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How to study the location and size of rectal tumors that are candidates for local surgery: Rigid rectoscopy, Magnetic resonance imaging, En-dorectal Utrasound or colonoscopy? An inter-observational study
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31 July 2023
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02 August 2023
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Abstract
Background. Rectal Magnetic Resonance Imaging (MRI) is a key test in advanced rectal cancer and in the preoperative staging of a lesion suitable for transanal endoscopic surgery (TES). MRI is not operator-dependent, but its results when determining anatomical landmarks are variable.
Method. Observational study of inter-observer concordance regarding four diagnostic tests used to establish the anatomical characteristics of rectal lesions: colonoscopy, rectal ultrasound (EUS), rectal MRI, and intraoperative rigid rectoscopy (IRR) in patients scheduled for transanal endoscopic surgery (TES) with curative intent. This inter-observational study assessed the concordance between four expert radiologists regarding the topographic evaluation by means of rectal MRI of lesions under consideration for TES.
Results. Fifty-five consecutive rectal tumors were studied. For most of the items, the correlation between IRR and colonoscopy or EUS was generally very good (intraclass correlation coefficient -ICC-)>0.75), although the correlation between MRI and IRR in relation to size by quadrants (ICC=0.092) and location by quadrants (ICC=0.292) was weak. The ICC for the other items obtained excellent correlations: Kappa index >0.80 for all items except for the distance from the peritoneal reflection to the anal verge, where it was merely good (IK=0.606).
Conclusions. The anatomical description of rectal lesions that are candidates for TES provided by means of IRR, EUS, colonoscopy and MRI is reliable. The MRI is less reliable, but in the hands of expert radiologists, the anatomical study of rectal lesions is accurate and reproducible.
Keywords:
Subject: Medicine and Pharmacology - Oncology and Oncogenics
1. Introduction
A third of colorectal cancers present non-negligible morbidity and mortality [0,2]. The initial study of the rectal lesion is the basis for defining the best treatment. Depending on the TNM at diagnosis, the range of cancer treatment includes neoadjuvant, surgical and adjuvant approaches
In early locoregional stages without the presence of distant metastases (M0), the initial study of the tumor is key to determining the best surgical strategy, which may range from local surgery through transanal endoscopic surgery (TES) to total mesorectal excision (TME). This initial study also determines whether the patient is eligible for neoadjuvant treatment, or for a combination of neoadjuvant treatment with TES in the initial stages (i.e., T2-T3 without pathological nodes in the preliminary study) [3]. The initial diagnostic test is usually colonoscopy, which provides topographic information about the tumor (location, height, appearance) and obtains biopsies for confirmation in the pathology study. Endorectal ultrasound (EUS) and rectal magnetic resonance imaging (MRI) are the diagnostic tests used for tumor staging (T) and suspicion of lymph node involvement (N) [4,5]. Each test provides relevant information, but their conclusions are not definitive.
A prerequisite for performing EUS is rigid rectoscopy, which allows an assessment of the height and location of the rectal lesion. The EUS evaluates the T with an accuracy of 63-95% and the N with an accuracy of 63-85% [1,], but its main drawback is the fact that it is operator-dependent [2,6]. Rectal MRI provides topographical data and evaluates T and N [7]. It also gives us information about the peritoneal reflection and the radial margin [8].
However, the anatomical references used for surgery differ from those used by radiologists to interpret MRI findings. The interpretation of these findings is a complex task and requires considerable experience, and even between expert observers there may be disagreement [9]. Furthermore, several anatomical guidelines are used to analyse the images obtained by MRI, without any clear consensus on the one that is the most suitable for this purpose [10].
Local surgery of rectal adenocarcinoma by TES is indicated in T1 tumors with favorable pathological characteristics [11] and a distance from the superior or proximal edge less than 18-20 cm [12]. For the satisfactory performance of the TES, precise information is needed on the height of the tumor in relation to the anal verge. Its relation to the peritoneal reflection must also be assessed, due to the risk of perforation of the peritoneal cavity [13]. The importance of the height of the tumor is clear because rectal tumors located above or below 5 cm have a different pathological response [14]. The location by quadrants is also important for the positioning of the patient on the operating room table.
In tumors with an indication for TES, confirmation of the exact topographic characteristics of the tumor is required prior to surgery. This is performed by intraoperative rigid rectoscopy (IRR) [11], in the initial supine position. Once the exact location of the lesion by quadrants has been determined, the patient's position may be changed accordingly.
Based on all these premises, and taking into account the topographic study of rectal lesions performed using colonoscopy, EUS, and MRI, the main objective of the study is to assess the concordance of these tests with respect to IRR. The secondary objectives are to answer the following questions: Is rectal MRI reliable enough to avoid systematic performance of IRR? Is MRI more reliable than colonoscopy and EUS for determining the topographic characteristics of the tumor? Are there differences in the interpretations of rectal MRI made by expert radiologists regarding these topographic characteristics?
2. Materials and Methods
2.1. Study Design
Observational study of inter-observer agreement regarding patients undergoing TES with curative intent consecutively between four diagnostic tests: colonoscopy, EUS, rectal MRI and IRR. To determine the variability between radiologists’ interpretations, an inter-observer agreement study was carried out of four radiologists who are experts in rectal MRI.
The data were recorded prospectively and analysed retrospectively. Computerized data management was carried out using Microsoft® Access 2003, introduced in a protected format.
2.2. Patients and Settings
The study was carried out at the Parc Taulí University Hospital in Sabadell. All 55 patients included had undergone transanal endoscopic surgery with curative intent at the Coloproctology Unit.
All rectal tumors had been submitted to the preoperative study protocol in place at our center [11]. In this protocol, tumors that are candidates for TES after preoperative FCS, EUS, and rectal MRI tests are classified into five groups of preoperative surgical indication: group I, with curative intent (with preoperative biopsy of adenoma), which after EUS (us) and magnetic resonance (mr) are staged as us-mr T0-1 and us-mr N0; group II, with curative intent (preoperative biopsy of low-grade adenocarcinomas), us-mr T0-1 and us-mr N0; group III, consensus indication (low-grade adenocarcinomas), us-mr T2 and us-mr N0, who reject radical surgery; group IV, palliative indication and group V, atypical indications [15].
The colonoscopies were performed by the gastroenterologists at our center. EUS and rigid rectoscopy were carried out by surgeons from our colorectal surgery unit, and rectal MRIs were assessed by expert radiologists.
In all patients with an indication for TES, IRR was performed by the surgeon prior to the insertion of the TEM/TEO equipment with the patient in supine position (Figure 1). All the variables related to the tumor were checked at this stage (size, morphology, location by quadrants, height relative to the anal verge of the proximal and distal edge of the lesion). IRR is considered the gold standard for the topographic study of rectal lesions [8,11].
2.3. Inclusion Criteria
Patients with indication of curative TES in preoperative groups I and II described above; lesions less than 15 cm from the anal verge.
2.4. Exclusion Criteria
Patients in preoperative indication groups III, IV and V; patients who, after intraoperative evaluation of possible TES, underwent abdominal surgery because TES was deemed technically impossible; patients who, for technical or patient-specific circumstances, did not undergo any of the three tests under study.
2.5. Preoperative Preparation, Surgical Technique
All patients with an indication for TES underwent antegrade mechanical colon preparation together with antibiotic and thromboembolic prophylaxis according to the protocol [11]. Anesthesia was mainly general, except when the anesthesiologist recommended spinal anesthesia. The techniques used for local excision were either TEM (Richard Wolf, Knittlingen, Germany) or transanal endoscopic operation (TEO, Karl Storz GmbH, Tüttlingen, Germany) [16].
2.6. Study Variables
Inter-observer study of the four tests: FCS, EUS, rectal MRI, IRR
Topographic variables of the tumor: height of the lesion with respect to the anal verge; the quadrant occupied by the lesion; lesion size; lesion size by quadrants.
Inter-observer study involving four expert radiologists in rectal MRI:
Distance from the tumor to the mesorectal fascia; distance from peritoneal reflection to anal verge; distance from the lower margin of the tumor to the anal verge; distance from the upper margin of the lesion to the anal verge; distance from the upper margin of the tumor to the peritoneal reflection; distance from the lower margin of the lesion to the peritoneal reflection; distance to the radial margin or mesorectal fascia.
2.7. Statistical Analysis
A sample of 55 patients was assessed. A large sample (above 50) was needed to ensure that the concordance analysis obtained results with the highest possible validity.
The statistical analysis was performed using the SPSS version 26 program (SPSS, Inc, Chicago, Illinois).
In the interobserver agreement analysis for categorical dichotomous variables, Cohen's Kappa index (KI) was used, which adjusts the effect of chance on the proportion of the observed agreement. For the interobserver agreement analysis of the continuous variables, Fisher's intraclass correlation coefficient (ICC) was applied. The ICC allows evaluation of the general agreement between two or more measurement or observation methods based on an analysis of variance (ANOVA) model with repeated measures.
The Kappa index and Fisher's ICC were qualitatively interpreted as: poor or weak for values less than 0.40; moderate, for values between 0.41 and 0.60; good, between 0.61 and 0.80; and very good for values greater than 1.
Two analyses were carried out: first, an interobserver analysis between the gold standard (IRR) and each of the diagnostic tests (colonoscopy, EUS and rectal MRI), and the analysis between them and the ICC; second, an analysis of the parameters studied in the pelvic MRI according to four expert radiologists using the ICC.
3. Results
Of the 55 consecutive patients with an indication for TES selected with curative intent, one patient was excluded because his indication was made following endoscopic polypectomy. In this patient, the pathology result indicated adenocarcinoma with involvement of a resection margin. No lesion was identified by EUS or MRI; a minimal scar was observed, which was removed by TES. No lesion was found in the definitive pathological analysis. Therefore, the total sample studied comprised 54 patients [17].
Table 1 shows the demographic characteristics, the features of the tumor identified by the intraoperative rectoscopy, and the pathology results of the lesions. The results are characteristic of a sample of patients and tumors indicated for TES with curative intent: a predominance of males (34, 63%), median tumor size 4 cm (IQR 50) (range: 1-9), location by quadrants mainly posterior (23, 42.6%) and a main indication of adenomas in 38 (70.4%) patients.
Table 2 shows the results of concordance using Cohen's Kappa Index between the gold standard (IRR) and the rest of the tests (MRI, EUS, and colonoscopy) and the concordance using Fisher's ICC of the four tests for the same measure. Concordance was very good in the distance from the lower margin of the tumor to the anal verge, and in the KI between IRR and rectal MRI, EUS and colonoscopy. Likewise, the correlation of the ICC among all the tests was excellent (0.969, 95% CI: 0.948-0.982).
In the topographic study of the location of the lesion by quadrants, the KI between IRR and rectal MRI obtained a weak correlation. The correlation between the KI and IRR and EUS was good, and between the KI and IRR and colonoscopy was very good.
In the evaluation of the size of the lesion by quadrants, the KI between IRR and rectal MRI presented a weak correlation. The KI obtained a very good correlation between IRR and EUS, and a moderate one between IRR and colonoscopy. The ICC for the correlation between all tests was not performed for this item.
Finally, in assessing the size of the lesion, the correlations of the KI between IRR and rectal MRI and between IOR and colonoscopy were good. The KI between IRR and EUS obtained a very good correlation. The ICC of all the tests for this item was excellent.
Table 3 shows the results of calculating Fisher’s ICC to evaluate the correlation between four expert radiologists for the analysis of a rectal MRI. In total, 50 different rectal MRIs were analyzed. In most of the variables (distance from the tumor to the mesorectal fascia, distance from the lower margin of the tumor to the anal verge, distance from the upper margin of the tumor to the anal verge, distance from the upper margin of the tumor to the peritoneal reflection, distance from the lower margin of the tumor to the peritoneal reflection, distance to the radial margin or mesorectal fascia) excellent correlations were observed, except in the case of the distance of the peritoneal reflection to the verge, where it was merely good.
4. Discussion
The study of a rectal lesion includes digital rectal examination, rigid rectoscopy, EUS, colonoscopy, rectal MRI and thoracoabdominal CT [2,4]. These tests identify certain characteristics that are essential for diagnosing lesions that may be candidates for transanal endoscopic surgery. After the biopsy, and once the benign or malignant nature of the lesion has been established, it is important to determine its height with respect to the anal verge, its size, and its location according to the quadrant. In this setting, rigid rectoscopy is considered the gold standard, and is performed in the operating room with the patient under general or local anesthesia. The present study aims to assess the reliability of the topographic findings obtained with the other techniques, namely EUS, colonoscopy, and MRI scans.
Colonoscopy is the examination of choice for the diagnosis of colon and rectal lesions. The quality indicators of a colonoscopy are: complete examination; the time between colonoscopies; the size of the resected lesions, the definition of the degree of colon cleansing [18]. However, the measurement of the height of the lesion, especially in the rectum, sigma and left colon, is not always accurate; frequently, the colonoscopy report of a lesion’s height is not borne out by the results of the rigid rectoscopy. From the point of view of surgical strategy, this is an extremely important issue.
There is little room for maneuver with tumors in the rectum, where every centimeter counts. Perhaps unexpectedly, our study showed very good agreement between FCS and rigid rectoscopy for determining the height of the lesion, the quadrant it occupies, and its size. The agreement for size by quadrants was moderate. These results show that the test has good reliability compared to the gold standard.
Endorectal ultrasound is operator-dependent, although with experienced raters the reliability of the test increases. EUS has good precision for the diagnosis of tumors in the initial stages, given its ability to correctly differentiate the distinct layers of the rectum, though its assessment of lymph node involvement is less accurate [1,5]. EUS can determine the size of the lesion, the quadrant it occupies, and therefore the size by quadrants. There is no consensus on its ability to determine the height of the lesion, but this measurement can be made by rigid rectoscopy which is performed before the introduction of the transanal ultrasound [1,19]. The results of our study confirm a very good ICC in all the topographic items.
The characterization of a rectal lesion by MRI is complex. The best way to describe these lesions and their anatomical relationships is by following a pre-established schema [8,20]. It is important to determine the distance of the tumor from the anal verge in order to establish its location in the upper, middle or lower rectum, and also its distance from the radial or circumferential margin, given that its proximity to the mesorectal fascia implies a worse prognosis [21,22]. Determining the location of the tumor with regard to the peritoneal reflection and the presence or absence of extramural venous involvement can allow an accurate assessment of the sphincter apparatus and the pelvic floor.
Regarding T staging, one of the limitations of rectal MRI is its poor ability to differentiate between a T1 (involvement of the submucosa) and a T2 (involvement of the muscularis propria) due to its difficulty in differentiating between these two sites [19,20,23]. On the other hand, it can correctly define whether the tumor is a superficial or deep T3, and whether it affects the visceral peritoneum or progresses beyond the rectum (T4). Similarly, rectal MRI is a good tool for the study and detection of lymph nodes suspected of malignancy.
In this study we found a very good correlation between MRI and rigid rectoscopy for defining the height and size of the lesion, but not to determine the size by quadrants of the lesion neither its location by quadrants. Therefore, the performance of IRR could not be avoided by the use of MRI alone, since the quadrant occupied by the lesion cannot be well characterized, and this information is important in the surgical planning of TES.
The discrepancies between radiologists’ interpretations of rectal MRI are well known [8]. In our study, one of the secondary objectives was to assess the variability regarding expert radiologists’ impressions of the topographic characteristics recorded in rectal MRI. In fact we found that the agreement between our four radiologists on the anatomy of the lesion and its location from the anal verge, the peritoneal reflection and the radial margin was excellent, and was good for the distance from the peritoneal reflection to the anal verge.
Regarding the issue of whether the MRI findings provide enough information to make IRR unnecessary, we conclude that the judgment of an expert radiologist to characterize a rectal lesion is reliable, but that, even so, IRR cannot be avoided.
Our results did not suggest that MRI is more reliable than colonoscopy and EUS for assessing the topographic characteristics of the tumor. Evaluating the distance of the tumor from the anal verge and its size may be equivalent (the ICC between MRI, FCS, EUS and IRR was excellent), but MRI had a weak KI in comparison with IRR as it failed to take into account the location and size by quadrants.
The findings of this study suggest that IRR could be avoided by using the joint results of EUS, FCS, and MRI. Before each EUS, a rigid rectoscopy is already performed and the agreement between the two techniques is very high. If the results are discordant, however, IRR is necessary.
Limitations of the study/Future lines:
Some centers do not have access to EUS and MRI is the only diagnostic technique available for rectal lesions. In view of the limitations of MRI for differentiating between a T1 and a T2, and even sometimes between a T2 and a superficial T3 [23] the use of EUS can further refine the diagnosis of the tumor stage. The agreement between the expert radiologists at our center was good or excellent. We now plan to carry out an inter-observational study to assess whether our radiologists are able to differentiate a T1 from a T2 by means of MRI, comparing the results with those obtained with EUS.
5. Conclusions
The anatomy of rectal lesions that are candidates for TES can be reliably assessed by IRR, EUS, colonoscopy and MRI. The topographic data obtained by EUS (bearing in mind that it is combined with rigid rectoscopy) and colonoscopy can serve as a reference to avoid an IRR, but this is not so in the case of results obtained by MRI. On the other hand, expert radiologists’ assessment of the anatomy of rectal lesions by MRI is reliable.
Author Contributions
Conceptualization: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Methodology: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Validation: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Formal analysis: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Investigation: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Resources: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Data curation: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Writing—original draft preparation: Anna Serracant, , Xavier Serra-Aracil. Writing—review and editing: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Visualization: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Supervision: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil. Project administration: Anna Serracant, Xavier Serra-Aracil. All authors have read and agreed to the published version of the manuscript: Anna Serracant, Eva Ballesteros, Noemi Montes, Marta Sola, Francesc Novell, Beatriz Consola, Xavier Serra-Aracil.
Funding
“This research received no external funding”
Institutional Review Board Statement
Study approved by the local Institutional Ethics Committee (CEIC: 2016-636) and adapted to the criteria of the Declaration of Helsinki.
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
The computerized data management was carried out using Microsoft® Access 2003. The data were entered in a relational database and in a protected format
Acknowledgments
We thank the rest of the members of the Coloproctology Unit for applying the study protocol. We thank Cristina Gomez Vigo for correcting the manuscript and Michael Maudsley for helping with the English..
Conflicts of Interest
The authors declare no conflict of interest
Source of support
No financial support was required, since this study was an evaluation of habitual clinical practice.
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Table 1.
Patients’ demographic and pre-operative variables (in surgery).
| Variables | Results (n=54 patients) | ||
|---|---|---|---|
| Demographic Preoperative |
Age (median-IQRs-range) years | 66 (IQR 17) (range: 42-87) | |
| Sex | |||
| Male | 34 (63%) | ||
| Female | 20 (37%) | ||
| Tumor-related (in surgery) | Distance from distal margin to anal verge (median-IQR-range) cm | 7 (IQR: 4.3) (range: 3-15) | |
| Distance from proximal margin to anal verge (median-IQR-range) | 10 (IQR: 5) (range: 4.5-16) | ||
| Size (median-IQRs-range) | 4 (IQR 50) (range: 1-9) | ||
| Size per quadants | |||
| Lesion morphology | Flat | 18 (33.4%) | |
| polypoid | 16 (29.6%) | ||
| Sessile | 17 (31.5%) | ||
| Ulcerated | 6 (5.6%) | ||
| Location by quadrant | Anterior | 15 (27.8) | |
| Left lateral | 10 (18.5%) | ||
| Right lateral | 6 (11.1%) | ||
| Posterior | 23 (42.6%) | ||
| Indication for surgery | I | 38 (70.4%) | |
| II | 9 (16.7) | ||
| III | 7 (13%) | ||
| Pathology | Adenomas | 39 (72%) | |
| Adenocarcinoma | T1 | 11 (20.4%) | |
| T2 | 2 (3.7%) | ||
| T3ab | 2 (3.7%) | ||
Table 2.
Shows the results of concordance using Cohen's Kappa Index.
| Cohen’s kappa index (95% CI)/interpretation | Interclass correlation coefficient (95% CI)/interpretation | |||
|---|---|---|---|---|
| Intraoperative rectoscopy (IRR) |
MRI | EUS | Colonoscopy | |
| 0,870 (0.757-0.931) Very good |
0.981 (0.968-0.989) Very good |
0.872 (0.770-0.928) Very good |
0.969 (0.948-0.982) Excellent |
|
| Location by quadrants | 0.292 (0.023-0.396) Débil |
0.746 (0.655-0.881) Good |
0.913 (0.788-0.996) Very good |
- |
| Size by quadrants* | 0.092 (0.005-0.174) Débil |
0.815 (0.722-0.913) Very good |
0.439 (0.333-0.594) Moderate |
- |
| Lesion size | 0.758 (0.516-0.88) Good |
0.805 (0.627-0.898) Muy-good |
0.660 (0.276-0.839) Good |
0.922 (0.869-0.957) Excellent |
Table 3.
Shows the results of calculating Fisher’s ICC to evaluate the correlation between four expert radiologists for the analysis of a rectal MRI.
Table 3.
Shows the results of calculating Fisher’s ICC to evaluate the correlation between four expert radiologists for the analysis of a rectal MRI.
| Measurement evaluated | ICC (interclass correlation coefficient) | 95% confidence interval | Interpretation |
|---|---|---|---|
| Distance from tumor to mesorectal fascia | 0.817 | 0.539-0.948 | Excellent |
| Distance from peritoneal reflection to anal verge | 0.606 | 0.341-0.786 | Good |
| Distance from the lower margin of the tumor to the anal verge | 0.969 | 0.948-0.982 | Excellent |
| Distance from the upper margin of the tumor to the anal verge | 0.958 | 0.93-0.976 | Excellent |
| Distance from the upper margin of the tumor to the peritoneal reflection | 0.724 | 0.498-0.863 | Excelente |
| Distance from the lower margin of the tumor to the peritoneal reflection | 0.918 | 0.852-0.959 | Excellent |
| Distance to the radial margin or mesorectal fascia | 0.836 | 0.565-0.958 | Excellent |
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