University of Pisa
Department of Translational Research and New
Technologies in Medicine and Surgery
Residency program in Diagnostic Radiology
(2016-2020)
Chairman: Prof. D. Caramella
Rectal cancer staging: comparison between the 2012 and 2016
MRI report templates proposed by the ESGAR
Supervisors Candidate
Prof. Davide Caramella Dr.ssa Kathrine Bani Dr. Piero Boraschi
ABSTRACT
Purpose
The purpose of our study was to compare the 2012 and 2016 MRI report templates and recommendations proposed by the ESGAR for T and N staging of rectal cancer and for MRF status; moreover, we evaluated the possible role of DWI.
Materials and Methods
A series of fifty-six patients affected by rectal cancer were retrospectively included in our study; twenty-five out of them underwent directly to surgical treatment (Primary Staging group) whereas the remaining thirty-one had undergone neo-adjuvant chemo-radiotherapy (nCRT) before surgery (Restaging group). Patients belonging to both groups underwent to 3T MRI examination for local staging before surgery while patients of Restaging group underwent to MRI examination even before the beginning of nCRT. Operative specimens were used as standard of reference for determination of T and N stage, Mesorectal Fascia (MRF) status and Extramural Vascular Invasion (EMVI). The imaging protocol employed T2-weighted sequences in axial, sagittal, coronal and the “true axial” planes and Diffusion Weighted MR images. All MR examinations were interpreted blindly by two radiologists with 20 years and 4 years of experience, respectively, according to 2012 ESGAR and 2016 ESGAR guidelines, to evaluate TN stages, MRF status and EMVI. The agreement between MRI parameters and hystopathological findings was assessed by using the Cohen’s kappa statistics.
Results
In the Primary Staging group we found moderate agreement between MRI-T Stage and the standard of reference for the expert reader according to 2012 and good agreement according to 2016 ESGAR guidelines; moderate agreement was found for the resident according to both 2012 and 2016 ESGAR guidelines. For N Stage we found moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016; poor agreement was found for the resident according to 2012 ESGAR guidelines and fair agreement according to 2016 ESGAR guidelines.
For MRF status we found very good agreement between MRI staging and the standard of reference for the two readers according to both guidelines while as regards EMVI the agreement is moderate for the expert reader and fair for the resident. In the Restaging group we found moderate agreement between MRI-T Stage and the standard of reference for the expert reader according to both 2012 and 2016 ESGAR guidelines; fair agreement was found for the resident according to 2012 ESGAR guidelines and moderate according to 2016 ESGAR guidelines. For N Stage there is a moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016; fair agreement was found for the resident according to 2012 ESGAR guidelines and moderate according to 2016 ESGAR guidelines. For MRF status there is a poor agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016 guidelines; fair agreement was found for the resident according to both 2012 and 2016 guidelines while as regards EMVI the agreement is fair for the expert reader while there is no agreement for the resident.
Conclusions
Our data confirm that MRI has a crucial role in the staging and restaging of rectal cancer. Both 2012 and 2016 ESGAR structured MRI report templates are reliable tools to assess the radiological T and N stage of rectal cancer, especially for non-expert readers. The 2016 report template is more accurate in estimating T and N stage in the primary staging group, whereas no significant improvement was observed in the Restaging group of patients.
Introduction
Magnetic Resonance Imaging (MRI) plays a pivotal role in the management of patients with rectal cancer as it is recommendend by National Comprehensive Cancer Network International (NCCN) guidelines [1]. The correct staging of rectal cancer is of high relevance since the treatment options depend on the stage at presentation [1]. In the primary staging MRI is crucial to identify those patients who need neoadjuvant chemio-radiation therapy (nCRT) from those who can be directed towards surgery according to important features of prognosis such as the depth of invasion (T stage), lymph node involvement (N stage) and the relationship between tumor and mesorectal fascia (MRF status) [1]. Besides MRI allows to evaluate other important marker of aggressiveness such as vascular invasion (EMVI), local peritoneal involvement and, for tumor of lower rectum, the relationship with anal sphincter complex [2].
MRI is a reliable tool even in the assessment of response to preoperative treatment, in order to identify the best treatment options [3].
In 2012 the European Society of Gastrointestinal and Abdominal Radiology (ESGAR) developed internationally accepted guidelines for the correct MRI rectal cancer staging [3]. MRI showed high accuracy for MRF status and T staging with MRI main pitfalls lying in the assessment of T1 lesions since the submucosal layer is not visualized on MRI and in the differentiation between T2 from T3 tumors at the immediate interface between muscolaris propria and the extramural fat [4]. Anyway, as regards (y)N stage, MRI showed less accuracy in the identification of metastatic lymphnodes with the risk of overstaging which could mean unnecessary preoperative treatment. [5, 6, 7]. 2012 ESGAR guidelines did not identify a dimensional significant cut-off and stressed the role of morphological criteria to help characterization with well-known inaccuracies affecting nodal staging [3]. Besides, DWI was recommended only for the evaluation of response to neoadjuvant therapy in terms of yT staging without recommendations for T and (y)N staging and (y)MRF status [3].
In 2016 ESGAR updated these guidelines introducing practical criteria including both size and morphology in order to improve nodal staging [8]. As regards the role of DWI, the panel agreed that diffusion-weighted MRI should be performed to evaluate the yT stage after nCRT; no consensus was reached for the role of DWI in the evaluation of other items such as primary T-staging, nodal restaging and EMVI suggesting a potential role in the evaluation of Mesorectal fascia status after neoadjuvant therapy [8].
recommendation for reporting with the introduction of a structured template [8].
The purpose of our study was to compare the 2012 and 2016 MRI report templates and recommendations proposed by the ESGAR for T and N staging of rectal cancer and for MRF status; moreover, we evaluated the possible role of DWI.
Materials and Methods
A written informed consent was obtained from all the patients included in our study group. This single-institution retrospective study was approved by our Institutional Ethical Committee.
Patients
A series of fifty-six patients (twenty women and thirty-six men; mean age: 64 years ±15) affected by rectal cancer were retrospectively included. Twenty-five out of fifty-six patients underwent directly to surgical treatment (Primary Staging group), whereas the remaining thirty-one had undergone nCRT before surgery (Restaging group).
The inclusion criteria were:
1) histologically confirmed rectal adenocarcinoma;
2) patients whose MRI protocol was completed and DW images have been acquired; 3) patients who performed MR examination before surgery (Staging group);
4) patients who had MRI performed before and after nCRT (Restaging group); The exclusion criteria were:
1) patients who had undergone to prior rectal surgery;
2) patients whose interval between MRI examination and surgery was longer than 30 days. Patients’ characteristics are summarized in Table 1.
Tab. 1 Patient’s characteristics.
Mean Age 64 years ± 15 (SD)
Gender 20 women
36 men
nCRT No in 25 patients (Staging group) Yes in 31 patients (Restaging group)
Tumor location • Upper rectum (6 patients among Staging Group and 10 patients among Restaging
group)
• Middle rectum (6 patients among Staging Group and 6 patients among Restaging Group)
• Lower rectum (13 patients among Staging Group and 15 patients among Restaging Group)
Following surgery, operative specimens were analysed by a pathologist and the surgical resection specimen was used as standard of reference for determination of T and N stage, MRF status and EMVI.
MRI protocol
All MRI examinations were performed with a 3-Tesla-scanner (GE DISCOVERY MR750; GE Healthcare, Milwaukee, Wisconsin, USA) using an eight-channel phased-array body coil.
Before exam, rectal filling with ultrasound gel (60 to 120 ml relating to the location of the tumor) was performed and a spasmolytic agent (Buscopan®, Boehringer Ingelheim) was intramuscularly administered.
The imaging protocol employed T2-weighted sequences in axial, sagittal, coronal planes and in the “true axial” plane. The true axial plane is the one that is acquired at an angle perpendicular to the tumour longest axis. Axial diffusion-weighted MR images (DW-MRI) were acquired through the entire rectum using a single-shot spin-echo echo-planar sequence (SE-EPI) with multiple b-values, parallel imaging technique (acceleration phase, 2) and diffusion-weighted gradients applied in all the three orthogonal directions (Tab. 2).
SEQUENCE TR (ms) TE (ms) BW (hz/pixel) Slice Thick-ness/Spacing (mm) Acceleration (Phase/Slice) NEX b-value (sec/mm2) 2D Axial FRFSE T2w 500-8000 130 83,33/100 4/1 4 2D Sagittal FRFSE T2w 500-8000 130 83,33/100 4/1 4 2D Coronal FRFSE T2w 500-8000 130 83,33/100 4/1 4 2D Oblique FRFSE T2w “true axial” 500-8000 130 83,33/100 4/1 4 2D Axial SE/EPI multi-b DWI T2w 4500-7000 Mini-mum 250 5/0 2/1 1 1 2 4 6 0 150 500 1000 1500
Table 2. MRI protocol for rectal examination. The table shows the imaging parameters of each
MRI images analysis
All MR examinations were interpreted blindly by two reader: an MR abdominal radiologist with 20 years of experience and a resident attending the last year of the residency program with 4 years of experience.
Two data-set of imaging for each patient were evaluated by the readers independently and
randomly: the dataset evaluated according to the 2012 ESGAR guidelines without DWI images and the dataset evaluated according to the 2016 ESGAR guidelines with DWI images.
In the Primary staging group the following features were evaluated: • T stage;
• N stage; • MRF status;
The T stage was described according to TNM system of the American Joint Committee on Cancer (7th edition, 2010). Since the differentiation between T1 and T2 tumours is not possible with MRI
imaging [3, 8, 10] the readers classified these two types of T stage as a single cathegory named “T1/T2”. (Tab. 3).
As regards N staging, it was expressed with N+ (almost one positive regional node, mesorectal or extra-mesorectal if included in the exam acquisition volume) or N0 (any positive node).
According to 2012 ESGAR guidelines positive lymph nodes (N+) were considered if they have irregular borders, round shape and mixed intensity signal,
According to 2016 ESGAR guidelines Positive lymph nodes (N+) were considered if • short axis diameter ≥ 9 mm;
• short axis diameter 5-8 mm and two morphologically suspicious characteristics; • short axis < 5mm and three morphologically suspicious characteristics.
The morphologically suspicious criteria are round shape, irregular borders and mixed intensity signal.
As regards MRF status, MRF is considered to be involved if the distance between MRF and tumour is ≤ 1mm according to 2012 ESGAR guidelines [8] while MRF is considered involved if the distance between tumor and MRF is ≤ 2mm according to 2016 ESGAR guidelines [3].
The EMVI was evaluated only during the examination of imaging data-set according to 2016 ESGAR guidelines since reporting of EMVI was not advised in 2012 [3].
T staging Data reported by the two readers
T0 No evidence of primary tumor T0
T1 Tumor invades submucosa T1/T2
T2 Tumor invades muscularis propria T1/T2
T3 Tumor invades through the muscolaris propria
into pericolorectal tissues
• T3a/b if ≤ 5mm extramural growth • T3 c/d if > 5mm extramural growth
T3
T4 Tumor directly invades or is adherent to other organ or structures
T4
Table 3. T staging according to AJCC, 7th edition 2010.
In the Restaging Group after nCRT, the following features were evaluated: • T stage;
• N stage; • MRF status;
• EMVI (ESGAR 2016).
First of all the readers expressed about the presence of residual tumor: in the presence of residual tumor mass they assigned a yT stage according to TNM system of the American Joint Committee on Cancer (7th edition, 2010); in the case of a completely normalised rectal wall (complete response) or fibrotic wall thickening without clear residual tumor (complete or near complete response) they assigned a yT0 [3,8].
As regards N staging, it was expressed with yN+ (almost one positive regional node, mesorectal or extra-mesorectal if included in the exam acquisition volume) or yN0 (any positive node).
According to 2012 ESGAR guidelines negative lymph nodes (N0) were considered in the case of nodal size reduction and homogeneity of nodal signal intensity [3].
According to 2016 ESGAR guidelines negative lymph nodes (N0) were considered in the case of • No remaining nodes or
• Only nodes < 5mm.
Positive lymph nodes (N+) were considered in the presence of any nodes with a short axis diameter ≥ 5mm [8].
As regards MRF status, MRF is considered to be involved if the distance between MRF and tumour is ≤ 1mm according to 2012 ESGAR guidelines [8] while MRF is considered involved if the distance
between tumor and MRF is ≤ 2mm according to 2016 ESGAR guidelines [3].
The EMVI was evaluated only during the examination of imaging data-set according to 2016 ESGAR guidelines due to the emerging evidence of EMVI as an important prognostic factor [6, 8, 10, 11]. According to 2016 ESGAR guidelines, structured reporting is strongly recommended and the consensus meeting proposed two templates, both for primary staging and for restaging after nCRT (Fig.1 and Fig.2).
In our study the readers used these templates for the evaluation of T and N stage, MRF status and EMVI according to 2016 ESGAR guidelines. As regards 2012 ESGAR guidelines the readers referred to the key recommendations for MRI reporting both for primary staging and restaging after CRT [3].
Statistical analysis
All statistical computations were performed with dedicated software package (IBM SPSS v.26). Continous variables were reported as mean ± standard deviation (SD).
The agreement between MRI parameters and hystopathological findings was assessed by using the Cohen’s kappa statistics.
Results
Agreement between MRI staging and hystopathological findings
As regards the Primary Staging group we found moderate agreement between MRI-T Stage
(Figg.3) and the standard of reference for the expert reader according to 2012 and good
agreement according to 2016 ESGAR guidelines; there is a moderate agreement for the resident according to both 2012 and 2016 ESGAR (Tab. 4).
As regards N Stage we found moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016; there is a poor agreement for the resident according to 2012 ESGAR guidelines and a fair agreement according to 2016 ESGAR guidelines (Tab. 5).
As regards MRF status we found very good agreement between MRI staging and the standard of reference for the two readers according to both guidelines (Tab. 6).
Finally, as regards EMVI (Figg. 4) the agreement is moderate for the expert reader and fair for the resident (Tab.7).
Table 4. Agreement between MRI-T stage and standard of reference.
N STAGE Cohen’s K value
Expert ESGAR 2012 0.444 (moderate)
Resident ESGAR 2012 0.194 (poor)
Expert ESGAR 2016 0.601(moderate)
Resident ESGAR 2016 0.204(fair)
Table 5. Agreement between MRI-N stage and standard of reference.
T STAGE Cohen’s K value
Expert ESGAR 2012 0.516 (moderate)
Resident ESGAR 2012 0.415 (moderate)
Expert ESGAR 2016 0.644 (good)
Resident ESGAR 2016 0.569 (moderate)
Table 6. Agreement between MRI-MRF status and standard of reference.
EMVI Cohen’s K value
Expert ESGAR 2016 0.444 (moderate)
Resident ESGAR 2016 0.371 (fair)
Table 7. Agreement between MRI-EMVI and standard of reference.
Figure 3. T1/T2 tumor 3a, axial FRFSE T2w MRI; 3b, “true” axial FRFSE T2w MRI; 3c, DWI with
b-value of 500 sec/mm2; 3d, DWI with b-value of 1000 sec/mm2; 3e, DWI with b-value of 1500
sec/mm2.
MRF STATUS Cohen’s K value
Expert ESGAR 2012 0.884(very good)
Resident ESGAR 2012 0.884(very good)
Expert ESGAR 2016 0.884(very good)
Resident ESGAR 2016 0.896(very good)
3a 3b
Figure 4. T4 tumor. 4a, axial FRFSE T2w with MRF involvement and metastatic node (white arrow);
4b, axial FRFSE T2w shows involvement of sigmoid colon by the tumor.
Figure 5. 5a, T3 tumor with EMVI (white arrows); 5b, axial FRFSE T2w MRI; 5b, DWI with
b-value of 1000 sec/mm2. 4b 5a 5b 5a 5b 4a 4b 5a 5b 5a
Agreement between MRI restaging after neoadjuvant therapy and hystopathological findings
As regards the Restaging group we found moderate agreement between MRI-T Stage (Figg. 6) and the standard of reference for the expert reader according to both 2012 and 2016 ESGAR
guidelines; there is a fair agreement for the resident according to 2012 ESGAR guidelines and a moderate agreement according to 2016 ESGAR guidelines (Tab. 8).
As regards N Stage there is a moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016; there is a fair agreement for the resident according to 2012 ESGAR guidelines and a moderate agreement according to 2016 ESGAR guidelines (Tab. 9).
As regards MRF status there is a poor agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016 guidelines; there is a fair agreement for the resident according to both 2012 and 2016 guidelines (Tab. 10).
Finally, as regards EMVI the agreement is fair for the expert reader while there is no agreement for the resident (Tab. 11).
Table 8. Agreement between MRI-T stage and standard of reference.
N STAGE Cohen’s K value
Expert ESGAR 2012 0.565 (moderate)
Resident ESGAR 2012 0.326(fair)
Expert ESGAR 2016 0.475(moderate)
Resident ESGAR 2016 0.450 (moderate)
Table 9. Agreement between MRI-N stage and standard of reference.
MRF STATUS Cohen’s K value
Expert ESGAR 2012 0.147 (poor)
Resident ESGAR 2012 0.262 (fair)
T STAGE Cohen’s K value
Expert ESGAR 2012 0.521(moderate)
Resident ESGAR 2012 0.214((fair)
Expert ESGAR 2016 0.574(moderate)
Expert ESGAR 2016 0.197 (poor)
Resident ESGAR 2016 0.262 (fair)
Table 10. Agreement between MRI-MRF status and standard of reference.
EMVI Cohen’s K value
Expert ESGAR 2016 0.527 (moderate)
Resident ESGARD 2016 <0.1 (poor)
Table 11. Agreement between MRI-EMVI and standard of reference.
Figure 6. 6a, axial FRFSE T2w shows T3N+ tumor before nCRT; mesorectal lymphnode shows
irregularity of borders and disomogeneous signal intensity; 6b, axial FRFSE T2w after nCRT showing size-reduction of metastatic mesorectal lymph-node and of tumoral rectal tissue.
6b 6a
Figure 7. 7a, axial FRFSE T2w shows T3N+ tumor before nCRT; 7b, DWI with b-value of 1000
sec/mm2 shows hyperintensity of mesorectal lymphnode and of tumoral tissue; 7c, axial FRFSE
T2w shows reduction of lymph-node size and of tumoral tissue; 7d, DWI with b-value of 1000 sec/mm2 shows no hyperintesity of mesorectal node and tumoral tissue due to reduction of
tumoral cells.
7a 7b
Discussion
Determination of an optimal treatment plan for patients with rectal cancer is a complex process; clinical staging is at the basis of the decision-making process regarding choice of primary treatment and whether to recommend preoperative nCRT, so either understaging or overstaging rectal cancer can be substantial (Fig. 3, Fig.4 and Fig.5) [1]. According NCCN Clinical Guidelines for rectal cancer of 2018 [1] rectal cancer staging is based on total colonscopy, carcinoembryonic antigen determination, histopathologic examination of the specimen obtained via biopsy or local excision and preoperative imaging. Preoperative imaging, based on CT, endoscopic US and MRI, plays a critical role both for local staging of primary tumor and for the assessment of distant metastases. MRI has a pivotal role in local staging allowing an accurate prediction of T and N stage and of MRF status [2].
Figure 5. Therapeutic flow-chart for rectal cancer patients with a clinical stage T3, N any and clear
MRF.
Figure 6. Therapeutic flow-chart for rectal cancer patients with a clinical stage T3, N any and
Due to MRI crucial role in the diagnostic-therapeutic decision-making process for patients with rectal cancer, in 2012 ESGAR provided international guidelines in order to definy the state-of-the-art of MRI regarding MR image acquisition protocol and MR image evaluation and reporting [3,8].
In 2016 an ESGAR consensus meeting provided an update to these guidelines with the main addictions regarding:
• recommendations to report T3 substages;
• recommendations to perform structured reporting; • introduction of specified criteria for nodal staging; • specified indications for DWI [8].
In the primary staging group as regards T stage our study showed a moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016 ESGAR guidelines and a moderate to good agreement (with Cohen’s K value varying from 0,561 to 0,644) for the resident according to 2012 and 2016 ESGAR guidelines, respectively. The main discrepancies were founded in the differentiation between T1/T2 from T3 tumors, often caused by the presence of desmoplastic reaction within the peritumoral tissues [12]. In our database we didn’t take into account the subclassification of T3 tumours as it is suggested by 2016 ESGAR guidelines because these substages were not described in the hysto-pathologic report.
As regards N stage our study showed that it is improved by using ESGAR 2016 criteria; in particular, we can see a better agreement between MRI staging and the standard of reference for both readers, especially for the resident (with Cohen’s K value varying from 0,194 to 0, 204 ranging from poor to fair agreement). We can explain these discrepancies as due to the introduction of more stringent criteria for nodal staging, based both on size and morphology, improving the accuracy of MRI staging especially in the case of a non expert reader, avoiding overcalling nodes as malignant.
Improvement in T and N staging according to 2016 ESGAR guidelines could be justified by the introduction of DWI since it can improve the identification of tumoral tissue and pathological lymph-nodes.
As regards MRF status we found a very good agreement between MRI staging and the standard of reference for the two readers according to both guidelines, confirming that MRI is the best tool to assess MRF status.
Finally, as regards EMVI we found moderate agreement for the expert reader and fair for the resident.
In the restaging group as regards yT stage we found moderate agreement between MRI staging and the standard of reference for the expert reader according to both 2012 and 2016 ESGAR guidelines and a fair to moderate agreement (with Cohen’s K value varying from 0,214 to 0,479) for the resident according to 2012 and 2016 ESGAR guidelines, respectively: we can explain these improvement in the performance of the resident stressing the role of DWI in the setting of restaging [8].
As regards yN-staging we found a worse agreement between MRI and the standard of reference for the expert reader (with Cohen’s K value varying from 0,565 to 0,475 with moderate agreement) according to 2016 ESGAR guidelines while there was a better agreement for the resident (with Cohen’s K value varying from 0,326 to 0,450 with fair to moderate) according to 2016 ESGAR guidelines. We can explain these results stressing the fact that the introduction of a dimensional cut-off for the identification of metastatic nodes after nCRT could be useful for a non-expert reader while it could be a limiting factor in the diagnostic perfomance of an expert reader.
As regards yMRF status we found poor agreement between MRI staging and the standard of reference for the expert reader and fair agreement for the resident according to both 2012 and 2016 guidelines. Even in this case we can attribute this improvement in the diagnostic
performance of both readers to the introduction of DW images in the data-set evaluated according to 2016 recommendations, stressing the importance of this sequence especially in the setting of restaging after neoadjuvant therapy.
Finally, as regards EMVI the agreement is fair for the expert reader while there is no agreement for the resident.
Conclusion
Our data confirm that MRI has a crucial role in the staging and restaging of rectal cancer.
Both 2012 and 2016 ESGAR structured MRI report templates are reliable tools to assess the radiological T and N stage of rectal cancer, especially for non-expert readers.
The 2016 report template is more accurate in estimating T and N stage in the primary staging group, whereas no significant improvement was observed in the Restaging group of patients.
Improvement in T and N staging according to 2016 ESGAR guidelines could be justified by the introduction of DWI.
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