Research ArticleClinical Studies

Predicting Difficult Laparoscopic Total Mesorectal Excision for Locally-advanced Mid-low Rectal Cancer: The EuMaRCS Score Validation

NICOLA de'ANGELIS, ALEIX MARTÍNEZ-PÉREZ, GIULIO CESARE VITALI, FREDERIC PIGNEUR, ALAIN LUCIANI, FRANCESCO BRUNETTI, MIQUEL KRAFT, EVA MARTÍ-MARTÍNEZ, PAOLO MORONI, ELOY ESPIN, FREDERIC RIS, SALVATORE PUCCIARELLI and On behalf of the EuMaRCS Study Group
Anticancer Research April 2020, 40 (4) 2079-2087; DOI: https://doi.org/10.21873/anticanres.14166

Abstract

Background/Aim: The European MRI and Rectal Cancer Surgery (EuMaRCS) score was proposed to identify preoperatively difficult laparoscopic total mesorectal excision (L-TME) for locally advanced rectal cancer (LARC). This study aimed to test EuMaRCS's validity. Patients and Methods: Data were retrieved from a European multicenter database, including patients with mid/low LARC, treated with neoadjuvant chemoradiation therapy and L-TME with primary anastomosis. The EuMaRCS score was calculated on: BMI>30 (3 points), interspinous distance<96.4 mm (2 points), ymrT stage≥T3b (4 points), and male sex (1 point). Results: The sample was composed of 141 patients, of whom 23 (16.3%) had a difficult L-TME. The EuMaRCS score demonstrated high accuracy in predicting difficult surgery (AROC: 0.806, 95%CI=0.72-0.88), with a cut-off >3 being associated with the best balance in sensitivity (82.6%) and specificity (66.1%). Conclusion: The EuMaRCS score represents a validated tool to predict preoperatively difficult L-TME in LARC patients.

A multimodal approach is recommended for the treatment of locally advanced rectal cancer (LARC) of the middle or low rectum (1). This approach includes neoadjuvant chemoradiation therapy (NCRT) and radical surgery, which represents the curative treatment that impacts patient prognosis the most (2-4). The gold standard procedure is a total mesorectal excision (TME) with clear resection margins (5), which is currently performed more frequently via a minimally invasive approach such as laparoscopy (L-TME) (2, 6-9). Several patient- and tumor-related factors can influence surgical difficulty and make surgical outcomes worse. Among these, anatomical constraints (e.g., narrow pelvis), obesity, tumor volume and height have been shown to be associated with more difficult L-TME procedures, namely, longer operative times, blood loss, intraoperative complications, and conversion to open surgery (4, 10-15). Incomplete mesorectal excision or positive resection margins should be considered to indicate unsuccessful surgical treatment because they are associated with a significantly increased risk of both local and systemic recurrence (3, 11, 16-19). Thus, predicting surgical difficulties and adapting the surgical strategy (technique and approach) to the patient and tumor characteristics could impact the probability of achieving optimal surgical outcomes, consequently improving rectal cancer patient survival.

Recently, a morphometric score to predict surgical difficulty in LARC patients who are candidates for L-TME has been proposed (20). This score was developed based on a multicentric European database, namely, the European MRI and Rectal Cancer Surgery (EuMaRCS) database, composed of data from consecutive patients with LARC located at the middle or low rectum who were treated with NCRT and L-TME in four referral hospitals in Spain, France and Switzerland (20). The proposed EuMaRCS score is easy to assess by taking into account criteria related to the patient (i.e., male sex, obesity, and the pelvimetric measure of the interspinous distance) and the tumor (i.e., ymrT stage), which can all be assessed preoperatively. In the training population set on which the EuMaRCS score was developed, the score showed good accuracy with an area under the receiving operating characteristics (ROC) curve of 0.802 (20).

The aim of the present study was to test the external validity of the EuMaRCS score in an independent multicentric population and to evaluate the accuracy and usefulness of this score to predict L-TME surgical difficulty in LARC patients.

Patients and Methods

Study design and study population. To validate the EuMaRCS score (20) in an independent population (validation set), we build a new European multicentric database of consecutive patients with locally advanced mid- or low-rectal cancer treated between February 2016 and June 2019 in 5 colorectal referral centers: Henri Mondor University Hospital of Créteil, France; Doctor Peset University Hospital of Valencia, Spain; Geneva University Hospital of Geneva, Switzerland; University Hospital of Padova, Italy; and Vall d'Hebron University Hospital of Barcelona, Spain. All included patients signed an informed consent form allowing their data to be used for retrospective analyses and research. Thus, the study was conducted exclusively with anonymous patient records that were treated in conformity to the principles declared by the National Commission for Data Protection and Liberties and in accordance with the ethical principles described in the Declaration of Helsinki. The inclusion criteria were the same as those of the EuMaRCS original population (11, 20, 21) and consisted of patients diagnosed with histologically proven, locally advanced [American Joint Committee on Cancer (AJCC) stages II to IIIc] (22) mid- or low-rectal cancer (within 12 cm from the anal verge), who received NCRT and were operated on by elective laparoscopic anterior resection (LAR) with total mesorectal excision (L-TME) (23, 24) and who had undergone an MRI before (pretreatment MRI) and after (restaging MRI) NCRT (11, 25). Records of patients who had received laparoscopic abdominoperineal resections (L-APR) and low Hartmann's procedures with TME, open surgery, transanal TME (Ta-TME), and robotic procedures were not considered.

Pretreatment MRI was used for primary tumor staging and pelvimetry (12, 26-31), as previously described (11). Restaging MRI, performed 8-10 weeks after the completion of NCRT, was used for tumor restaging and tumor response evaluation by applying the magnetic resonance tumor regression grade (mrTRG) (1 to 5) (32, 33), with an mrTRG of 4 or 5 identifying poor responders (34). All MRIs were performed following standard protocols (2-dimensional T2-weighted fast spin-echo sequences in 3 orthogonal directions and an additional diffusion-weighted sequence in the axial plane) (25).

View this table:
Table I.

The EuMaRCS predictive score for surgical difficulty.

Treatment protocols and definition of surgical difficulty. All patients completed long-course NCRT with a total radiation dose of 45-50.4 Gy delivered in daily fractions of 1.8-2 Gy over a 5- to 6-week period, combined with 5-fluorouracil or capecitabine (Xeloda) (2, 35).

All procedures were L-TMEs with low colorectal or coloanal anastomosis and were carried out according to the standard protocols by senior colorectal surgeons highly experienced in minimally invasive surgery (2, 11, 20). Conversion was defined as the premature interruption of the laparoscopic approach followed by the need for a conventional laparotomy to complete the procedure.

The predictable endpoint of surgical difficulty was defined using the grading system proposed by Escal et al. (12) and was previously applied for the development of the EuMaRCS score (20). Difficult surgeries were identified based on a composite variable including the following operative and postoperative parameters: operative time (>300 min), blood loss (>200 ml), conversion to laparotomy, use of transanal dissection, occurrence of postoperative Dindo-Clavien complications grades II and III (36), and duration of hospital stay (>15 days). The surgical difficulty grade ranges from 0 to 12; a score of 6 or more is considered to indicate high surgical difficulty (12).

Estimating the EuMaRCS score. The EuMaRCS score was originally proposed in two versions: the 3-criteria score and the 4-criteria score. However, the 4-criteria score showed a better accuracy than the 3-criteria one and it was then chosen to be externally validated (20). Thus, the EuMaRCS score was calculated based on the following 4 variables: BMI (≥30 kg/m2), interspinus distance (<96.4 mm), ymrT stage (≥T3b) measured on restaging MRI, and male sex. Each variable contributes to the score with a specific weight, as displayed in Table I. The obtained total score can range from 0 to 10 (20).

Statistical analysis. Based on the surgical difficulty grade (12), the sample was divided into two groups: the low and high surgical difficulty groups. Patient demographics, clinical characteristics, and operative and postoperative variables were evaluated by descriptive statistics and compared between groups by the chi-squared test, Fisher's exact test, and Mann-Whitney U-test. The validity and accuracy of the EuMaRCS score were assessed by calculating sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and the area under the receiver operating characteristics (ROC) curve (AROC). Sensitivity and specificity were considered low for values <60%, moderate for values between 60% and 79%, and high for values ≥80%. The accuracy determined by the AROC curve was interpreted as poor if the value was between 0.51 and 0.69; useful if the value was between 0.70 and 0.79; and good if the value was ≥0.80 (37-40). Sensitivity, specificity, and AROC were scrutinized to find the cut-off point that provides the best predictive value to identify patients at risk of difficult surgery. The product of sensitivity*specificity and a weighted Youden index were used to determine the best cut-off to predict a difficult surgery (41). Statistical analyses were performed using Statistical Package for Social Sciences software (Statistical Package for Social Science, IBM SPSS Statistics, Version 23 for Macintosh; IBM Corp., Armonk, NY, USA). p-Values <0.05 were considered to indicate statistical significance.

Figure 1.
Figure 1.

Characteristics of the study populations in which the EuMaRCS score was originally developed (training set) (20) and validated (validation set, present study). LARC: Locally advanced rectal cancer; L-TME: laparoscopic total mesorectal excision; MRI: magnetic resonance imaging; NCRT: neoadjuvant chemoradiation therapy.

Results

The study population (validation set) was comparable to the population in which the EuMaRCS score was originally developed (training set) (20) (Figure 1). The study population consisted of 141 LARC patients undergoing L-TME with primary anastomosis. Based on the surgical difficulty grade, 118 (83.7%) patients were classified as having low surgical difficulty, and 23 (16.3%) were classified as having high surgical difficulty. Demographic, clinical, and histopathological variables were similar between the groups. As expected, group differences were observed for operative and postoperative outcomes that contributed to defining surgical difficulty (Table II).

Compared to patients with low surgical difficulty, patients in the high surgical difficulty group had a significantly higher proportion of cancers staged as ymrT3 or more (69.6% vs. 28.8%; p=0.001) and a significantly smaller mean interspinous distance (99.23±13.63 mm vs. 103.01±13.06 mm; p=0.033). Differences concerning obesity (26.1% vs. 16.9%; p=0.376) and male sex (78.3% vs. 61.9%; p=0.158) were not significantly different between the high and low surgical difficulty groups.

EuMaRCS score validity. The accuracy of the EuMaRCS score is displayed by the ROC curve (Figure 2). The score was associated with good accuracy (AROC: 0.806). Once plotted the score values to determine the cut-off with the best balance between sensitivity and specificity and the higher weighted Youden score (Table III), a total score >3 appeared to best differentiate patients with low and high surgical difficulty. Using this cut-off value, the EuMaRCS score was associated with a sensitivity of 82.6%, a specificity of 66.1%, a PPV of 32.2% and an NPV of 95.1%.

View this table:
Table II.

Demographic, operative and histopathological variables of LARC patients undergoing L-TME after NCRT. The sample was divided into two groups based on the assessed surgical difficulty.

Figure 2.
Figure 2.

Receiver operating characteristics (ROC) curves of the EuMaRCS predictive score for surgical difficulty. The area under the curve, AROC, is 0.806 (95%CI=0.728-0.884; p<0.0001).

Discussion

The present study validated the EuMaRCS score in an independent population of LARC patients undergoing L-TME. This score is calculated preoperatively, and can help to predict the difficulty of L-TME with 82.6% sensitivity and 66.1% specificity, which indicate a good accuracy. However, when looking at the positive and negative predictive values, a LARC patient scoring 3 or less has a 95.1% chance of having a low difficult surgery (NPV), whereas a patient scoring >3 has a 32.3% chance of having a highly difficult surgery (PPV). It must be considered that the PPV is influenced by the sensitivity of the test and the prevalence of the outcome in the analyzed population. In this case, only 23/141 patients (16.3%) were classified as having highly difficult surgeries, thus limiting the observed PPV to approximately one-third of the population. Nevertheless, the EuMaRCS score performed similarly or even better than other predictive scores for postoperative complications widely used in rectal cancer patients, such as the Colorectal Physiological and Operative Severity Score for the Enumeration of Mortality and Morbidity (CR-POSSUM), the Onodera's Prognostic Nutritional Index (PNI), and the Estimation of Physiologic Ability and Surgical Stress Comprehensive Risk Score (E-PASS CRS) (42). Thus, taking these findings together and considering the AROC of 0.806, the present study suggests that the EuMaRCS score is a valuable tool to preoperatively identify LARC patients at risk of having a difficult L-TME.

View this table:
Table III.

Detailed report of sensitivity (Sn) and specificity (Sp) for the EuMaRCS predictive score for surgical difficulty.

In the era of personalized medicine, there is an urgent need to develop scores and algorithms to predict treatment outcomes and prognoses. In the context of rectal cancer surgery, several studies have investigated the role of pelvic dimensions in predicting surgical difficulty or poor-quality surgery. Most often, male sex was associated with an increased risk of conversion from laparoscopy to laparotomy (14, 27, 30, 43), and this risk was mainly related to the narrow pelvic space that can cause insufficient counter traction and lead to an unfeasible L-TME. A previous EuMaRCS study that analyzed pelvimetry on pretreatment MRI of LARC patients found that the interspinous distance and the intertuberous distance were significantly associated with the need for conversion and postoperative complications, respectively (11). More recently, Chau and coworkers have investigated the predictive value of pelvic dimension in identifying poor quality resection as defined by incomplete mesorectal excision and positive resection margins (10). The authors have shown that only the S1-S5-bottom of a symphysis angle >74/3° was an independent predictor of poor-quality resection after adjustment for BMI, tumor height and pathologic T stage. Their results, however, support the use of pretreatment MRI to identify patients at risk and guide surgical planning, in accordance with several other studies assessing the role of pelvimetry in rectal cancer patients (11, 13, 26, 27, 29-31, 44-47). Conversely, Curtis and coworkers have reported that patient, tumor, and bony pelvic anatomical characteristics seemed to not influence the surgical difficulty of L-TME except for the mesorectal area, which was associated with major intraoperative adverse events and postoperative morbidity (48). However, the studied population included 71 rectal cancer patients at different stages, as deemed by the fact that only 24% of the cases received NCRT; the heterogeneity of the tumor characteristics (e.g., tumor location, stage, and treatment protocols) may significantly impact the surgical difficulty and bias the observed associations between the bony structures assessed by pelvimetry and the surgical outcomes (11).

Instead of using a single clinical or pelvimetric parameter, a comprehensive score that combines anatomical, morphological and clinical factors that appear to affect the technical difficulty of L-TME may be more useful and precise to identify patients at risk (12, 20). The use of a predictive score has several advantages, as it is objective, easy to assess, and may represent an optimal tool to assist the decision-making process and facilitate communication between colleagues, as well as between surgeons and patients. However, the score must be valid, accurate and associated with good sensitivity and specificity to be widely accepted.

In 2018, Escal and coworkers (12) proposed an MRI morphometric score based on 4 equally weighted criteria, including BMI ≥30, intertuberous distance <10.1 cm, mesorectal fat area ≥20.7 cm2, and the need for a coloanal anastomosis to predict surgical difficulty as defined in the present study. The score proposed by Escal and coworkers is easy to assess, but it includes a variable, i.e., the need for coloanal or colorectal anastomosis, which is not always possible to determine preoperatively. Moreover, the diagnostic performance and accuracy of the score remain uncertain, although they were found to be poor when tested in an independent population (20).

The EuMaRCS score was found to have good accuracy in both the training set population (20) and the present validation set population, composed of homogeneous samples of LARC patients, all of which had received NCRT and L-TME. This demonstrated true replication in a similar but independent sample and supports the generalizability of the findings to the specific target population of patients with LARC (39, 49). Consistency was also shown because the outcome, i.e., surgical difficulty, was defined by applying the same surgical grading system, which included meaningful operative and postoperative parameters. While proving to be a valuable tool, the EuMaRCS score has the specificity to be, in our knowledge, the only score in the literature to consider a post-NCRT item such as the ymrT stage, which allows for the prediction of the impact of tumor characteristics on surgical difficulty, taking into account the tumor response to NCRT (11, 20). Growing evidence supports a strong relationship between the response to NCRT, restaging MRI findings and histopathological outcomes (e.g., depth of tumor invasion and involvement of CRM) (11, 34, 50-52). However, a restaging MRI is not yet systematically prescribed for all LARC patients, although an increased use in referral centers has been reported (53).

By using the EuMaRCS score, colorectal surgeons may be able to more easily and more precisely identify difficult cases that may deserve further evaluation, complementary treatments (e.g., prolonged NCRT), extended resections, alternative approaches (e.g., TaTME, robotic surgery) or surgical intervention performed by highly experienced surgeons rather than novice ones. Indeed, the assessment of risk and the identification of those factors that contribute most to the patient's risk can substantially assist in tailoring the surgical treatment. For instance, the presence of an ymrT3b or more should be considered to indicate a poor response to NCRT and a lower chance of achieving a complete mesorectal resection (25, 54, 55). The combination of male sex, narrow pelvis and BMI highlights the presence of anatomical factors that may particularly influence surgical difficulty during L-TME (26, 27, 30). Conversely, these parameters were recently found to have no influence on surgical quality outcomes if operating by TaTME (56), which may be seen as a valuable alternative in these cases.

The EuMaRCS score may also be useful for research applications. The score could be convenient in both retrospective and prospective studies to stratify patient populations by surgical difficulty risk and to compare the outcomes of different techniques or approaches, taking into account the predicted difficulty related to the patient and the rectal cancer characteristics. Moreover, future studies may evaluate the predictive role of the EuMaRCS score on oncological outcomes, such as recurrence rate and survival, which are strictly dependent on the possibility of achieving successful surgical resection.

In conclusion, the EuMaRCS score is a valid tool to identify patients susceptible to highly difficult L-TME, and it could be useful to choose the optimal treatment strategy for LARC.

Acknowledgements

The Authors would like to thank the entire EuMaRCS Study Group for their contributions: Filippo Landi, Giorgio Bianchi, Riccardo Memeo, Segundo A. Gómez-Abril, Teresa Torres, Tomás Ripollés, Romain Breguet, Michela Assalino, Giacomo Puppa, Silavain Terraz, David Armario, Victor Rodrigues, Marta Vera, Filippo Crimí, Ivan Gigantelli, Francesco Marchegiani, Laurene Aupin.

Footnotes

  • Authors' Contributions

    Study conception and design: Nicola de'Angelis, Aleix Martínez-Pérez, Alain Luciani, Francesco Brunetti, Eloy Espin, Frederic Ris, Salvatore Pucciarelli; Data collection: Giulio Cesare Vitali, Nicola de'Angelis, Aleix Martínez-Pérez, Giulio Cesare Vitali, Francesco Brunetti, Miquel Kraft, Eva Martí-Martínez, Paolo Moroni; Data analyses and interpretation: Nicola de'Angelis, Aleix Martínez-Pérez, Frederic Pigneur; Manuscript drafting: Nicola de'Angelis, Aleix Martínez-Pérez; Critical revisions and approval of the final version: Nicola de'Angelis, Aleix Martínez-Pérez, Giulio Cesare Vitali, Frederic Pigneur, Alain Luciani, Francesco Brunetti, Miquel Kraft, Eva Martí-Martínez, Paolo Moroni, Eloy Espin, Frederic Ris, Salvatore Pucciarelli.

  • Conflicts of Interest

    All Authors have no conflicts of interest to disclose regarding this study.

  • Received February 14, 2020.
  • Revision received February 24, 2020.
  • Accepted February 27, 2020.

References

  1. ↵
    1. Kusters M,
    2. Valentini V,
    3. Calvo FA,
    4. Krempien R,
    5. Nieuwenhuijzen GA,
    6. Martijn H,
    7. Doglietto GB,
    8. Del Valle E,
    9. Roeder F,
    10. Buchler MW,
    11. van de Velde CJ,
    12. Rutten HJ
    : Results of european pooled analysis of iort-containing multimodality treatment for locally advanced rectal cancer: Adjuvant chemotherapy prevents local recurrence rather than distant metastases. Ann Oncol 21(6): 1279-1284, 2010. PMID: 19889621. DOI: 10.1093/annonc/mdp501
    OpenUrlCrossRefPubMed
  2. ↵
    1. de'Angelis N,
    2. Landi F,
    3. Vitali GC,
    4. Memeo R,
    5. Martinez-Perez A,
    6. Solis A,
    7. Assalino M,
    8. Vallribera F,
    9. Mercoli HA,
    10. Marescaux J,
    11. Mutter D,
    12. Ris F,
    13. Espin E,
    14. Brunetti F
    : Multicentre propensity score-matched analysis of laparoscopic versus open surgery for t4 rectal cancer. Surg Endosc 31(8): 3106-3121, 2017. PMID: 27826780. DOI: 10.1007/s00464-016-5332-9
    OpenUrl
  3. ↵
    1. Nussbaum DP,
    2. Speicher PJ,
    3. Ganapathi AM,
    4. Englum BR,
    5. Keenan JE,
    6. Mantyh CR,
    7. Migaly J
    : Laparoscopic versus open low anterior resection for rectal cancer: Results from the national cancer data base. J Gastrointest Surg 19(1): 124-131; discussion 131-122, 2015. PMID: 4336173. DOI: 10.1007/s11605-014-2614-1
    OpenUrl
  4. ↵
    1. Garlipp B,
    2. Ptok H,
    3. Schmidt U,
    4. Stubs P,
    5. Scheidbach H,
    6. Meyer F,
    7. Gastinger I,
    8. Lippert H
    : Factors influencing the quality of total mesorectal excision. Br J Surg 99(5): 714-720, 2012. PMID: 22311576. DOI: 10.1002/bjs.8692
    OpenUrlPubMed
  5. ↵
    1. Heald RJ,
    2. Ryall RD
    : Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1(8496): 1479-1482, 1986. PMID: 2425199. DOI: 10.1016/s0140-6736(86)91510-2
    OpenUrlCrossRefPubMed
  6. ↵
    1. Jeong SY,
    2. Park JW,
    3. Nam BH,
    4. Kim S,
    5. Kang SB,
    6. Lim SB,
    7. Choi HS,
    8. Kim DW,
    9. Chang HJ,
    10. Kim DY,
    11. Jung KH,
    12. Kim TY,
    13. Kang GH,
    14. Chie EK,
    15. Kim SY,
    16. Sohn DK,
    17. Kim DH,
    18. Kim JS,
    19. Lee HS,
    20. Kim JH,
    21. Oh JH
    : Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (corean trial): Survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol 15(7): 767-774, 2014. PMID: 24837215. DOI: 10.1016/S1470-2045(14)70205-0
    OpenUrlCrossRefPubMed
    1. Bonjer HJ,
    2. Deijen CL,
    3. Abis GA,
    4. Cuesta MA,
    5. van der Pas MH,
    6. de Lange-de Klerk ES,
    7. Lacy AM,
    8. Bemelman WA,
    9. Andersson J,
    10. Angenete E,
    11. Rosenberg J,
    12. Fuerst A,
    13. Haglind E,
    14. Group CIS
    : A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med 372(14): 1324-1332, 2015. PMID: 25830422. DOI: 10.1056/NEJMoa1414882
    OpenUrlCrossRefPubMed
    1. Martinez-Perez A,
    2. Carra MC,
    3. Brunetti F,
    4. de'Angelis N
    : Pathologic outcomes of laparoscopic vs. open mesorectal excision for rectal cancer: A systematic review and meta-analysis. JAMA Surg 152(4): e165665, 2017. PMID: 28196217. DOI: 10.1001/jamasurg.2016.5665
    OpenUrlCrossRefPubMed
  9. ↵
    1. Martinez-Perez A,
    2. Carra MC,
    3. Brunetti F,
    4. de'Angelis N
    : Short-term clinical outcomes of laparoscopic vs open rectal excision for rectal cancer: A systematic review and meta-analysis. World J Gastroenterol 23(44): 7906-7916, 2017. PMID: 29209132. DOI: 10.3748/wjg.v23.i44.7906
    OpenUrl
  10. ↵
    1. Chau J,
    2. Solomon J,
    3. Liberman AS,
    4. Charlebois P,
    5. Stein B,
    6. Lee L
    : Pelvic dimensions on preoperative imaging can identify poor-quality resections after laparoscopic low anterior resection for mid- and low rectal cancer. Surg Endosc, 2019. PMID: 31620910. DOI: 10.1007/s00464-019-07209-8
  11. ↵
    1. de'Angelis N,
    2. Pigneur F,
    3. Martinez-Perez A,
    4. Vitali GC,
    5. Landi F,
    6. Torres-Sanchez T,
    7. Rodrigues V,
    8. Memeo R,
    9. Bianchi G,
    10. Brunetti F,
    11. Espin E,
    12. Ris F,
    13. Luciani A,
    14. EuMa RCSSG
    : Predictors of surgical outcomes and survival in rectal cancer patients undergoing laparoscopic total mesorectal excision after neoadjuvant chemoradiation therapy: The interest of pelvimetry and restaging magnetic resonance imaging studies. Oncotarget 9(38): 25315-25331, 2018. PMID: 29861874. DOI: 10.18632/oncotarget.25431
    OpenUrl
  12. ↵
    1. Escal L,
    2. Nougaret S,
    3. Guiu B,
    4. Bertrand MM,
    5. de Forges H,
    6. Tetreau R,
    7. Thezenas S,
    8. Rouanet P
    : Mri-based score to predict surgical difficulty in patients with rectal cancer. Br J Surg 105(1): 140-146, 2018. PMID: 29088504. DOI: 10.1002/bjs.10642
    OpenUrl
  13. ↵
    1. Akiyoshi T,
    2. Kuroyanagi H,
    3. Oya M,
    4. Konishi T,
    5. Fukuda M,
    6. Fujimoto Y,
    7. Ueno M,
    8. Miyata S,
    9. Yamaguchi T
    : Factors affecting the difficulty of laparoscopic total mesorectal excision with double stapling technique anastomosis for low rectal cancer. Surgery 146(3): 483-489, 2009. PMID: 19715805. DOI: 10.1016/j.surg.2009.03.030
    OpenUrlCrossRefPubMed
  14. ↵
    1. Boyle KM,
    2. Petty D,
    3. Chalmers AG,
    4. Quirke P,
    5. Cairns A,
    6. Finan PJ,
    7. Sagar PM,
    8. Burke D
    : Mri assessment of the bony pelvis may help predict resectability of rectal cancer. Colorectal Dis 7(3): 232-240, 2005. PMID: 15859960. DOI: 10.1111/j.1463-1318.2005.00819.x
    OpenUrlCrossRefPubMed
  15. ↵
    1. Targarona EM,
    2. Balague C,
    3. Pernas JC,
    4. Martinez C,
    5. Berindoague R,
    6. Gich I,
    7. Trias M
    : Can we predict immediate outcome after laparoscopic rectal surgery? Multivariate analysis of clinical, anatomic, and pathologic features after 3-dimensional reconstruction of the pelvic anatomy. Ann Surg 247(4): 642-649, 2008. PMID: 18362627. DOI: 10.1097/SLA.0b013e3181612c6a
    OpenUrlCrossRefPubMed
  16. ↵
    1. Kitz J,
    2. Fokas E,
    3. Beissbarth T,
    4. Strobel P,
    5. Wittekind C,
    6. Hartmann A,
    7. Ruschoff J,
    8. Papadopoulos T,
    9. Rosler E,
    10. Ortloff-Kittredge P,
    11. Kania U,
    12. Schlitt H,
    13. Link KH,
    14. Bechstein W,
    15. Raab HR,
    16. Staib L,
    17. Germer CT,
    18. Liersch T,
    19. Sauer R,
    20. Rodel C,
    21. Ghadimi M,
    22. Hohenberger W,
    23. German Rectal Cancer Study G
    : Association of plane of total mesorectal excision with prognosis of rectal cancer: Secondary analysis of the cao/aro/aio-04 phase 3 randomized clinical trial. JAMA Surg 153(8): e181607, 2018. PMID: 29874375. DOI: 10.1001/jamasurg.2018.1607
    OpenUrl
    1. Kusters M,
    2. Marijnen CA,
    3. van de Velde CJ,
    4. Rutten HJ,
    5. Lahaye MJ,
    6. Kim JH,
    7. Beets-Tan RG,
    8. Beets GL
    : Patterns of local recurrence in rectal cancer; a study of the dutch tme trial. Eur J Surg Oncol 36(5): 470-476, 2010. PMID: 20096534. DOI: 10.1016/j.ejso.2009.11.011
    OpenUrlCrossRefPubMed
    1. van Gijn W,
    2. Marijnen CA,
    3. Nagtegaal ID,
    4. Kranenbarg EM,
    5. Putter H,
    6. Wiggers T,
    7. Rutten HJ,
    8. Pahlman L,
    9. Glimelius B,
    10. van de Velde CJ,
    11. Dutch Colorectal Cancer G
    : Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer: 12-year follow-up of the multicentre, randomised controlled TME trial. Lancet Oncol 12(6): 575-582, 2011. PMID: 21596621. DOI: 10.1016/S1470-2045(11)70097-3
    OpenUrlCrossRefPubMed
  19. ↵
    1. Quirke P,
    2. Durdey P,
    3. Dixon MF,
    4. Williams NS
    : Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 2(8514): 996-999, 1986. PMID: 2430152.
    OpenUrlCrossRefPubMed
  20. ↵
    1. de'Angelis N,
    2. Pigneur F,
    3. Martinez-Perez A,
    4. Vitali GC,
    5. Landi F,
    6. Gomez-Abril SA,
    7. Assalino M,
    8. Espin E,
    9. Ris F,
    10. Luciani A,
    11. Brunetti F,
    12. EuMa RCSSG
    : Assessing surgical difficulty in locally advanced mid-low rectal cancer: The accuracy of two mri-based predictive scores. Colorectal Dis 21(3): 277-286, 2019. PMID: 30428156. DOI: 10.1111/codi.14473
    OpenUrl
  21. ↵
    1. Petrucciani N,
    2. Carra MC,
    3. Martinez-Perez A,
    4. Vitali GC,
    5. Landi F,
    6. Genova P,
    7. Memeo R,
    8. Brunetti F,
    9. Espin E,
    10. Ris F,
    11. De'angelis N,
    12. Group ES
    : Comparison of different nodal staging in patients with locally advanced mid-low rectal cancer after long-term neoadjuvant chemoradiation therapy. Anticancer Res 39(4): 2113-2120, 2019. PMID: 30952757. DOI: 10.21873/anticanres.13324
    OpenUrlAbstract/FREE Full Text
  22. ↵
    1. Edge SB,
    2. Compton CC
    : The american joint committee on cancer: The 7th edition of the ajcc cancer staging manual and the future of tnm. Ann Surg Oncol 17(6): 1471-1474, 2010. PMID: 20180029. DOI: 10.1245/s10434-010-0985-4
    OpenUrlCrossRefPubMed
  23. ↵
    1. Landi F,
    2. Espin E,
    3. Rodrigues V,
    4. Vallribera F,
    5. Martinez A,
    6. Charpy C,
    7. Brunetti F,
    8. Azoulay D,
    9. de'Angelis N
    : Pathologic response grade after long-course neoadjuvant chemoradiation does not influence morbidity in locally advanced mid-low rectal cancer resected by laparoscopy. Int J Colorectal Dis 32(2): 255-264, 2017. PMID: 27757541. DOI: 10.1007/s00384-016-2685-4
    OpenUrl
  24. ↵
    1. Law WL,
    2. Chu KW
    : Anterior resection for rectal cancer with mesorectal excision: A prospective evaluation of 622 patients. Ann Surg 240(2): 260-268, 2004. PMID: 15273550.
    OpenUrlCrossRefPubMed
  25. ↵
    1. Lambregts DM,
    2. Rao SX,
    3. Sassen S,
    4. Martens MH,
    5. Heijnen LA,
    6. Buijsen J,
    7. Sosef M,
    8. Beets GL,
    9. Vliegen RA,
    10. Beets-Tan RG
    : Mri and diffusion-weighted mri volumetry for identification of complete tumor responders after preoperative chemoradiotherapy in patients with rectal cancer: A bi-institutional validation study. Ann Surg 262(6): 1034-1039, 2015. PMID: 25211270. DOI: 10.1097/SLA.0000000000000909
    OpenUrl
  26. ↵
    1. Salerno G,
    2. Daniels IR,
    3. Brown G,
    4. Heald RJ,
    5. Moran BJ
    : Magnetic resonance imaging pelvimetry in 186 patients with rectal cancer confirms an overlap in pelvic size between males and females. Colorectal Dis 8(9): 772-776, 2006. PMID: 17032323. DOI: 10.1111/j.1463-1318.2006.01090.x
    OpenUrlCrossRefPubMed
  27. ↵
    1. Salerno G,
    2. Daniels IR,
    3. Brown G,
    4. Norman AR,
    5. Moran BJ,
    6. Heald RJ
    : Variations in pelvic dimensions do not predict the risk of circumferential resection margin (crm) involvement in rectal cancer. World J Surg 31(6): 1313-1320, 2007. PMID: 17468974. DOI: 10.1007/s00268-007-9007-5
    OpenUrlPubMed
    1. Killeen T,
    2. Banerjee S,
    3. Vijay V,
    4. Al-Dabbagh Z,
    5. Francis D,
    6. Warren S
    : Magnetic resonance (mr) pelvimetry as a predictor of difficulty in laparoscopic operations for rectal cancer. Surg Endosc 24(12): 2974-2979, 2010. PMID: 20464426. DOI: 10.1007/s00464-010-1075-1
    OpenUrlPubMed
  29. ↵
    1. Baek SJ,
    2. Kim CH,
    3. Cho MS,
    4. Bae SU,
    5. Hur H,
    6. Min BS,
    7. Baik SH,
    8. Lee KY,
    9. Kim NK
    : Robotic surgery for rectal cancer can overcome difficulties associated with pelvic anatomy. Surg Endosc 29(6): 1419-1424, 2015. PMID: 25159651. DOI: 10.1007/s00464-014-3818-x
    OpenUrl
  30. ↵
    1. Ferko A,
    2. Maly O,
    3. Orhalmi J,
    4. Dolejs J
    : Ct/mri pelvimetry as a useful tool when selecting patients with rectal cancer for transanal total mesorectal excision. Surg Endosc 30(3): 1164-1171, 2016. PMID: 26123334. DOI: 10.1007/s00464-015-4324-5
    OpenUrl
  31. ↵
    1. Ogiso S,
    2. Yamaguchi T,
    3. Hata H,
    4. Fukuda M,
    5. Ikai I,
    6. Yamato T,
    7. Sakai Y
    : Evaluation of factors affecting the difficulty of laparoscopic anterior resection for rectal cancer: “Narrow pelvis” is not a contraindication. Surg Endosc 25(6): 1907-1912, 2011. PMID: 21136101. DOI: 10.1007/s00464-010-1485-0
    OpenUrlCrossRefPubMed
  32. ↵
    1. Shihab OC,
    2. Taylor F,
    3. Salerno G,
    4. Heald RJ,
    5. Quirke P,
    6. Moran BJ,
    7. Brown G
    : Mri predictive factors for long-term outcomes of low rectal tumours. Ann Surg Oncol 18(12): 3278-3284, 2011. PMID: 21590453. DOI: 10.1245/s10434-011-1776-2
    OpenUrlCrossRefPubMed
  33. ↵
    1. Vecchio FM,
    2. Valentini V,
    3. Minsky BD,
    4. Padula GD,
    5. Venkatraman ES,
    6. Balducci M,
    7. Micciche F,
    8. Ricci R,
    9. Morganti AG,
    10. Gambacorta MA,
    11. Maurizi F,
    12. Coco C
    : The relationship of pathologic tumor regression grade (trg) and outcomes after preoperative therapy in rectal cancer. Int J Radiat Oncol Biol Phys 62(3): 752-760, 2005. PMID: 15936556. DOI: 10.1016/j.ijrobp.2004.11.017
    OpenUrlCrossRefPubMed
  34. ↵
    1. Bhoday J,
    2. Smith F,
    3. Siddiqui MR,
    4. Balyasnikova S,
    5. Swift RI,
    6. Perez R,
    7. Habr-Gama A,
    8. Brown G
    : Magnetic resonance tumor regression grade and residual mucosal abnormality as predictors for pathological complete response in rectal cancer postneoadjuvant chemoradiotherapy. Dis Colon Rectum 59(10): 925-933, 2016. PMID: 27602923. DOI: 10.1097/DCR.0000000000000667
    OpenUrl
  35. ↵
    1. Kapiteijn E,
    2. Marijnen CA,
    3. Nagtegaal ID,
    4. Putter H,
    5. Steup WH,
    6. Wiggers T,
    7. Rutten HJ,
    8. Pahlman L,
    9. Glimelius B,
    10. van Krieken JH,
    11. Leer JW,
    12. van de Velde CJ,
    13. Dutch Colorectal Cancer G
    : Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 345(9): 638-646, 2001. PMID: 11547717. DOI: 10.1056/NEJMoa010580
    OpenUrlCrossRefPubMed
  36. ↵
    1. Dindo D,
    2. Demartines N,
    3. Clavien PA
    : Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2): 205-213, 2004. PMID: 15273542.
    OpenUrlCrossRefPubMed
  37. ↵
    1. Simundic AM
    : Measures of diagnostic accuracy: Basic definitions. EJIFCC 19(4): 203-211, 2009. PMID: 27683318.
    OpenUrlPubMed
    1. Nelson DE,
    2. Holtzman D,
    3. Bolen J,
    4. Stanwyck CA,
    5. Mack KA
    : Reliability and validity of measures from the behavioral risk factor surveillance system (brfss). Soz Praventivmed 46: S3-42, 2001. PMID: 11851091.
    OpenUrlCrossRefPubMed
  39. ↵
    1. Lee YH,
    2. Bang H,
    3. Kim DJ
    : How to establish clinical prediction models. Endocrinol Metab (Seoul) 31(1): 38-44, 2016. PMID: 26996421. DOI: 10.3803/EnM.2016.31.1.38
    OpenUrl
  40. ↵
    1. Carra MC,
    2. Gueguen A,
    3. Thomas F,
    4. Pannier B,
    5. Caligiuri G,
    6. Steg PG,
    7. Zins M,
    8. Bouchard P
    : Self-report assessment of severe periodontitis: Periodontal screening score development. J Clin Periodontol 45(7): 818-831, 2018. PMID: 29611224. DOI: 10.1111/jcpe.12899
    OpenUrl
  41. ↵
    1. Habibzadeh F,
    2. Habibzadeh P,
    3. Yadollahie M
    : On determining the most appropriate test cut-off value: The case of tests with continuous results. Biochem Med (Zagreb) 26(3): 297-307, 2016. PMID: 27812299. DOI: 10.11613/BM.2016.034
    OpenUrlCrossRef
  42. ↵
    1. Miyakita H,
    2. Sadahiro S,
    3. Saito G,
    4. Okada K,
    5. Tanaka A,
    6. Suzuki T
    : Risk scores as useful predictors of perioperative complications in patients with rectal cancer who received radical surgery. Int J Clin Oncol 22(2): 324-331, 2017. PMID: 27783239. DOI: 10.1007/s10147-016-1054-1
    OpenUrl
  43. ↵
    1. Veenhof AA,
    2. Engel AF,
    3. van der Peet DL,
    4. Sietses C,
    5. Meijerink WJ,
    6. de Lange-de Klerk ES,
    7. Cuesta MA
    : Technical difficulty grade score for the laparoscopic approach of rectal cancer: A single institution pilot study. Int J Colorectal Dis 23(5): 469-475, 2008. PMID: 18185936. DOI: 10.1007/s00384-007-0433-5
    OpenUrlPubMed
  44. ↵
    1. Li Q,
    2. Li D,
    3. Jiang L,
    4. Qiu P,
    5. Fu Z,
    6. Tang L,
    7. Chen W
    : Factors influencing difficulty of laparoscopic abdominoperineal resection for ultra-low rectal cancer. Surg Laparosc Endosc Percutan Tech 27(2): 104-109, 2017. PMID: 28212258. DOI: 10.1097/SLE.0000000000000378
    OpenUrl
    1. Boyle KM,
    2. Chalmers AG,
    3. Finan PJ,
    4. Sagar PM,
    5. Burke D
    : Morphology of the mesorectum in patients with primary rectal cancer. Dis Colon Rectum 52(6): 1122-1129, 2009. PMID: 19581856. DOI: 10.1007/DCR.0b013e31819ef62f
    OpenUrlPubMed
    1. Akasu T,
    2. Iinuma G,
    3. Fujita T,
    4. Muramatsu Y,
    5. Tateishi U,
    6. Miyakawa K,
    7. Murakami T,
    8. Moriyama N
    : Thin-section mri with a phased-array coil for preoperative evaluation of pelvic anatomy and tumor extent in patients with rectal cancer. AJR Am J Roentgenol 184(2): 531-538, 2005. PMID: 15671375. DOI: 10.2214/ajr.184.2.01840531
    OpenUrlPubMed
  47. ↵
    1. Zhou XC,
    2. Su M,
    3. Hu KQ,
    4. Su YF,
    5. Ye YH,
    6. Huang CQ,
    7. Yu ZL,
    8. Li XY,
    9. Zhou H,
    10. Ni YZ,
    11. Jiang YI,
    12. Lou Z
    : Ct pelvimetry and clinicopathological parameters in evaluation of the technical difficulties in performing open rectal surgery for mid-low rectal cancer. Oncol Lett 11(1): 31-38, 2016. PMID: 26870163. DOI: 10.3892/ol.2015.3827
    OpenUrl
  48. ↵
    1. Curtis NJ,
    2. Thomas C,
    3. Dennison G,
    4. Ockrim JB,
    5. Conti JA,
    6. Dalton R,
    7. Allison AS,
    8. Francis NK
    : Factors predicting operative difficulty of laparoscopic total mesorectal excision. Dis Colon Rectum 62(12): 1467-1476, 2019. PMID: 31567928. DOI: 10.1097/DCR.0000000000001490
    OpenUrl
  49. ↵
    1. Lee YH,
    2. Bang H,
    3. Park YM,
    4. Bae JC,
    5. Lee BW,
    6. Kang ES,
    7. Cha BS,
    8. Lee HC,
    9. Balkau B,
    10. Lee WY,
    11. Kim DJ
    : Non-laboratory-based self-assessment screening score for non-alcoholic fatty liver disease: Development, validation and comparison with other scores. PLoS One 9(9): e107584, 2014. PMID: 25216184. DOI: 10.1371/journal.pone.0107584
    OpenUrl
  50. ↵
    1. Lambregts DM,
    2. Vandecaveye V,
    3. Barbaro B,
    4. Bakers FC,
    5. Lambrecht M,
    6. Maas M,
    7. Haustermans K,
    8. Valentini V,
    9. Beets GL,
    10. Beets-Tan RG
    : Diffusion-weighted mri for selection of complete responders after chemoradiation for locally advanced rectal cancer: A multicenter study. Ann Surg Oncol 18(8): 2224-2231, 2011. PMID: 21347783. DOI: 10.1245/s10434-011-1607-5
    OpenUrlCrossRefPubMed
    1. Patel UB,
    2. Brown G,
    3. Rutten H,
    4. West N,
    5. Sebag-Montefiore D,
    6. Glynne-Jones R,
    7. Rullier E,
    8. Peeters M,
    9. Van Cutsem E,
    10. Ricci S,
    11. Van de Velde C,
    12. Kjell P,
    13. Quirke P
    : Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 19(9): 2842-2852, 2012. PMID: 22526897. DOI: 10.1245/s10434-012-2309-3
    OpenUrlCrossRefPubMed
  52. ↵
    1. Quah HM,
    2. Chou JF,
    3. Gonen M,
    4. Shia J,
    5. Schrag D,
    6. Saltz LB,
    7. Goodman KA,
    8. Minsky BD,
    9. Wong WD,
    10. Weiser MR
    : Pathologic stage is most prognostic of disease-free survival in locally advanced rectal cancer patients after preoperative chemoradiation. Cancer 113(1): 57-64, 2008. PMID: 18442099. DOI: 10.1002/cncr.23516
    OpenUrlCrossRefPubMed
  53. ↵
    1. Beets-Tan RGH,
    2. Lambregts DMJ,
    3. Maas M,
    4. Bipat S,
    5. Barbaro B,
    6. Curvo-Semedo L,
    7. Fenlon HM,
    8. Gollub MJ,
    9. Gourtsoyianni S,
    10. Halligan S,
    11. Hoeffel C,
    12. Kim SH,
    13. Laghi A,
    14. Maier A,
    15. Rafaelsen SR,
    16. Stoker J,
    17. Taylor SA,
    18. Torkzad MR,
    19. Blomqvist L
    : Correction to: Magnetic resonance imaging for clinical management of rectal cancer: Updated recommendations from the 2016 european society of gastrointestinal and abdominal radiology (ESGAR) consensus meeting. Eur Radiol 28(6): 2711, 2018. PMID: 29322331. DOI: 10.1007/s00330-017-5204-2
    OpenUrl
  54. ↵
    1. Battersby NJ,
    2. How P,
    3. Moran B,
    4. Stelzner S,
    5. West NP,
    6. Branagan G,
    7. Strassburg J,
    8. Quirke P,
    9. Tekkis P,
    10. Pedersen BG,
    11. Gudgeon M,
    12. Heald B,
    13. Brown G,
    14. Group MIS
    : Prospective validation of a low rectal cancer magnetic resonance imaging staging system and development of a local recurrence risk stratification model: The MERCURY II study. Ann Surg 263(4): 751-760, 2016. PMID: 25822672. DOI: 10.1097/SLA.0000000000001193
    OpenUrl
  55. ↵
    1. Chand M,
    2. Swift RI,
    3. Tekkis PP,
    4. Chau I,
    5. Brown G
    : Extramural venous invasion is a potential imaging predictive biomarker of neoadjuvant treatment in rectal cancer. Br J Cancer 110(1): 19-25, 2014. PMID: 24300971. DOI: 10.1038/bjc.2013.603
    OpenUrlCrossRefPubMed
  56. ↵
    1. Roodbeen SX,
    2. de Lacy FB,
    3. van Dieren S,
    4. Penna M,
    5. Ris F,
    6. Moran B,
    7. Tekkis P,
    8. Bemelman WA,
    9. Hompes R,
    10. International Ta TMERC
    : Predictive factors and risk model for positive circumferential resection margin rate after transanal total mesorectal excision in 2653 patients with rectal cancer. Ann Surg 270(5): 884-891, 2019. PMID: 31634183. DOI: 10.1097/SLA.0000000000003516
    OpenUrl
Back to top

In this issue

Print
Download PDF
Article Alerts
Email Article
Citation Tools
Reprints and Permissions
Predicting Difficult Laparoscopic Total Mesorectal Excision for Locally-advanced Mid-low Rectal Cancer: The EuMaRCS Score Validation
NICOLA de'ANGELIS, ALEIX MARTÍNEZ-PÉREZ, GIULIO CESARE VITALI, FREDERIC PIGNEUR, ALAIN LUCIANI, FRANCESCO BRUNETTI, MIQUEL KRAFT, EVA MARTÍ-MARTÍNEZ, PAOLO MORONI, ELOY ESPIN, FREDERIC RIS, SALVATORE PUCCIARELLI, On behalf of the EuMaRCS Study Group
Anticancer Research Apr 2020, 40 (4) 2079-2087; DOI: 10.21873/anticanres.14166
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo

Jump to section

Keywords