An optimal imaging modality based on different predictive risk factors for evaluating local staging of rectal cancer preoperatively: a comparative study of MRI and endorectal ultrasound

Introduction

Colorectal cancer is the second most common cancer worldwide, with an estimated 190 million new cases per year, ultimately responsible for 9% of all cancer deaths in 2020. Approximately one-third of these tumors are rectal cancers (1). Precise preoperative staging is needed to develop a therapeutic plan before treatment, especially for those with locally advanced rectal cancer (mainly stage T4), as long-term neoadjuvant chemoradiotherapy (NCRT) is required, aimed at downsizing, downstaging, and thereby enhancing its resectability (2). Moreover, according to the recent guidelines of the National Comprehensive Cancer Network (NCCN), mesorectal fascia (MRF)-affected patients should also receive NCRT before surgery, because the involvement of MRF is an independent risk factor for local recurrence, distant metastases, and poorer survival (3-6). It is imperative to conduct a precise preoperative evaluation of T-staging and MRF status, particularly targeting patients susceptible to local recurrence and projected to gain advantages from NCRT.

At present, preoperative local staging for rectal cancer is usually evaluated by imaging modalities, most commonly including magnetic resonance imaging (MRI), endorectal ultrasound (ERUS), computed tomography (CT), etc. Some previous studies have noted that each modality is advantageous in different areas: MRI may be useful in identifying infiltration of the MRF, ERUS is considered more accurate for assessing tumor growth in the mucosa and confined to the rectal wall, and CT may be used to assess both local tumor extent and regional or distant metastases (7,8). In recent years, with the popularization of three-dimensional endorectal ultrasound (3D-ERUS), some researchers have proposed that 3D-ERUS and MRI may have comparable accuracy in assessing MRF status (7,9,10). Therefore, which imaging method is preferred for local staging evaluation remains controversial. Additionally, several studies reported that precise local staging can be interfered with by tumor location (on longitudinal and transverse sections), patients’ body mass index (BMI), and whether or not the patients have received NCRT (11-14). There is still no consensus on how these factors affect the accuracy of preoperative staging and how to perform individualized imaging evaluations.

Thus, we designed this study to compare the ability of MRI and ERUS for local staging of rectal cancer, and to determine how to choose an optimal imaging modality to stage rectal cancer based on different predictive risk factors. We present this article in accordance with the STARD reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2120/rc).

Methods

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the institutional ethics committee of the West China Hospital of Sichuan University, and informed consent was provided by all participants.

Study population

Inclusion criteria were considered as follows: (I) a patient who was diagnosed with rectal cancer pathologically; (II) a patient who had complete ERUS or MRI data, as well as pathological data. Exclusion criteria were: (I) patients who did not undergo surgery for rectal cancer or the information on surgical pathological staging was unavailable; (II) the time interval between completion of ERUS or MRI evaluation and surgery was more than 2 weeks; (III) the time interval between the completion of ERUS and MRI was more than 2 weeks for the same patient. From January 2018 to December 2021, a total of 277 patients in our institution were included based on our inclusion and exclusion criteria. All patients underwent 2D-ERUS, and 243 and 54 patients received MRI and 3D-ERUS, respectively.

Radiologic evaluation

ERUS was performed by MyLab Twice (Esaote, Genova, Italy) equipped with a biplane endoscopic probe (TRT33, linear frequency of 4–13 MHz, convex frequency of 3–9 MHz) and B-K Medical Systems (B-K Medical, Herlev, Denmark) with both 2D and 3D diagnostic ultrasound systems, using a rotating endoprobe (type 9038, 2D frequency of 6–12 MHz, 3D frequency of 10 MHz) with a 360° view. The MRI examination was performed on a 3.0 T scanner (Magnetom Skyra, Siemens Healthineers, Erlangen, Germany) with an 18-channel torso phased-array coil.

ERUS was operated by two sonographers with at least 5 years of experience, and they were randomly assigned per the hospital’s daily schedule. 3D-ERUS data were recorded and read by another sonographer at a post-processing stage. The MRI data were evaluated by two experienced radiologists independently, both of whom were blinded to the patient’s medical history, and a consensus was reached by discussion between the radiologists.

Staging and grouping criteria

The T-staging was evaluated according to the eighth edition of the TNM classification system (15). According to the guidelines of European Society for Medical Oncology (ESMO) published in 2017 (16), MRF invasion on MRI and 3D-ERUS was compared with pathology measurements using a 1-mm criterion (Figure 1).

Figure 1 The ultrasonic and MRI images of a rectum adenocarcinoma. A 40-year-old female patient. Before surgery, the patient was evaluated with 2D-ERUS (A), 3D-ERUS (B), and MRI (C,D). All three imaging modalities showed that the lesion infiltrated the whole rectal wall (T4). No abnormal perirectal lymph nodes were detected on 2D and 3D-ERUS, and they were detected on MRI [shown by the single arrow in (C)]. The distance between the location of the maximal infiltration depth and the MRF was measured as 2 mm on the 3D-ERUS [shown by the double arrow in (B)] and 4 mm on the MRI image [shown by the double arrow in (C)]. 2D-ERUS, two-dimensional endorectal ultrasound; 3D-ERUS, three-dimensional endorectal ultrasound; MRF, mesorectal fascia; MRI, magnetic resonance imaging.

Of the 277 tumors, according to the BMI, 148 were in high-index groups (BMI ≥23 kg/m²), 129 were in low index group (BMI <23 kg/m²); based on the location of the maximal depth of tumor infiltration (on the transverse section), we divided the patients into anterior group (lithotomy position, 10–14 o’clock) and non-anterior group (lithotomy position, the remaining parts). There were 68 tumors in the anterior group and 209 in the non-anterior group. Considering tumor distance from the anal verge (on the longitudinal section), 130 were in the low rectum (≤5 cm from the anal verge), and 147 were in the middle to high rectum (>5 cm from the anal verge).

Statistical analysis

Statistical package for social analysis (SPSS for Windows, IBM Corp, USA) version 27.0 was used for all statistical calculations. Categorical variables were presented as means of frequencies (percentages) and continuous variables as medians [range]. For statistical analysis, taking the postoperative pathological results as the reference standard, the Kappa consistency test was used to evaluate the consistency of imaging methods in evaluating preoperative T-stage and pathological findings (0–0.20 poor, 0.21–0.40 fair, 0.41–0.60 moderate, 0.61–0.80 good, and 0.81–1.00 excellent agreement). The sensitivity (SEN), specificity (SPE), positive predictive value (PPV), and negative predictive value (NPV) were used to evaluate the diagnostic performance of 3D-ERUS and MRI for MRF status. We used the Chi-squared test to compare the accuracy of ERUS and MRI in evaluating T-staging and MRF status. P values <0.05 were considered statistically significant for all tests.

Results

Within the 4-year study period, 277 patients with rectal cancer who had undergone rectal resection at our institution were included. The baseline information is summarized in Table 1.

Performance of MRI and analysis of risk factors associated with its inaccurate predictions

On the issue of T-staging evaluation, 203 cases were accurately staged by MRI, yielding an overall accuracy rate of 83.53% (203/243). The depth was understaged in 7 cases and overstaged in 33 cases by MRI (Table 2).

Regarding the evaluation of MRF status, 139 cases were accurately predicted by MRI, resulting in an overall accuracy rate of 84.24% (139/165). Twenty-three cases were overstaged, and 3 cases were understaged (Table 3).

Univariate analysis showed that the accuracy of MRI dropped significantly after NCRT, both in the evaluation of T-staging (78.05% vs. 91.14%) and MRF status (79.82% vs. 94.12%). Low BMI and location were the risk factors for accurate predictions of T-staging (75.93% vs. 89.63% for BMI; 78.15% vs. 88.71% for location) and MRF status (77.03% vs. 90.11% for BMI, 78.12% vs. 89.66% for location) (P<0.05). Compared with the non-anterior group, the predictive accuracy of MRI decreased in the anterior group, with no statistical significance (Tables 4,5).

Performance of ERUS and risk factors associated with its inaccurate predictions

Rectal wall invasion depth was accurately staged in 215 cases by 2D-ERUS and 45 cases by 3D-ERUS, resulting in overall accuracy rates of 77.62% (215 out of 277) and 83.33% (45 out of 54), respectively (Table 2).

In this study, we only discussed the performance of 3D-ERUS in diagnosing MRF status, because some patients who underwent 2D-ERUS did not undergo pre- and post-operative assessment of MRF status, whereas every patient who underwent 3D-ERUS received this assessment. 3D-ERUS correctly evaluated the MRF involvement in 45 cases, with an overall accuracy rate of 83.33% (45/54) (Table 3).

Univariate analysis showed that the accuracy of 3D-ERUS in T-staging and MRF status after NCRT was obviously lower than that of the non-treatment group. (65.38% vs. 100% for T-staging, 73.08% vs. 92.86% for MRF status). In addition, 3D-ERUS was not affected by the patient’s BMI and tumor location (P>0.05) (Tables 4,5).

Comparison of MRI and ERUS in predicting T-staging and MRF status

In the T-staging assessment, the accuracy of 3D-ERUS and MRI was higher than that of 2D-ERUS (83.33%, 83.53% vs. 77.62%, P=0.204).

In MRF status evaluation, MRI had a slightly higher diagnostic accuracy than 3D-ERUS (84.24% vs. 83.33%, P=0.874).

In the subgroups, we found no significant differences between MRI and 3D-ERUS in T-staging and MRF status (P>0.05, Tables 4,5).

Discussion

This retrospective study not only compared the performance of MRI with ERUS, including preoperative T-staging and MRF status, but also explored the risk factors associated with accurate predictions. The aim is to help in selecting an optimal imaging modality for each patient.

From previous literature, a wide range of papers have confirmed that ERUS and MRI are highly accurate in evaluating local staging for rectal cancer without NCRT, and both are superior to CT (7,17-19). In contrast, in patients with locally advanced rectal cancer, conditions such as edema, inflammation, or fibrosis due to neoadjuvant therapy may cause a further decrease in the staging accuracy of ERUS and MRI (20). Most of the research also suggested that ERUS had an advantage in early tumor staging (T1–T2), while MRI is more accurate in assessing the relationship of more advanced tumors to important anatomic structures, such as the MRF status (7,12,13,21-23). A meta-analysis that included 90 articles showed that ERUS provided more accurate data than CT or MRI in the evaluation of T-staging (7). However, in a one-year large prospective multicenter study in Germany, a total of 75 hospitals were included, and 422 patients underwent 2D-ERUS before surgery. The results showed that the overall accuracy in assessing T-staging was approximately 63.3%. In this study, the diagnostic accuracy of ERUS was lower than that previously reported literature. The researchers believe that the main reason may be due to the fact that 2D-ERUS is highly dependent on the examiner, and accurate results can only be obtained when performed by an experienced sonographer (24). The recently updated 3D-ERUS system, which enables volumetric evaluation with better anatomic planes for adjacent structures, further enhanced the capabilities of conventional ERUS evaluation, resulting in a reported overall T-staging accuracy of 92.9–94.44% (25,26). Therefore, these authors considered that 3D-ERUS may become a powerful alternative for preoperative T-staging in the future.

Using the pathological findings as the reference standard, our results showed that the accuracy of T-staging by 3D-ERUS and MRI was higher than that of 2D-ERUS (83.33%, 83.53% vs. 77.62%). For patients without NCRT, the accuracy of MRI and 3D-ERUS reached 91.94% and 100%, which was consistent with previous findings (7,25,26). We also found that 3D-ERUS improves the accuracy of 2D-ERUS from 77.62% to 83.33%. The reason may be due to the difficulty of 2D-ERUS in fully visualizing the lesion and its surrounding structures. 3D-ERUS can capture images of all sections and angles of the lesion, which can provide the spatial three-dimensional relationship between the tumor and the surrounding structures. On the other hand, for the operator, 3D-ERUS only needs to fix the probe in the center of the rectal cavity, and then the probe can automatically scan at a constant speed, which reduces the possible distortion of images and thus improves the results without operator dependence (25,26).

In terms of MRF status assessment, 3D-ERUS and MRI presented comparable accuracy (83.33% vs. 84.24%, P=0.874). 3D-ERUS showed sensitivity and specificity of 80.00% and 83.67%, compared with 85.00% and 84.14% for MRI. The overall diagnostic performance of MRI was better than that of 3D-ERUS (Table 3). Granero-Castro et al. (27) enrolled 76 patients with middle to low rectal cancer, showing that the overall accuracy of ERUS and MRI in assessing the MRF status was 83.7% and 91.8%. Liu et al. (28) reviewed preoperative 3D-ERUS of 80 patients with stage T3 rectal cancer, using MRI as the reference standard; 3D-ERUS and MRI showed excellent agreement (kappa value =0.82). 3D-ERUS showed sensitivity and specificity of 95.3% and 86.5%. Our results were basically similar to previous studies.

However, precise local staging by ERUS and MRI can be influenced by several factors. First, the evaluation after NCRT, particularly for rectal cancer with pathological complete responses (pCR), remains a major point of concern. Both in T-staging and MRF status evaluation, our results showed that the accuracy of ERUS and MRI decreased significantly after NCRT. Meanwhile, in patients with pCR, the number of correct T-staging was only 3/21 and 0/4, by MRI and 3D-ERUS. It is probably because they were affected by the inflammation of residual tumor tissue, which resembled previous studies (29-32).

Then, many scholars showed that low and anterior rectal tumors were the main risk factors for MRI (12). Considering the location of tumors (on the longitudinal section), the study of Ren et al. (14) showed that ERUS had the highest accuracy in the diagnosis of tumors located 3–6 cm above the anal verge, and high levels of tumor location was a risk factor for T-staging by ERUS, which was mainly due to the limited distance that the probe can reach; the study of Shihab et al. (11) proposed that the accuracy of MRI in predicting MRF status after NCRT was still high, but the closer to the anal verge, the less accurate the results became; the research of Granero-Castro (27) showed that the accuracy of assessing MRF involvement by ERUS and MRI was 83.7% and 91.8%, and when focusing only on low rectal tumors, the overall accuracy of 3D-ERUS increased to 87.5%, while the accuracy of MRI decreased to 87.5%. Our results showed similar results; MRI is more accurate in diagnosing rectal cancer located in the middle to high rectum, whereas 3D-ERUS shows the opposite trend.

Peschaud et al. (12) suggested that anterior rectal tumors may lead to a reduction in the accuracy of MRI in assessing the MRF involvement, which was also reflected in our findings. We observed that low BMI is also a risk factor for T-staging and MRF status evaluation. The reduction in fat thickness in the low and anterior rectum is accountable for the aforementioned outcomes, potentially leading to a rise in erroneous positives. Furthermore, the anterior aspect of the lower rectum maintains close associations with the bladder, prostate, and seminal vesicles in male subjects, while in female subjects, it is linked with the vaginal wall. Within the anterior section of the rectum, the mesorectal tissue (thin perirectal fat located anteriorly) is relatively sparse, and the MRF is thin. Moreover, the MRF in the anterior position lacks clear identification due to its thin and translucent nature, thereby complicating preoperative staging processes (12,13).

There are some limitations in this study. First, we collected a relatively limited sample size of 3D-ERUS, and the ERUS data and MRI data could not correspond exactly, which led us not to evaluate MRI and ERUS on the same patient. Then, tumors of our patients were mostly concentrated in relatively lower (≤7 cm from the anal verge) and advanced-stage (T3–T4), which may introduce bias. Finally, in addition to 3D-ERUS, two new ultrasound techniques, ultrasound elastography and contrast-enhanced ultrasound, were not studied in this study. Therefore, we will further include a larger sample size in future studies to evaluate MRI and ERUS on the same patient and investigate in depth the ability of ultrasound elastography and contrast-enhanced ultrasound to assess the staging of rectal cancer.

Conclusions

Preoperative local staging of rectal cancer can be accurately assessed by ERUS and MRI, and MRI has a higher accuracy. However, the accuracy of MRI is usually influenced by the fat content surrounding the lesion, specifically indicating that MRI is more accurate in patients with high BMI, tumors located in non-anterior and middle to high rectum. The accuracy of 3D-ERUS is not affected by these factors. Therefore, MRI remains the preferred imaging modality for staging assessment in most patients with rectal cancer. However, in specific populations [such as those with low BMI (BMI <23 kg/m²) or tumors located in the lower rectum (≤5 cm from the anal margin)], 3D-ERUS may demonstrate unique clinical utility as an important adjunct to MRI staging.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2120/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2120/dss

Funding: This study was supported by the Science and Technology Planning Project of Sichuan Province in China (No. 2021YJ0243).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2120/coif). All authors report that this work was supported by the Science and Technology Planning Project of Sichuan Province in China (No. 2021YJ0243). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the institutional ethics committee of the West China Hospital of Sichuan University, and informed consent was provided by all participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2021;71:209-49. [Crossref] [PubMed]
2. Opara CO, Khan FY, Kabiraj DG, Kauser H, Palakeel JJ, Ali M, Chaduvula P, Chhabra S, Lamsal Lamichhane S, Ramesh V, Mohammed L. The Value of Magnetic Resonance Imaging and Endorectal Ultrasound for the Accurate Preoperative T-staging of Rectal Cancer. Cureus 2022;14:e30499. [Crossref] [PubMed]
3. Monson JR, Weiser MR, Buie WD, Chang GJ, Rafferty JF, Buie WD, Rafferty J. Practice parameters for the management of rectal cancer (revised). Dis Colon Rectum 2013;56:535-50. [Crossref] [PubMed]
4. Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. Rectal Cancer, Version 2.2018, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 2018;16:874-901. [Crossref] [PubMed]
5. Moore HG. Importance of the Circumferential Resection Margin. J Am Coll Surg 2020;230:1018-9. [Crossref] [PubMed]
6. Liu Q, Luo D, Cai S, Li Q, Li X. Circumferential resection margin as a prognostic factor after rectal cancer surgery: A large population-based retrospective study. Cancer Med 2018;7:3673-81. [Crossref] [PubMed]
7. Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker J. Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging--a meta-analysis. Radiology 2004;232:773-83. [Crossref] [PubMed]
8. Nougaret S, Gormly K, Lambregts DMJ, Reinhold C, Goh V, Korngold E, Denost Q, Brown G. MRI of the Rectum: A Decade into DISTANCE, Moving to DISTANCED. Radiology 2025;314:e232838. [Crossref] [PubMed]
9. Phang PT, Gollub MJ, Loh BD, Nash GM, Temple LK, Paty PB, Guillem JG, Weiser MR. Accuracy of endorectal ultrasound for measurement of the closest predicted radial mesorectal margin for rectal cancer. Dis Colon Rectum 2012;55:59-64. [Crossref] [PubMed]
10. Ye D, Zhu Z, Chen F, Lie C, Li W, Lin Y, Qiu S. Correlation Between Endorectal Ultrasound and Magnetic Resonance Imaging for Predicting the Circumferential Resection Margin in Patients With Mid-Low Rectal Cancer Without Preoperative Chemoradiotherapy. J Ultrasound Med 2020;39:569-77. [Crossref] [PubMed]
11. Shihab OC, Moran BJ, Heald RJ, Quirke P, Brown G. MRI staging of low rectal cancer. Eur Radiol 2009;19:643-50. [Crossref] [PubMed]
12. Peschaud F, Cuenod CA, Benoist S, Julié C, Beauchet A, Siauve N, Taieb-Kasbi F, Penna C, Nordlinger B. Accuracy of magnetic resonance imaging in rectal cancer depends on location of the tumor. Dis Colon Rectum 2005;48:1603-9. [Crossref] [PubMed]
13. Kim YW, Cha SW, Pyo J, Kim NK, Min BS, Kim MJ, Kim H. Factors related to preoperative assessment of the circumferential resection margin and the extent of mesorectal invasion by magnetic resonance imaging in rectal cancer: a prospective comparison study. World J Surg 2009;33:1952-60. [Crossref] [PubMed]
14. Ren Y, Ye J, Wang Y, Xiong W, Xu J, He Y, Cai S, Tan M, Yuan Y. The Optimal Application of Transrectal Ultrasound in Staging of Rectal Cancer Following Neoadjuvant Therapy: A Pragmatic Study for Accuracy Investigation. J Cancer 2018;9:784-91. [Crossref] [PubMed]
15. Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, Meyer L, Gress DM, Byrd DR, Winchester DP. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more "personalized" approach to cancer staging. CA Cancer J Clin 2017;67:93-9.
16. Glynne-Jones R, Wyrwicz L, Tiret E, Brown G, Rödel C, Cervantes A, Arnold D. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2017;28:iv22-40. [Crossref] [PubMed]
17. Brown G, Davies S, Williams GT, Bourne MW, Newcombe RG, Radcliffe AG, Blethyn J, Dallimore NS, Rees BI, Phillips CJ, Maughan TS. Effectiveness of preoperative staging in rectal cancer: digital rectal examination, endoluminal ultrasound or magnetic resonance imaging? Br J Cancer 2004;91:23-9. [Crossref] [PubMed]
18. García Botello S, Martí Fernández R, Cozar Lozano C, Campos Salher S, Martín Arévalo J, Moro Valdezate D, Pla Martí V, Espí Macías A. Concordance and survival implications of preoperative subclassification of T3 rectal cancers by depth of mesorectal invasion using a 5-mm cut-off point with endorectal ultrasound and magnetic resonance imaging. Quant Imaging Med Surg 2022;12:2356-67. [Crossref] [PubMed]
19. Zhong G, Xiao Y, Zhou W, Pan W, Zhu Q, Zhang J, Jiang Y. Value of endorectal ultrasonography in measuring the extent of mesorectal invasion and substaging of T3 stage rectal cancer. Oncol Lett 2017;14:5657-63. [Crossref] [PubMed]
20. Mezzi G, Arcidiacono PG, Carrara S, Perri F, Petrone MC, De Cobelli F, Gusmini S, Staudacher C, Del Maschio A, Testoni PA. Endoscopic ultrasound and magnetic resonance imaging for re-staging rectal cancer after radiotherapy. World J Gastroenterol 2009;15:5563-7. [Crossref] [PubMed]
21. Cârțână ET, Gheonea DI, Săftoiu A. Advances in endoscopic ultrasound imaging of colorectal diseases. World J Gastroenterol 2016;22:1756-66. [Crossref] [PubMed]
22. Schaffzin DM, Wong WD. Endorectal ultrasound in the preoperative evaluation of rectal cancer. Clin Colorectal Cancer 2004;4:124-32. [Crossref] [PubMed]
23. Wang D, Xu J, Zhang Z, Li S, Zhang X, Zhou Y, Zhang X, Lu Y. Evaluation of Rectal Cancer Circumferential Resection Margin Using Faster Region-Based Convolutional Neural Network in High-Resolution Magnetic Resonance Images. Dis Colon Rectum 2020;63:143-51. [Crossref] [PubMed]
24. Marusch F, Koch A, Schmidt U, Zippel R, Kuhn R, Wolff S, Pross M, Wierth A, Gastinger I, Lippert H. Routine use of transrectal ultrasound in rectal carcinoma: results of a prospective multicenter study. Endoscopy 2002;34:385-90. [Crossref] [PubMed]
25. Kolev NY, Tonev AY, Ignatov VL, Zlatarov AK, Bojkov VM, Kirilova TD, Encheva E, Ivanov K. The role of 3-D endorectal ultrasound in rectal cancer: our experience. Int Surg 2014;99:106-11. [Crossref] [PubMed]
26. Murad-Regadas S, Almeida R, Barreto R, Lima D, Regadas F. Three-Dimensional Ultrasound: Is it Useful for Decision Making in the Management of Rectal Cancer? Is 3D Ultrasound Useful in Rectal Tumor. Int J Cancer Clin Res 2016;3:068.
27. Granero-Castro P, Muñoz E, Frasson M, García-Granero A, Esclapez P, Campos S, Flor-Lorente B, Garcia-Granero E. Evaluation of mesorectal fascia in mid and low anterior rectal cancer using endorectal ultrasound is feasible and reliable: a comparison with MRI findings. Dis Colon Rectum 2014;57:709-14. [Crossref] [PubMed]
28. Liu M, Yin S, Li Q, Liu Y, Pei X, Han F, Li AH, Zhou J. Evaluation of the Extent of Mesorectal Invasion and Mesorectal Fascia Involvement in Patients with T3 Rectal Cancer With 2-D and 3-D Transrectal Ultrasound: A Pilot Comparison Study With Magnetic Resonance Imaging Findings. Ultrasound Med Biol 2020;46:3008-16. [Crossref] [PubMed]
29. Zhao RS, Wang H, Zhou ZY, Zhou Q, Mulholland MW. Restaging of locally advanced rectal cancer with magnetic resonance imaging and endoluminal ultrasound after preoperative chemoradiotherapy: a systemic review and meta-analysis. Dis Colon Rectum 2014;57:388-95. [Crossref] [PubMed]
30. Memon S, Lynch AC, Bressel M, Wise AG, Heriot AG. Systematic review and meta-analysis of the accuracy of MRI and endorectal ultrasound in the restaging and response assessment of rectal cancer following neoadjuvant therapy. Colorectal Dis 2015;17:748-61. [Crossref] [PubMed]
31. van den Broek JJ, van der Wolf FS, Lahaye MJ, Heijnen LA, Meischl C, Heitbrink MA, Schreurs WH. Accuracy of MRI in Restaging Locally Advanced Rectal Cancer After Preoperative Chemoradiation. Dis Colon Rectum 2017;60:274-83. [Crossref] [PubMed]
32. Kye BH, Kim HJ, Kim G, Kim JG, Cho HM. Multimodal Assessments Are Needed for Restaging after Neoadjunvant Chemoradiation Therapy in Rectal Cancer Patients. Cancer Res Treat 2016;48:561-6. [Crossref] [PubMed]