New coil concept for endoluminal MR imaging

Our aim was to conduct a prospective study to evaluate staging accuracy of a new coil concept for endoluminal magnetic resonance imaging (MRI) on ex vivo gastric carcinomas. Twenty-eight consecutive patients referred to surgery with a clinically proven primary gastric malignancy were included. Surgical specimens were examined with a foldable and self-expanding loop coil (8-cm diameter) at 1.5 Tesla immediately after total gastrectomy. T1- and T2-weighted and opposed-phase sequences (axial, frontal sections; 3- to 4-mm slice thickness) were acquired. Investigators blinded to any patient information analyzed signal intensity of normal gastric wall, gastric tumor, and lymph nodes. Findings were compared with histopathological staging. On surgical specimens, 2–5 gastric wall layers could be visualized. All gastric tumors (26 carcinomas, two lymphomas) were identified on endoluminal MR data (100%). Overall accuracy for T staging was 75% (18/24); sensitivity to detect serosal involvement was 80% and specificity 89%. N staging correlated in 58% (14/24) with histopathology (N+ versus N−). The endoluminal coil concept is feasible and applicable for an ex vivo setting. Endoluminal MR data provided sufficient detail for gastric wall layer differentiation, and therefore, identification of T stages in gastric carcinoma is possible. Further investigations in in vivo settings should explore the potential of our coil concept for endoluminal MR imaging.
Introduction
Despite the fact that the incidence of gastric cancer is declining in most Western countries, it remains the second leading cause of cancer mortality worldwide [1, 2]. Simultaneously, the incidence and prevalence of cancer arising from the gastric cardia has been increasing since the 1970s [3]. Adenocarcinoma of the esophagogastric junction can be classified according to Siewert et al. based on morphology and anatomical location [4]. Adequate surgical resection (R0) is the only potentially curative therapy for eligible patients with gastric carcinoma [4]. In the West, gastric cancer is often diagnosed at an advanced stage of disease not eligible for surgery. Fewer than 50% of patients undergo R0 resection [5, 6]. Recently, new concepts of multimodal treatment strategies for locally advanced gastric carcinoma have been investigated [7, 8]. Local treatment by endoscopic mucosal resection for early gastric carcinomas is currently being evaluated [9, 10]. Several phase II and III clinical trials for neoadjuvant chemotherapy in gastric carcinoma showed its feasibility and safety [11, 12]. Its purpose is to eliminate or delay systemic metastasis and reduce micrometastatic spread of disease. Another benefit is potential reduction of tumor volume in initially unresectable advanced tumor stages (downstaging), therefore increasing resectability rate. An adequate treatment strategy, especially in regard to the concept of neoadjuvant chemotherapy, requires precise clinical staging to depict relevant prognostic factors and identify resectable tumor stages. This also accounts for endoscopically treated early gastric cancers as well as for adenocarcinomas of the gastroesophageal (GE) junction since each type of tumor requires a different surgical approach. Thus, the exact knowledge of tumor morphology and tumor invasion into gastric wall is a crucial information for clinical staging.
Up to now, computed tomography (CT) and magnetic resonance imaging (MRI) have not provided the spatial resolution to fulfill this requirement with sufficient accuracy [1, 13–16]. Results for staging accuracy of endoscopic ultrasound (EUS) also seem to be improvable [17–19]. The main aspect of gastric wall differentiation is spatial resolution. By using endoluminal radiofrequency (RF) coils for MRI, image quality and spatial resolution can be enhanced. MRI provides superior soft tissue contrast, which makes it useful for tumor invasion detection; furthermore, information not obtainable by other imaging modalities is acquired. Various authors reported the use of endoluminal RF coils as a diagnostic and staging tool in gastrointestinal diseases and rectal and prostate cancer [20–27]. A major problem with endoluminal RF coils is placement close to the region of interest and depth of visualization. Our approach uses a foldable and afterward self-expanding loop coil design (8-cm diameter), which enhances spatial resolution and depth of visualization The aim of our study was to assess normal gastric wall architecture and signal intensity (SI) on endoluminal MRI as well as signal intensity and appearance of gastric carcinomas and their related lymph nodes. Subsequently, we used endoluminal MRI as staging modality on ex vivo gastric carcinomas. Findings were compared with histopathological staging.
Materials and methods
Patients
A prospective study was conducted on patients with gastric malignancies referred for total gastrectomy to the surgery department of our university hospital. They were included in the study if the lesion was identified by EUS or CT suggesting a gastric carcinoma or if histological workup of biopsies confirmed the diagnosis. The study protocol was approved by the institutional review board, and informed consent was acquired from each patient prior to surgery. We investigated 28 consecutive patients, 11 women and 17 men (age range 46–87, median 67 years). Tumors were located at the cardiac region in 11 cases, the fundal area in two, the corpus in six, and the antropyloric area in nine. Immediately after surgery, gastrectomy specimens were taken to the MR suite to conduct the examination within a time frame of 2–3 h (Fig. 1). Specimens where then sent to histopathology unchanged from the procedure.
Fig. 1Flowchart of study design
Endoluminal RF coil
The endoluminal RF coil (patent issued 10/2005, German Patent and Trade Mark Office, No: 10127850.0–35, Grenacher et al.), developed in collaboration with Fraunhofer Institute for Biomedical Engineering (IBMT, St. Ingbert, Germany) consists of a foldable and self-expanding receiver loop (8-cm diameter). It is coated with a biocompatible material (silicone) to prevent direct contact of the wire with stomach tissue [29]. The flexible characteristics of the shape memory metal (nitinol) used allow passage through the instrument channel (13-mm diameter) of a specially designed MR-compatible endoscope. The MR-compatible endoscope was not used in this study and is described elsewhere, but it is mentioned in this context because RF coil design is reflected by the specifications of the endoscope. A nonferromagnetic tuning box connects the RF coil via a standard interface with a 1.5-Tesla MRI scanner (Symphony, Siemens, Erlangen, Germany), which was used in this study. Gastrectomy specimens were placed in a container with 3–4 l of 0.9% sodium chloride solution to ensure good contrast with gastric tissue and adequate expansion of gastric folds. The loop of the RF coil was placed on the mucosa side of the tumor. After the tumor was located with a scout sequence, images where acquired in axial and frontal sections of 3- to 4-mm thickness. Scanning was performed with T1- and T2-weighted and opposed-phase sequences (Table 1).
Table 1Imaging sequence parametersSequenceRepetition time (TR)Echo time (TE)AcquisitionsSlice thickness (mm)MatrixField of view (FOV) (mm)Pixel size (mm)T1-weighted TSE5511424512x5122000.39x0.39T2-weighted TSE3,52070231024x10242200.21x0.21T2-weighted GRE1,0503513512x5122200.43x0.43T1-weighted GRE opposed phase187743256x2652200.86x0.86TSE turbo spin echo, GRE gradient recalled echo
Image evaluation
Image data were read on certified diagnostic work stations independently by two board-certified radiologists with 10 and 12 years of experience, respectively, and one board-certified surgeon with 8 years of experience in endoscopic ultrasound on gastric carcinomas. Investigators were blinded to any clinical information as well as patient identification. After separate reading, a discussion was held about the quality of data and unique features of the case. Additionally, final agreement was achieved if disagreement on tumor stage had initially occurred. With respect to the unique imaging technique, the resolution and detail of image data a consensus staging was reasonable. Radiological and histopathological classification of the tumor was done according to the Tumor Node Metastisis (TNM) staging system of the Union Internationale Contre le Cancer (UICC) [30]. Determination of tumor stage was done as follows:
T1: tumor invasion of the lamina propria of mucosa or invasion of submucosa, wall thickening, and signal intensity changes confined to these layers.T2: tumor invasion extended to the muscularis propria, and additional thickening through gastric layers with signal intensity changes showing either a homogeneous or inhomogeneous lesion without serosal abnormalities. If invasion extended beyond muscularis propria into an adjacent fat tissue plane without serosal infiltration, it was considered as T2.T3: tumor invasion of mucosa, submucosa, and muscularis propria, with infiltration of the serosa or changes in signal intensity presenting with micronodular strands as growth into extraserosal fat tissue.T4: tumor invasion into adjacent organs or structures clearly presenting as contiguous tumor extension or a mass with similar signal intensity as the gastric tumor.
N staging was done counting the lymph nodes detectable on MRI, regarding them as pathologic due to their signal intensity. Since gastrectomy samples varied in lymph node content due to surgical technique and extension of the gastrectomy not comparable to an in vivo situation, N factor was graded into N+ for positive findings of lymph nodes and into N− for absence of lymph nodes. In each case, normal gastric wall features were assessed. Signal intensities of the mucosa, submucosa, muscularis propria, and serosa or subserosa were recorded, as well as the amount of layers in which the normal gastric wall could be differentiated into. A score system from 1 to 5 (1=poor; 5=very good) was used for several study items to weigh the power of their findings. Each sequence, for example, was rated for image quality on a range from 1 to 5, representing insufficient to very good. Signal intensity and morphology of the gastric tumors and demarcation to normal gastric wall were used to describe characteristics of tumor presentation. The lesion was identified by irregular architecture of gastric wall, abnormal thickening, and change in signal intensity of gastric wall layers, which usually present with sharp and clear demarcation into three to five different layers with distinct signal intensities and thickness. Tumor size was not measured, as it does not influence T staging or provide further information. Histopathology was considered the gold standard, and radiological data where compared with its results.
All data are presented as absolute numbers and relatively as percentages. Concordance of histopathological results and radiological findings are reported as overall accuracy. Sensitivity, specificity, and accuracy for T factor, N+/− factor are provided. Detection rate of serous membrane invasion or the differentiation between T2 and T3 stages was assessed, as it defines advanced stages of disease. Ninety-five percent confidence intervals (CI) are given if statistically applicable.
Results
The setup of our study proved to be feasible, as shown elsewhere [29]. Two cases were not included because of insufficient image quality. Histopathology found 26 carcinomas (15 adenocarcinomas, nine signet cell carcinomas, two mixed type carcinomas) and two gastric lymphomas. Four tumors were classified as pT1, 15 as pT2, 3 as pT3, and 2 as pT4. Gastric lymphomas were excluded from the study although they where detected as such in both cases (100%).
Gastric tumor staging
In 24 (100%) cases, the tumor was identified. Initially 46% (11/24) of T stages were staged correctly; 1/4 of pT1 tumors, 7/15 of pT2 tumors, 2/3 of pT3 tumors, and 1/2 of pT4 tumors were classified correctly (Table 2). Interpretation of image data was done without knowledge of tumor location in respect to the gastric region, such as cardia, fundus, corpus, or antrum, as it would be possible on an in vivo setting such as endoscopy or CT. In a second reading session, the interpreters were informed about the gastric region of the primary tumor for each case. In knowledge of gastric region, six, first as T3 classified carcinomas of the cardia, were correctly staged as pT2 and one, first as T3 classified tumor (cardia), was correctly identified as pT4 (Table 3). This gives an overall accuracy of 75% (18/24)± –17.32 (CI) (Table 4). The mean score for T-factor staging was 3.54 (range 2–5). Sensitivity, specificity, and accuracy for detecting serosal involvement was 80%±16.00, 89%±12.27, and 88%±13.23, with a mean score of 4.5 (range 3–5; Table 5). Overstaging occurred in 4/24, three pT1 tumors were classified as T2 or T3 stages, and one pT2 tumor was identified as T3 stage (Table 6). In this case, the tumor replaced all gastric wall layers and invaded perigastric fat tissue but did not infiltrate the serous membrane. Insufficient separation of gastric wall layers and the presence of abnormal signal intensities most likely desmoplastic reactions or peritumor inflammation were identified retrospectively as reasons for overstaging of pT1 tumors. Two tumors (pT2, pT3) were understaged as T1 and T2 stage. One case was a diffuse type pT2 adenocarcinoma with disseminated infiltration into the muscularis propria, which is not visualized and thus presented as T1 stage.
Table 2Comparison of histologic with endoluminal findings without knowledge of tumor region Endoluminal magnetic resonance imaging (MRI) findingsHistologic findingsT1T2T3T4Total (n=24)T1121–4T2177 –15T3–12 –3T4––11 2Table 3Comparison of histologic findings with endoluminal findings acquired with knowledge of tumor region Endoluminal magnetic resonance imaging (MRI) findingsHistologic findingsT1T2T3T4Total (n=24)T1121 —4T21131—15T3–12 –3T4–––22Table 4Sensitivity, specificity, and accuracy for each T stage; overstaging and understaging rates T1T2T3T4OverallSensitivity1/413/15 2/3 2/2 –Specificity19/20 6/9 19/21 22/22 –Accuracy20/24 19/24 21/ 24 24/24 18/24 Overstaging3/4 1/15 ––4/24 Understaging–1/15 1/3 –2/24 Table 5Results for serosal invasion detectionEvaluation of serosal invasionSensitivity4/5Specificity17/19Accuracy21/24False positive2Table 6Signal intensities of gastric wall layers on T1-weighted, T2-weighted, and opposed-phase imaging from inside to outside T1 imaging (n=21)aT2 imaging (n=27)aOpposed phase imaging (n=3)aTwo layers (n=7)bHigh––IntermediateThree layers (n=33)bHighIntermediateHighLowHighLowIntermediateIntermediateHighFour layers (n=10)bHighIntermediate–LowLowIntermediateIntermediateLowLowfive layers (n=1)*–Intermediate–HighIntermediateLowIntermediateaNumber of sequences analyzedbNumber of sequences with n layers
Nodal involvement
Lymph node detection resulted in N+ for detected lymph nodes in 17 cases with N− in 7 cases. Sensitivity for detecting N+ was 71%±18.22, specificity 29%±18.07, and accuracy 58%±19.72. This reflects the limitation of the study design. Ex vivo gastrectomy specimens do not provide the same quantity of lymph nodes as pathological workup. The mean score rating N factor staging was 4.4 (range 2–5).
Image analysis
Separation of gastric wall layers ranged from a minimum of two visible layers to five distinct visible layers (mean 3.10) in 51 analyzed sequences: 21 T1-weighted and 27 T2-weighted sequences and three opposed-phase sequences (Table 6). T2-weighted sequences depicted an average of 3.37 gastric wall layers; T1-weighted sequences 2.76. Mean score for image quality of the sequences used was 3.88 (range 2–5), with 4.11 for T2- and 3.62 for T1-weighted sequences. Image analysis revealed that in four out of six incorrectly staged T factors, tumors were described as inhomogeneous or diffuse concerning demarcation to normal gastric wall. This may be one reason for misinterpretation of T factor. Signal intensity of the mucosa for T1-weighted sequences was mostly classified as hyperintense; for T2-weighted, it was intermediate. Submucosa, muscularis propria, and serosa or subserosa presented with hypointense, intermediate, hypointense SI for T1-weighted; hyperintense, intermediate, hypointense for T2-weighted sequences (Table 6). Lymph node and tumor appearance correlated in 86%±9.9 (44/51 sequences), with intermediate SI for T1- and T2-weighted sequences. Out of eight sequences without correlation in lymph node and tumor SI, two sequences showed a homogeneous tumor in T1-weighted and an inhomogeneous lesion in T2-weighted images (Fig. 3). In three opposed-phase sequences, lymph nodes (hypointense) showed different signal intensity than the primary tumor (intermediate). T2-weighted sequences (Table 4) visualized more gastric wall layers and provided the interpreter with a better demarcation of tumor volume from normal gastric wall than did T1. T1-weighted sequences showed a better delineation and contrast of lymph nodes in adjacent structures (Fig. 2).
Fig. 2a, bTwo consecutive T2-weighted images (a, b) of a T1 early gastric carcinoma (white arrowheads), well differentiated (intestinal type of Lauren classification), located at the subcardial region. Lymph nodes in adjacent fat tissue with a high signal intensity (white arrows) are visualized. Morphology of normal gastric wall is pointed out by open arrows. (*) marks the position of the receiver coilFig. 3a, bT2 signet cell tumor of the cardia region (diffuse type of Lauren classification, white arrowhead) on T1-weighted (a) and T2-weighted imaging (b). The extent of tumor mass and the diffuse infiltration into gastric wall is better visualized on T2-weighted images due to the mucinous character of the tumor (black arrowheads). The tumor appears more homogeneous on T1-weigthed images (a). (*) marks the position of the receiver coil
Discussion
Endoluminal MRI has been used by various groups to asses its ability for locoregional imaging of esophageal and gastrointestinal disease. The first group [20, 31] to introduce an MR endoscope reported promising results for the diagnosis of gastrointestinal diseases and pointed out limitations of their design [20, 31]. Image quality of endoluminal MRI was not as clear as those acquired by EUS, and their success rate of obtaining clear images of the stomach was low (58%) [20]. Although their study achieved 89% for T-staging accuracy, its patient collective consisted mainly of advanced gastric carcinomas (T3, T4). Other authors reported the use of an MR endoscope with a similar design [21, 28, 32], sharing the incorporation of the RF coil with 10×30 and 10×47 mm into the tip of the MR endoscope. This is a useful design for imaging at the esophagus, where both groups showed good results in staging esophageal cancer [20, 28]. The small cylindrical RF coil design implemented in the tip of the MR endoscope may be a reason for problems in obtaining sufficient images in the stomach. Our approach using an insertable and self-expandable RF coil (8-cm diameter), independent from the MR endoscope, seems to be more suitable for imaging of the stomach by providing enhanced depth of visualization. In 93%, sufficient image data was obtained. Detection of resectable lesions can only be accomplished by exact knowledge of tumor invasion in relation to gastric wall layers. New multimodal treatment strategies require the information of tumor stage, as it defines enrollment into neoadjuvant therapy approach. Clinical staging based on imaging studies can provide important information for adequate therapy decision if they fulfill this requirement. Gastric wall differentiation and identification is essential for accurate staging of gastric malignancies.
Our approach can depict between two to five gastric wall layers and therefore deliver sufficient detail as basis for tumor invasion detection. Signal intensities of gastric layers assessed in our study correspond mainly to those reported previously by other authors [20, 33, 34]. Visualization of the serosa layer remains a problem in all published studies with MRI or endoluminal MRI on gastric wall. Some authors investigated ex vivo gastrectomy specimen with a 1.0-Tesla MRI device and were able to differentiate up to five different gastric layers, but visualization of the serosa or subserosa was not achieved [35]. One reported study used a 2.4-Tesla MRI system and failed, as did another study with a 4.7-Tesla MRI system, to visualize serosa or subserosa as a distinct layer [34, 36]. One work group reported possible identification of serosa or subserosa on gastrectomy specimens after fixation with formalin [33]. With the use of a 1.5-Tesla MRI device and a 4-cm-diameter loop coil, muscularis propria and serosa or subserosa showed isointense signal intensities but were outlined by subserosal fat tissue with contrasting signal intensity. The results were confirmed by another work group using a similar setup [37]. Identification of the serosa is necessary to securely differentiate between T2- and T3-stage gastric carcinoma. Although a detection rate of 88% for serosal involvement was achieved in this study, serosa as a single gastric wall layer was not clearly visualized. In seven cases with four to five visible gastric layers, a thin outer layer on T2-weighted sequences was detected and could possibly be identified as serosa or subserosa with subserosal fat tissue. This finding was inconsistent and varied in different T-stage carcinomas. This may be because of isointense signal intensity of muscularis mucosae and serosa or subserosa or the fact that the thickness of the serosa layer is not sufficient for secure identification [38]. It is not certain whether tumor invasion into or close to the serosa or subserosa layer changes its signal intensity presentation. Indirect detection by subserosal fat tissue seems possible, but in our experience, there is some variance in the thickness of subserosal fat tissue in gastric carcinoma specimens. One reason for this could be tumor cachexia.
An interesting learning point is reflected by the results of T staging. Knowledge of the gastric region where the tumor is located is important since T staging of the stomach depends on the gastric region. Tumors of the cardia and part of the fundus region where a serosal layer is missing are considered T2 whereas they would be T3 in other gastric regions. The study setup was intended to be as close as possible to a future in vivo setting with an MR endoscope, but tumor location and gastric region cannot be read on image data from gastrectomy specimens. An in vivo setting would enable investigators to acquire this information. After providing the tumors' gastric region, T staging accuracy improved to 75%. Thus, the gastric region of tumor location is an important fact for adequate staging of tumor invasion. While this study used an ex vivo model of gastric carcinomas and the amount of patients included could be higher, the entire range of T factors for gastric carcinomas is covered. Another limitation of this study is the missing congruence of lymph nodes present in the gastrectomy specimens due to surgical technique to those available for histopathology. This is reflected by N-factor staging results. An in vivo setting should be more accurate but poses new problems, such as motion artefacts due to patient or endoscope movement. Modern rapid MRI sequences and spasmolytic agents may be able to overcome these obstacles in an in vivo setting, but this is a goal for future studies. It is important to point out pitfalls of this imaging technique, as overstaging is a problem in many imaging modalities. Peritumor inflammation, micronodular affection of the serosal membrane, and diffuse-type gastric carcinoma were retrospectively identified as reasons for misinterpretation of tumor invasion. Overstaging occurred in 17%, with three T1 tumors not correctly classified. This is encouraging since all T1 tumors were detected as tumors but in two cases were classified as T2 tumors and one as T3. Only one incorrectly classified T2 tumor contributed to overstaging. This indicates that overstaging was not a problem of differentiation between T2 and T3 stages of disease.
It is necessary to focus on T1 carcinomas, as experience with T1 carcinomas in imaging modalities in Western countries is low due to the fact that most gastric cancers are diagnosed at an advanced stage. It is important to learn more about signal intensity and morphologic presentation of early gastric carcinomas on endoluminal MRI to improve detection rate. Endoluminal MR imaging provides enough detail to visualize a T1 tumor (Fig. 2). Endoscopic mucosal resection as one treatment option for early gastric carcinoma requires an imaging method that is able to visualize and identify these stages securely and provide information that is observer independent. Further studies should include a larger quantity of early stages of gastric carcinomas to analyze accuracy potential of endoluminal MRI. MR images provide information not obtainable by other imaging modalities. A gastric tumor can present with different appearances on T1-weighted imaging than on a T2-weighted imaging (Fig. 3). Depth of visualization of a method is essential for staging a gastric tumor, assessing its depth of invasion into gastric wall and into adjacent organs and structures, as well as depicting involved lymph nodes. Our image data can provide detailed information about gastric wall invasion as well as organ invasion (Figs. 2 and 4).
Fig. 4a, bT4 gastric tumor (intestinal type of Lauren classification, open arrows) on T2-weighted images of the same plane. Transition of normal gastric wall into tumor mass (white arrows). Pancreas (white arrowheads) adjacent to the gastric wall demonstrates depth of visualization (a). Tumor invasion into pancreas (black arrowheads) (b)
In this study, we have shown that our concept is functional and feasible for MRI of the stomach, and staging results comparable with other imaging modalities were achieved. Endoluminal MRI in combination with conventional MRI could assess local and regional imaging in one session, giving accurate information about local staging and metastatic spread of disease. Secondary contrast media should be evaluated for its use in improving gastric wall layer discrimination and identification as well as tumor demarcation. Additional studies are needed to assess the clinical feasibility of this coil concept in vivo for imaging of the upper gastrointestinal tract. High-resolution imaging of the pancreas could be another possible application. Today, most tumors of the stomach and esophagus are staged by conventional methods, such as endoscopy, EUS, or CT. Future prospects of endoscopic MRI may be limited to certain tumor entities, such as early or advanced carcinomas, but it could be able to answer additional specific clinical questions for relevant therapy decisions.
Summary Endoluminal MRI with the coil concept is feasible and applicable. T staging of ex vivo gastric carcinomas is possible. Results for T-factor staging are preliminary but promising, as they reflect the first experience with this technique. Image quality and resolution obtained with the endoluminal RF coil are convincing for future use in gastrointestinal imaging. Limitations of this study include missing congruence in quantity of lymph nodes for N staging, a limited amount of some T-stage gastric carcinomas, and the ex vivo setting. Taking the limitations into account, the coil design should be investigated in an in vivo setting after assessing safety aspects to evaluate the prospects given by the ex vivo results. The clinical potential may be limited by providing a staging tool for certain tumor entities. With more experience in endoluminal MRI and interpretation of endoluminal image data, its use could be extended toward other fields in gastrointestinal imaging.

coils
magnetic resonance imaging
stomach neoplasms
neoplasm staging
experimental study


How valid are current diagnostic criteria for dental erosion?

In principle, there is agreement about the clinical diagnostic criteria for dental erosion, basically defined as cupping and grooving of the occlusal/incisal surfaces, shallow defects on smooth surfaces located coronal from the enamel–cementum junction with an intact cervical enamel rim and restorations rising above the adjacent tooth surface. This lesion characteristic was established from clinical experience and from observations in a small group of subjects with known exposure to acids rather than from systematic research. Their prevalence is higher in risk groups for dental erosion compared to subjects not particularly exposed to acids, but analytical epidemiological studies on random or cluster samples often fail to find a relation between occurrence or severity of lesions and any aetiological factor. Besides other aspects, this finding might be due to lack of validity with respect to diagnostic criteria. In particular, cupping and grooving might be an effect of abrasion as well as of erosion and their value for the specific diagnosis of erosion must be doubted. Knowledge about the validity of current diagnostic criteria of different forms of tooth wear is incomplete, therefore further research is needed.
The process of diagnosis and current criteria for dental erosion
From the chemical view, the aetiology of dental erosion can be defined as the chronic exposure of the teeth to extrinsic or intrinsic acids under the condition that the oral fluids are undersaturated with respect to tooth mineral [23, 26]. Under in vitro conditions without physical impact, teeth demineralise centripetally (Fig. 1), a feature of substance loss which is normally not observed in the mouth. In fact, the multitudes of physical and chemical assaults occurring during a lifetime result in a more or less characteristic pattern of tooth wear. The classification of wear is therefore made from morphological features which are frequently seen clinically. The tooth morphology as apparent after eruption is the idealised status, deviations of which, if not caries or trauma, are diagnosed as (erosive) tooth wear. Various forms of wear including dental erosion are listed in the International Classification of Diseases [52] thus defining them as a disease (for critical discussion of this notion see [12]).
Fig. 1Effect of the continuous exposure of a human third molar to 10% citric acid. The amorphous, centripetal tissue loss is obvious (a unaffected tooth, b tissue loss after 4, c 8, and d 12 h immersion time)
Looking at what “diagnosis” is, one will find mostly definitions like “identification of disease from signs or symptoms”, implicating that the physician or scientist “reads off” from the patient thus detecting the disease. Health and disease, however, is not a given condition, but is constituted by the theoretical concepts and the discursive practice the physician or scientist is subjected to [12]. That is to say, rather than reading off the disease from the patient, a pattern of criteria is projected onto the diagnosed subject which determines the diagnostic procedure and outcome. Following this approach, the diagnostic process, in a first step, is a theoretical concept ordering signs and symptoms to diseases which takes place within the configurative power of the discourses. In whatever discourse the physician acts, the act of clinical diagnosis, in a second step, is classification. The conclusion reached through this process is called “a diagnosis”. From this background, it becomes obvious that the diagnostic process must be accompanied by a recurrent reconsideration of its theoretical concepts and the reevaluation of the criteria used. The latter is what the paper aims to achieve.
The diagnosis of tooth wear in general and erosion in particular is made from its lesion characteristics, from the results of nutritional, medical and occupational analysis, and from dietary records. The diagnostic process can be more differentiated with the individual patient, whereas in field trials it is restricted to the classification of lesion shape.
Throughout the literature, there is more or less consensus about the aetiology of the various forms of tooth wear, the clinical criteria for dental erosion and its differential diagnosis [12, 14].
The early signs of erosive tooth wear appear as changes of the optical properties of enamel resulting in a smooth silky–shining glazed surface. When the tissue loss continues, changes in the original morphology occur. On smooth surfaces, convex areas flatten or concavities develop, the width of which clearly exceeds the depth. Lesions are located coronal from the enamel–cementum junction (CEJ) with an intact enamel rim along the gingival margin. On occlusal and incisal surfaces, rounding and cupping of the cusps and grooving of the incisal edges occur, and restorations may rise above the level of the adjacent tooth surfaces. In advanced cases, the whole occlusal morphology disappears.
The validity of these clinical criteria for erosion, however, has not been under critical consideration. Validity, in general terms, means the degree, to which a measurement measures what it purports to measure. For the issue addressed here, criterion validity is the relevant term, meaning the extent to which the measurement correlates with an external criterion under study. A further aspect of validity is concurrent validity. Concurrent validity means to which extent the measurement and the criterion refer to the same time [24]. In the case of erosion this would address the question if (a) the diagnostic criteria reflect lesions being an effect of an exposure to acids and (b) if the presence of characteristic signs is concurrent with an acid exposure.
The implementation of current diagnostic criteria
Considering how the diagnostic criteria for erosion were established, the literature reveals that it was individual clinical experience and case reports rather than systematic research. One of the first publications on the characteristics of acid induced tissue loss was in 1946 from Robinson [43] and in 1947 from Stafne and Lovestedt [47]. Robinson, whilst being in doubt about the aetiology of dental erosion, described the lesions as located on smooth surfaces and as wedge shaped, cup shaped, disk shaped, irregular in form, L- or U-shaped, or simply as small round depressions or larger surface lesions. It is not clear how these descriptions were established, but Robinson referred to a work from McClure and Ruzicka [31] describing the morphology of lesions of rats teeth after being fed with lactate and citrate drinking fluid.
Stafne and Lovestedt presented their observations in subjects with known acid exposure, amongst them 50 patients with frequent consumption of lemon juice. They did not give a concrete description of lesion shape, but attributed hypersensitivity, absence of stain and defects with rounded margins as effect of the action of the acids. Their most important sign of diagnostic value was the presence of fillings projecting above the surface of the tooth. In their publication, a number of clinical images were included, presenting lesions clearly matching current erosion criteria.
More than twenty years later, in 1970, it was Pindborg [40] who gave the often cited definition of erosion as being superficial loss of dental hard tissue by a chemical process which does not involve bacteria. He described the clinical signs of chemically-induced tissue loss as usually located to the gingival third of the facial surfaces, possibly also located at proximal surfaces, lesions to appear shallow, disc-shaped, smooth, polished, or scooped out. In contrast to abrasion, he attributed erosive lesions to be located evenly on the left and right side.
It appears noteworthy, that Pindborg, as well as Robinson, ascribed cupping of the cusps, loss of the occlusal morphology or loss of crown height, and incisal grooving to attrition which in their publications was defined as result of mastication.
It is probably Eccles and Jenkins [8, 10] who were the first to give a detailed and systematic description of the lesion characteristics and also suggested a system for classification. The basis of the development of the clinical criteria was a sample of 72 patients seen in the dental hospital over a period of 9 years [8]. All cases were thoroughly documented with respect to their medical and dietary history, that is, it was a group of subjects with known exposure to intrinsic or dietary acids. The findings derived from this group of subjects (Table 1) have been retained nearly unchanged until now. The main aspects are in general terms loss of surface contour, shallow concavities on smooth surfaces, cupping and grooving on occlusal/incisal surfaces and restorations rising above the level of the adjacent tooth surface.
Table 1Diagnostic criteria for dental erosion as outlined by Eccles and Jenkins [10] and Eccles [8]Diagnostic criteria for dental erosionInitialAbsence of developmental ridges of the enamel, smooth glazed surfaceAdvanced Facial/oral surfacesConcavities whose breadth greatly exceeds their depthLesion ovoid or crescentic in outline, concave in cross section orLesion entirely in the crown, irregular in outline, punched out appearance Occlusal/incisal surfacesSurfaces appear flattened, depression of the cusps (cupping) and on the incisal edges (grooving), edges of restorations raising above the level of the adjacent tooth surface
Conclusions from epidemiological studies using current diagnostic criteria
Current criteria, derived from a relatively small sample, have been applied in case reports [8, 9, 16, 32, 39, 50] and studies with risk groups [15, 17, 21, 25, 34, 38, 44, 48, 51]. Indeed, when used in subjects with known or strongly assumed exposure to acids, most studies revealed a higher prevalence of lesions in the exposed groups compared to the control groups (Table 2).
Table 2Prevalence of lesions in risk groups deriving from the use of current diagnostic criteria for dental erosion IndexGroup sizePrevalence risk groupPrevalence control groupIntrinsic acid exposureMeurman et al. [34] reflux diseaseEccles and Jenkins indexn = 11728/117 = 24%No control groupRytömaa et al. [44] eating disordersEccles and Jenkins indexn = 14022/35 = 63%12/105 = 11%Öhrn et al. [38] eating disordersLussi indexn = 13379/81 = 98%Minor, less severeIncisal/occlusalIncisal/occlusalGrade 1: 93%Grade 1: 73%Grade 2: 52%Grade 2: 23%BuccalBuccalGrade 1: 30%Grade 1: 19%Grade 2: 9%Grade 2: 6%PalatalPalatalGrade 1: 21%Grade 1: 10%Grade 2: 5%Grade 2: 0%Extrinsic acid exposureLinkosalo and Markkanen [25] vegetariansEccles and Jenkins indexn = 5216/26 = 60%0/26 = 0%Wiktorsson et al. [51] wine tastersEccles and Jenkins indexn = 1914/19 = 74%No control groupGanss et al. [15] raw food dietLussi indexn = 206127/130 = 98%66/76 = 87%
These observations support the finding that subjects with continuous exposure to acids have a higher rate of lesions with a specific characterisation. This is, however, not enough support for the assumption that, vice versa, subjects presenting with such defects must be exposed to acids.
Analytical epidemiological studies on random or cluster samples attempted to relate the occurrence of lesions with any of the known aetiological factors for erosion, but only few studies of this type have been published. Most of them include children or adolescents, but there is lack of studies on older population groups. Furthermore, off the few studies, some used the Tooth Wear Index (TWI [46]) which is not designed to assess dental erosion specifically. The overall findings (Table 3) are controversial since some authors found no or only a partial relation between aetiological factors and the occurrence or severity of lesions [2, 3, 5, 7, 20, 30, 35, 37, 49], whereas others revealed strong relationships [22]. In addition, a relation to the intake of yoghurt or other foodstuff which certainly has no erosive potential was mentioned [1, 27, 35].
Table 3Analytical epidemiological studies attempting to relate the occurrence of (erosive) wear to aetiological factors Index, group size, age and prevalenceConclusionJärvinen et al. [22]Eccles & Jenkins indexCitrus fruits: odds ratio (OR) 2Case-control, n = 100 eachSoft drinks: OR 413–83-year-oldsLussi et al. [27]Lussi indexSignificant relation to the consumption of fruit, acidic drinks, yoghurt, vomitingn = 41726–30- and 46–50-year-olds at least 36 and 43% resp. with any erosionBartlett et al. [5]TWI (Smith and Knight)No significant relation to drinks or other acidic foodn = 210Significant relation to heart burn11–14-year-olds57% had wear in enamel on more than 10 teethJaeggi et al. [20]Lussi indexNo relation to any aetiological factorn = 41719–25-year-olds at least 82% with erosionAl-Dlaigan et al. [1]TWI (Smith and Knight)Significant relation to drinks and fruit, but also to milk, yoghurt and beern = 41814-year-olds48% low, 51% moderate 1% severe lesionsAl-Majed at al. [2]TWI (Smith and Knight) modified for erosionNo association to erosive drinks for the total samplen = 862Significant association to frequency of drinks at night and duration of drinks retained in the mouth only in advanced cases (n = 95)12–14-year-olds95% with erosionMathew et al. [30]Lussi indexNo relation to the intake of sport drinksn = 30418–28-year-olds37% with erosionVan Rijkom et al. [49]Modified Lussi indexNo relation to acidic drinks and fruitsn = 40015–16-year-olds30% with visible smooth wearArnadottir et al. [3]Modified Lussi indexNo significant association to risk factorsn = 27815-year-olds72% grade 124% grade 25% grade 3Nunn et al. [37]TWI (Smith and Knight) modified for erosionNo significant association with dietary factorsn = 1726Significant relationship with gastro-oesophageal symptoms4–18-year-olds36, 56 and 34% with any erosion on buccal and palatal surfaces of the incisors, and first permanent molars resp.Dugmore and Rock [7]TWI (Smith and Knight) modified for erosionDrinking fizzy pop: odds ratio 1.59–2.52 depending on amount and frequencyn = 114912-year-oldsNo relation to eating apples, citrus fruit56% with erosionMilosevic et al. [35]TWI (Smith and Knight) on labial and lingual surfaces in front teeth, occlusal surfaces of first molarsNo association to apples, fresh orangesn = 2385Weak association (OR 1–1.4) to yoghurt, grapefruit, salad dressing, vinegar, fruit juice, fizzy drinks14-year-oldsStrong association to herbal/lemon tea (OR 3.97)53.5% with exposed dentine
There are many points of discussion for explanation. At first, (erosive) wear is the effect of various concurrent or past chemical exposures from different sources, the variety of which can hardly be covered by simple questionnaires, and especially in younger people the dietary intake and lifestyle might be open to variations. Furthermore, questionnaires may reflect only in part the dietary habits due to interpretation by the responder or seasonal changes in daily life habits. When the young age of the groups studied is considered, the determinants for dental erosion may not have acted for long enough, and, in addition, there might be considerable differences in the individual susceptibility to erosive demineralisation [15].
It must, however, also be taken into consideration that current diagnostic criteria might not be valid enough to really reflect the effect of a chronic acid exposure.
Taking into account that tooth wear is the result of various factors, the occlusal and incisal surfaces of teeth are not only exposed to acids but are particularly prone to physical impacts from mastication. From this background, the finding that many studies using erosion indices reveal that occlusal lesions are the most prevalent and that it is the first lower molar which is most affected [19], is of particular importance. Occlusal surfaces might be the only location exhibiting a relation between lesion severity and prevalence, and age [28] thus indicating a significant contribution of abrasion from mastication. Furthermore, particularly the teeth from ancient remains exhibit defects being strikingly of the same shape as those attributed to erosion today (Fig. 2).
Fig. 2a Occlusal aspect of a subject living on a raw food diet with multiple acid impacts, and a medieval subject b with an assumed abrasive diet (images a, b, and c samples from [13, 15]). Occlusal/incisal defects in a subject with chronic vomiting d and in a medieval subject c. The shape of lesions from predominantly erosive and predominantly abrasive aetiology is strikingly similar
Comparative studies on lesion characteristics of wear
Attempts have been made to characterise the shape of wear resulting from abrasion and erosion [6, 13].
A comparison of subjects with known exposure to a non-acidic but coarse diet and subjects with an acidic, but refined diet using silicon impressions revealed that in the former, the scooped out dentine was significantly shallower than in the latter. Furthermore, the deepest lesion region in teeth from subjects with abrasive diet was located at the functional cusps, whereas in teeth from subjects with an erosive diet, the deepest region of the defects was located more centrally. The authors concluded that in cases when the dentine is severely scooped out, the causative agent is most likely of erosive origin whereas scooping tends to be shallower when wear is caused by abrasion. The conclusion of the study was to suggest a quantitative diagnostic procedure by calculating the depth/breadth ratio for clinical differential diagnosis [6].
Another approach was to compare the shape of defects occurring in subjects with substantially different nutrition patterns [13]. The study included three groups of age matched individuals — randomly selected contemporary subjects, medieval remains and a group of subjects living on raw food diet. From the latter group, extensive information was available on their intake of acid food qualifying their nutrition as rather erosive. For the medieval group, an abrasive nutrition was assumed from knowledge about the general nature of the early medieval diet.
As to the smooth surfaces, the most interesting finding was that in the medieval group, no lesions were observed (Table 4). Even in cases with severe wear, the lingual and buccal aspects of the teeth appeared undisturbed and, in many cases, even developmental ridges were present. The lack of cervical defects is also reported by Aubry et al. [4] and Kaidonis (in this issue) and also inherently supported by the fact that the overwhelming number of anthropological studies on tooth wear only deal with occlusal and proximal wear and that the indices used there do not include criteria for cervical wear [11, 36]. There are, however, few studies reporting wear on lingual surfaces in archaeological remains [18, 41] and there is one publication discussing regurgitation as a possible aetiological factor [42]. In this study, 151 adult pre-Conquest British skulls were examined using the TWI. Indeed, buccal and lingual wear was observed to the same degree as in a contemporary comparison group, but cervical wear did not develop beyond criterion 0 in most individuals. In 20% of the skulls, however, a cervical wear to TWI score of 2–3 occurred. No information was given about the shape of the lesions, and from the images included, it appears that their characteristics would not match the current criteria for dental erosion.
Table 4Prevalence of lesions of defined shape in three groups (n = 100 each) of subjects with substantially different nutrition patterns [13] Abrasive diet (medieval group)Acidic diet (raw food group)Average western diet Incisal/occlusal surfacesIncisors/caninesGrooving93%96%90%n.s. Molars/premolarsShallow cupping (<0.5 mm)87%59%47%p < 0.001Deep cupping (>0.5 mm)78%45%4%p < 0.0001 Smooth surfaces (all teeth)Concavity coronal to the CEJ0%63%8%p < 0.0001V-shaped defects0%38%10%p < 0.0001
In contrast to the findings in the medieval group, shallow defects located coronal from the CEJ were considerably prevalent in the raw food group (Table 4, Fig. 3b), whereas in the western diet group, the prevalence of this kind of lesions was much lower and corresponds to its general prevalence in Germany [45].
Fig. 3a Buccal aspect of teeth 44–47 with significant loss of crown height, but without any lesion in a medieval remain [13] with severe generalised occlusal wear c. b Occlusal defects in a subject living on a raw food diet with a high intake of acidic food [15]. The shape of the occlusal lesions is similar to c, but combined with shallow lesions with intact cervical rim lesions. d Same subject with Fig. 4b with an initial buccal lesion
As to the occlusal/incisal surfaces, grooving and cupping was common in all groups even though most often in the medieval group, followed by the raw food group, and the western diet group.
The conclusion from this study was that shallow defects on smooth surfaces might be a valid criterion for dental erosion, whereas cupping, and especially incisal grooving, was common in all groups and therefore not valid for a differential diagnosis.
The similarity of occlusal/incisal defects in all groups might be explained from a tribological view [29]. Wear, as a result of abrasion, occurs as three body wear that means the intervention of an abrasive slurry or bolus. During mastication, the abrasive tends to hollow out softer surface regions. Cupping or grooving can occur when deeper enamel regions with lower microhardness [33] are exposed or when the dentine is reached. In the case of erosion, tissue loss is on one hand caused by direct dissolution of mineral but also due to an increased susceptibility of acid softened surfaces to physical wear. In these cases, also a non- or less abrasive bolus could cause similar defects when acting on acid weakened surfaces.
Hence, the occlusal/incisal substance loss observed in individuals prone to dietary acids may be explained as pronounced abrasion/demastication of acid softened surfaces. Therefore, it is questionable if the occlusal morphological criteria used for the diagnosis of occlusal erosion per se are valid.
Even though there are often striking similarities between lesions of predominantly abrasive or predominantly erosive origin, there is, on the other hand, often also considerable variation in lesion shape in cases of erosion. The morphology of occlusal lesions in subjects with known exposure to acids varies from deep hollowing out of the cusps to totally amorphous loss of the occlusal structure even in subjects with a similar dietary history (Fig. 4).
Fig. 4Occlusal tissue loss from erosive aetiology can also be of strikingly different shape either presenting as deeply hollowed out lesions (a subject with raw food diet [15], b subject with excessive consumption of orange juice) or as amorphous generalised tissue loss affecting the entire surface (c, d subjects with excessive consumption of erosive drinks). An interesting feature is seen in an adolescent with a history of severe anterior open bite with only the molars being in function e Substance loss occurred from excessive consumption of a cola type drink. In the premolars, dentine is proud of the surface. f Hollowing out the entire occlusal surface with enamel remnants in the centre, aetiology is the excessive consumption of sport drinks
Conclusion
The validity of current diagnostic criteria for dental erosion has not been systematically studied, even though there is consensus about their definition.
The following conclusions can be drawn:
Grooving of incisal surfaces is a common phenomenon and possibly the effect of any physical or chemical impact. It should be considered to abandon grooving of anterior teeth and canines as a clinical criterion for dental erosion.Shallow defects located coronal from the CEJ may predominantly occur as effect of chronic acid exposure and might be pathogonomic for dental erosion. This assumption is supported by the finding that these types of lesions are not present in ancient remains even in cases of severe wear.Cupping of cusps is the most uncertain criterion because it can be an effect of abrasion as well as of erosion. In industrialised countries, abrasion is not expected to be a significant factor in young people. Cupping occurring at younger ages can therefore be an effect of erosion. At older ages, however, physical and chemical impacts add up increasingly and cupping will therefore be of little diagnostic value in adults.
These conclusions are drawn from very few studies; therefore systematic research on this issue is needed. Nevertheless, there is enough support for a criticism of current diagnostic criteria particularly in the light of the development of a new index.

validity criteria erosion epidemiology diagnosis