Exemplarily, Figs. 3 and 4 show two patients presenting with similar clinical symptoms and lesion appearance on the CBCT and OPG images. From the respective MR images, both cases could be clearly differentiated into a simple fluid-filled cavity ([Fig. 3]) and an encapsulated cyst ([Fig. 4]), which was confirmed by histology. Multi-contrast MRI especially helped with the identification of fluids (T1 hypointense, T2 hyperintense) and fibrotic tissue (T1w and T2w isointense). While the signal from fluids was hypointense on the T1w image when compared to fibrotic tissue, the contrast is inverted on the respective T2w image, thus enabling identification of the cyst core and wall.
Fig. 3 Simple fluid-filled cavity (arrow): – OPG a, orthogonal reformatted CBCT b, orthogonally acquired MRI located in the center of the lesion with T1- c and T2-weighted d image contrast. Please note the close vicinity of the lesion to the root canal (open arrow), which can only be observed in the MR image.
Abb. 3 Flüssigkeitsgefüllter Raum (Pfeil) – OPG a, orthogonal zum Kieferkamm orientierte Schicht zentral durch die Läsion im DVT b und orthogonal zum Kiefer gemessene Schicht im MRT mit T1- c und T2- Wichtung d. Nur in der MRT Darstellung kann die enge Langebeziehung zum Wurzelkanal (offener Pfeil) eindeutig dargestellt werden.
Fig. 4 Encapsulated cyst (arrow) – OPG a, CBCT b, MRI with T1- c and T2-weighted d image contrast. In the MRI image, the lesions appears as fibrotically (open arrow, isointense in T1w and T2w) encapsulated fluid-filled (hypointense in T1w, hyperintense in T2w) space.
Abb. 4 Umschlossene Zyste (Pfeil) – OPG a, DVT b MRT T1-c und T2- gewichtetes MRT d der Läsion. In der MRT stellt sich die Zyste dar als fibrotisch (offener Pfeil, isointens in T1 und T2) umschlossener flüssigkeitsgefüllter Raum (hypointens im T1, hyperintens im T2) dar.
Discussion
In oral and maxillofacial surgery, panoramic radiography is still considered to be the gold standard for examination of the dentomaxillofacial region. Although findings of apical osteolysis or cysts, especially in advanced cases, can sometimes be detected on radiographic images, superimposition of bony structures, dental roots, and filling materials, misinterpretation of artifacts, and the relatively low resolution capacity may cause pathological changes to go undetected [51] and demand the use of additional views. Furthermore, many radicular cysts remain asymptomatic and are incidentally discovered on a panoramic radiography image as possibly unsuspected disease. Using the conventional X-ray techniques, it is not possible to distinguish a radicular cyst from a chronic apical granuloma, which may have an impact on the treatment regimen. Thus, the image quality of the panoramic radiography is clearly limited in its expressiveness and its use can only be justified by the low effective radiation dose [52].
To address these ambiguities, the investigators have moved along to three-dimensional imaging with CBCT [13]
[14]. Even on a CBCT scan, summation effects particularly occurring in the anterior region of the spinal column and the area of the palatal vault, have been shown to result in overlapping of root tips in the posterior region of the maxilla, thus the abovementioned issues partly come into play once more.
Even though magnetic resonance imaging (MRI) does not play a major role in current dental imaging, its potential for soft tissue characterization may raise interest especially in the imaging of periapical lesions. Concerns may arise from artifacts induced by dental fillings and also from limited assessment of the cortical bone.
This clinical study proves the applicability of conventional MRI sequences for the identification of periapical lesions. Comparing MRI to the standard CBCT scan used in daily clinical practice revealed a similar sensitivity in the diagnosis of periapical lesions. In the 19 patients randomly included in the study, no periapical lesion was missed due to metal artifacts on MRI, which was an issue for the authors in the beginning of the study.
However, significant differences in the lesion dimensions were observed between CBCT and MRI. One explanation might be the poorer spatial resolution of MRI compared to CBCT. However, we believe it is more likely that the overestimation on MR images resulted simply from the different physical principles behind these two modalities, since no differences were observed between the two investigated MRI sequences.
It has been shown [5]
[6] that at least 30 % mineral loss is required to detect a bony lesion on XR-based imaging methods. Instead, MRI can show the signal changes before substantial mineral loss occurs, due to its sensitivity to the changes in the number of water molecules in a given lesion [43]
[44].
From the clinical routine it is well known that the lesion extent is often underestimated by XR-based methods, indicating only a limited performance in definition of the accurate lesion border. MRI may be able to assess the real extension of a lesion more accurately and thus provides a better estimation of the relationship of the lesion to the nearby critical structures such as the nerves and the vessels.
Advantages of MRI may further help in the field of lesion characterization. Due to its superior soft tissue contrast compared to CBCT, the application of MRI may yield improved diagnostic information and pre-interventionally characterize the underlying pathology, which in turn affects the treatment regimen. This study focused on the comparison between CBCT and MRI regarding sensitivity and lesion dimensions. However even though destruction of the tumor structure during resection has so far precluded direct comparison between MRI appearance and histological tissue characterization, the presented data revealed strong evidence for the applicability of MRI for the delineation of different lesion types.
Fujita et al. recently described the diagnostic value of MRI for the differentiation of certain odontogenic tumors [21]. Although the results were promising, one limitation of MRI has been shown to be its relatively low diagnostic ability for the assessment of the course of filled root canals. Where vital nerves in the root showed a bright MRI signal and could easily be assessed by MRI, the general nerve dehydration with aging and especially root canal fillings hindered identification of the root canal and the apical foramen. Whether this demands additional XR-based images remains to be shown in further clinical studies.
Although this study shows the feasibility of applying MRI for the imaging of periapical lesions, several obstacles have to be overcome before its wide clinical application. A major limiting factor is the intrinsically poor signal-to-noise ratio (SNR) of MRI. All data presented in this study were acquired on a high-field (3 T) whole-body clinical MR system. The likely drop in SNR may be addressed e. g. by usage of intraoral-coils [34], surface coils [37], or even dedicated dental phased-array coils [53]. The high imaging costs and long acquisition times still likely restrict the application of MRI to clinical research. To overcome these obstacles, dedicated dental systems enabling lower imaging costs, easier installation and maintenance, and more rapid data acquisition may be employed. While complete coverage of the entire jaw with high-definition T1 and T2 contrast was obtained in this study, the overall acquisition time could be significantly reduced by restricting the region of interest to the suspicious area. Rapid overview scans could be realized e. g. by applying fast T1-weighted 3 D FLASH sequences enabling complete coverage of the jaw at isotropic spatial resolution in the minute range at slightly coarser spatial resolution, showing sufficient anatomic detail for the identification of culprit areas and enabling anatomically ideal reformats. By combining rapid overview imaging with subsequent high-definition local imaging of the culprit areas, substantial reduction of the overall scan time to the 15-minute range appears feasible.
Whether the required SNR values will be met by these systems and the quality of the images need to be further investigated.
Even though no severe limitations due to dental filling materials were observed in the present study, metal artifacts and image degradation cannot be completely excluded. Conductive materials will experience eddy currents, and the related magnetic field distortions likely cause signal cancelation in the proximity of the material, which may limit the application of the MRI e. g. in the presence of titanium implants. Ferromagnetic materials such as nickel and cobalt, which are frequently used in older alloys, dental prostheses, retainers and brackets, may also cause severe image degradation. However, compared to CBCT, MRI does not show long ranging banding and streaking artifacts, but only local image degradation, which is often restricted to the close proximity of the artifact source and does not impact neighboring teeth. The rather long acquisition times with MRI are prone to result in artifacts introduced by swallowing by the patient. Even though artifacts were not observed in this study, additional use of navigated MR sequences as used for high-resolution carotid imaging [54] may be required during larger clinical studies.
In summary, the identification of periapical lesions by means of MRI appears feasible. In comparison to the clinical standard, MRI may enable pre-interventional tissue characterization or at least an improved understanding of the lesion extent and pathology. Whether its limited spatial resolution, the prolonged acquisition time and the likely higher costs of imaging will prevent wide clinical application of the suggested technique is still unclear.
